Hostname: page-component-8448b6f56d-gtxcr Total loading time: 0 Render date: 2024-04-19T20:46:31.501Z Has data issue: false hasContentIssue false
  • English
  • Français

The molecular choreography of protein synthesis: translational control, regulation, and pathways

Published online by Cambridge University Press:  24 June 2016

Jin Chen ,
Junhong Choi ,
Seán E. O'Leary ,
Arjun Prabhakar ,
Alexey Petrov ,
Rosslyn Grosely ,
Elisabetta Viani Puglisi  and
Joseph D. Puglisi
Jin Chen
Affiliation:
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305-5126, USA Department of Applied Physics, Stanford University, Stanford, CA 94305-4090, USA
Junhong Choi
Affiliation:
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305-5126, USA Department of Applied Physics, Stanford University, Stanford, CA 94305-4090, USA
Seán E. O'Leary
Affiliation:
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305-5126, USA
Arjun Prabhakar
Affiliation:
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305-5126, USA Program in Biophysics, Stanford University, Stanford, CA 94305, USA
Alexey Petrov
Affiliation:
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305-5126, USA
Rosslyn Grosely
Affiliation:
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305-5126, USA
Elisabetta Viani Puglisi
Affiliation:
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305-5126, USA
Joseph D. Puglisi*
Affiliation:
Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305-5126, USA
*
*Author for correspondence: Joseph D. Puglisi, Department of Structural Biology, Stanford University School of Medicine, Stanford, CA 94305-5126, USA. Tel.: 650-723-9151; Email: puglisi@stanford.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Translation of proteins by the ribosome regulates gene expression, with recent results underscoring the importance of translational control. Misregulation of translation underlies many diseases, including cancer and many genetic diseases. Decades of biochemical and structural studies have delineated many of the mechanistic details in prokaryotic translation, and sketched the outlines of eukaryotic translation. However, translation may not proceed linearly through a single mechanistic pathway, but likely involves multiple pathways and branchpoints. The stochastic nature of biological processes would allow different pathways to occur during translation that are biased by the interaction of the ribosome with other translation factors, with many of the steps kinetically controlled. These multiple pathways and branchpoints are potential regulatory nexus, allowing gene expression to be tuned at the translational level. As research focus shifts toward eukaryotic translation, certain themes will be echoed from studies on prokaryotic translation. This review provides a general overview of the dynamic data related to prokaryotic and eukaryotic translation, in particular recent findings with single-molecule methods, complemented by biochemical, kinetic, and structural findings. We will underscore the importance of viewing the process through the viewpoints of regulation, translational control, and heterogeneous pathways.

Type
Review
Information
Quarterly Reviews of Biophysics , Volume 49 , 2016 , e11
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abaeva, I. S., Marintchev, A., Pisareva, V. P., Hellen, C. U. & Pestova, T. V. (2011). Bypassing of stems versus linear base-by-base inspection of mammalian mRNAs during ribosomal scanning. The EMBO Journal 30, 115–129.Google Scholar
Abramson, R. D., Dever, T. E., Lawson, T. G., Ray, B. K., Thach, R. E. & Merrick, W. C. (1987). The ATP-dependent interaction of eukaryotic initiation factors with mRNA. The Journal of Biological Chemistry 262, 3826–3832.Google Scholar
Acker, M. G., Kolitz, S. E., Mitchell, S. F., Nanda, J. S. & Lorsch, J. R. (2007). Reconstitution of yeast translation initiation. Methods in Enzymology 430, 111–145.CrossRefGoogle ScholarPubMed
Acker, M. G., Shin, B. S., Nanda, J. S., Saini, A. K., Dever, T. E. & Lorsch, J. R. (2009). Kinetic analysis of late steps of eukaryotic translation initiation. Journal of Molecular Biology 385, 491–506.Google Scholar
Adams, J. M. & Cory, S. (1975). Modified nucleosides and bizarre 5′-termini in mouse myeloma mRNA. Nature 255, 28–33.CrossRefGoogle Scholar
Afonina, Z. A., Myasnikov, A. G., Shirokov, V. A., Klaholz, B. P. & Spirin, A. S. (2014). Formation of circular polyribosomes on eukaryotic mRNA without cap-structure and poly(A)-tail: a cryo electron tomography study. Nucleic Acids Research 42, 9461–9469.CrossRefGoogle ScholarPubMed
Agirrezabala, X. & Frank, J. (2009). Elongation in translation as a dynamic interaction among the ribosome, tRNA, and elongation factors EF-G and EF-Tu. Quarterly Reviews of Biophysics 42, 159–200.Google Scholar
Agirrezabala, X., Lei, J., Brunelle, J. L., Ortiz-Meoz, R. F., Green, R. & Frank, J. (2008). Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Molecular Cell 32, 190–197.Google Scholar
Aitken, C. E. & Lorsch, J. R. (2012). A mechanistic overview of translation initiation in eukaryotes. Nature Structural & Molecular Biology 19, 568–576.Google Scholar
Aitken, C. E. & Puglisi, J. D. (2010). Following the intersubunit conformation of the ribosome during translation in real time. Nature Structural & Molecular Biology 17, 793–800.Google Scholar
Akabayov, S. R., Akabayov, B., Richardson, C. C. & Wagner, G. (2013). Molecular crowding enhanced ATPase activity of the RNA helicase eIF4A correlates with compaction of its quaternary structure and association with eIF4G. Journal of the American Chemical Society 135, 10040–10047.Google Scholar
Alekhina, O. M. & Vassilenko, K. S. (2012). Translation initiation in eukaryotes: versatility of the scanning model. Biochemistry (Mosc) 77, 1465–1477.Google Scholar
Algire, M. A., Maag, D. & Lorsch, J. R. (2005). Pi release from eIF2, not GTP hydrolysis, is the step controlled by start-site selection during eukaryotic translation initiation. Molecular Cell 20, 251–262.Google Scholar
Algire, M. A., Maag, D., Savio, P., Acker, M. G., Tarun, S. Z., Sachs, A. B., Asano, K., Nielsen, K. H., Olsen, D. S., Phan, L., Hinnebusch, A. G. & Lorsch, J. R. (2002). Development and characterization of a reconstituted yeast translation initiation system. RNA 8, 382–397.Google Scholar
Alkalaeva, E. Z., Pisarev, A. V., Frolova, L. Y., Kisselev, L. L. & Pestova, T. V. (2006). In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell 125, 1125–1136.Google Scholar
Altmann, M., Edery, I., Sonenberg, N. & Trachsel, H. (1985). Purification and characterization of protein synthesis initiation factor eIF-4E from the yeast Saccharomyces cerevisiae . Biochemistry 24, 6085–6089.Google Scholar
Altmann, M., Handschin, C. & Trachsel, H. (1987). mRNA cap-binding protein: cloning of the gene encoding protein synthesis initiation factor eIF-4E from Saccharomyces cerevisiae . Molecular and Cellular Biology 7, 998–1003.Google Scholar
Altmann, M., Müller, P. P., Pelletier, J., Sonenberg, N. & Trachsel, H. (1989). A mammalian translation initiation factor can substitute for its yeast homologue in vivo . The Journal of Biological Chemistry 264, 12145–12147.Google Scholar
Altmann, M., Wittmer, B., Methot, N., Sonenberg, N. & Trachsel, H. (1995). The Saccharomyces cerevisiae translation initiation factor Tif3 and its mammalian homologue, eIF-4B, have RNA annealing activity. The EMBO Journal 14, 3820–3827.Google Scholar
Amrani, N., Ghosh, S., Mangus, D. A. & Jacobson, A. (2008). Translation factors promote the formation of two states of the closed-loop mRNP. Nature 453, 1276–1280.Google Scholar
Anand, M., Balar, B., Ulloque, R., Gross, S. R. & Kinzy, T. G. (2006). Domain and nucleotide dependence of the interaction between Saccharomyces cerevisiae translation elongation factors 3 and 1A. The Journal of Biological Chemistry 281, 32318–32326.Google Scholar
Anand, M., Chakraburtty, K., Marton, M. J., Hinnebusch, A. G. & Kinzy, T. G. (2003). Functional interactions between yeast translation eukaryotic elongation factor (eEF) 1A and eEF3. The Journal of Biological Chemistry 278, 6985–6991.Google Scholar
Andersen, C. B., Becker, T., Blau, M., Anand, M., Halic, M., Balar, B., Mielke, T., Boesen, T., Pedersen, J. S., Spahn, C. M., Kinzy, T. G., Andersen, G. R. & Beckmann, R. (2006). Structure of eEF3 and the mechanism of transfer RNA release from the E-site. Nature 443, 663–668.Google Scholar
Andreou, A. Z. & Klostermeier, D. (2013). The DEAD-box helicase eIF4A: paradigm or the odd one out? RNA Biology 10, 19–32.Google Scholar
Andreou, A. Z. & Klostermeier, D. (2014). eIF4B and eIF4 G jointly stimulate eIF4A ATPase and unwinding activities by modulation of the eIF4A conformational cycle. Journal of Molecular Biology 426, 51–61.Google Scholar
Antoun, A., Pavlov, M. Y., Andersson, K., Tenson, T. & Ehrenberg, M. (2003). The roles of initiation factor 2 and guanosine triphosphate in initiation of protein synthesis. The EMBO Journal 22, 5593–5601.CrossRefGoogle ScholarPubMed
Aspden, J. L. & Jackson, R. J. (2010). Differential effects of nucleotide analogs on scanning-dependent initiation and elongation of mammalian mRNA translation in vitro . RNA 16, 1130–1137.Google Scholar
Bai, X. C., Fernandez, I. S., Mcmullan, G. & Scheres, S. H. (2013). Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. eLife 2, e00461.Google Scholar
Bauer, J. W., Brandl, C., Haubenreisser, O., Wimmer, B., Weber, M., Karl, T., Klausegger, A., Breitenbach, M., Hintner, H., Von Der Haar, T., Tuite, M. F. & Breitenbach-Koller, L. (2013). Specialized yeast ribosomes: a customized tool for selective mRNA translation. PLoS ONE 8, e67609.Google Scholar
Bellsolell, L., Cho-Park, P. F., Poulin, F., Sonenberg, N. & Burley, S. K. (2006). Two structurally atypical HEAT domains in the C-terminal portion of human eIF4G support binding to eIF4A and Mnk1. Structure 14, 913–923.Google Scholar
Benne, R. & Hershey, J. W. (1978). The mechanism of action of protein synthesis initiation factors from rabbit reticulocytes. The Journal of Biological Chemistry 253, 3078–3087.Google Scholar
Berset, C., Zurbriggen, A., Djafarzadeh, S., Altmann, M. & Trachsel, H. (2003). RNA-binding activity of translation initiation factor eIF4G1 from Saccharomyces cerevisiae . RNA 9, 871–880.Google Scholar
Berthelot, K., Muldoon, M., Rajkowitsch, L., Hughes, J. & Mccarthy, J. E. (2004). Dynamics and processivity of 40S ribosome scanning on mRNA in yeast. Molecular Microbiology 51, 987–1001.Google Scholar
Beznoskova, P., Cuchalova, L., Wagner, S., Shoemaker, C. J., Gunisova, S., von der Haar, T. & Valasek, L. S. (2013). Translation initiation factors eIF3 and HCR1 control translation termination and stop codon read-through in yeast cells. PLoS Genetics 9, e1003962.Google Scholar
Blaha, G., Stanley, R. E. & Steitz, T. A. (2009). Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science 325, 966–970.Google Scholar
Blanchard, S. C., Gonzalez, R. L., Kim, H. D., Chu, S. & Puglisi, J. D. (2004a). tRNA selection and kinetic proofreading in translation. Nature Structural & Molecular Biology 11, 1008–1014.Google Scholar
Blanchard, S. C., Kim, H. D., Gonzalez, R. L. Jr., Puglisi, J. D. & Chu, S. (2004b). tRNA dynamics on the ribosome during translation. Proceedings of the National Academy of Sciences of the United States of America 101, 12893–12898.Google Scholar
Blum, S., Mueller, M., Schmid, S. R., Linder, P. & Trachsel, H. (1989). Translation in Saccharomyces cerevisiae: initiation factor 4A-dependent cell-free system. Proceedings of the National Academy of Sciences of the United States of America 86, 6043–6046.Google Scholar
Bock, L. V., Blau, C., Schroder, G. F., Davydov, I. I., Fischer, N., Stark, H., Rodnina, M. V., Vaiana, A. C. & Grubmuller, H. (2013). Energy barriers and driving forces in tRNA translocation through the ribosome. Nature Structural & Molecular Biology 20, 1390–1396.Google Scholar
Bonven, B. & Gullov, K. (1979). Peptide chain elongation rate and ribosomal activity in Saccharomyces cerevisiae as a function of the growth rate. Molecular and General Genetics 170, 225–230.Google Scholar
Brandt, F., Carlson, L. A., Hartl, F. U., Baumeister, W. & Grunewald, K. (2010). The three-dimensional organization of polyribosomes in intact human cells. Molecular Cell 39, 560–569.Google Scholar
Brandt, F., Etchells, S. A., Ortiz, J. O., Elcock, A. H., Hartl, F. U. & Baumeister, W. (2009). The native 3D organization of bacterial polysomes. Cell 136, 261–271.Google Scholar
Budkevich, T., Giesebrecht, J., Altman, R. B., Munro, J. B., Mielke, T., Nierhaus, K. H., Blanchard, S. C. & Spahn, C. M. (2011). Structure and dynamics of the mammalian ribosomal pretranslocation complex. Molecular Cell 44, 214–224.Google Scholar
Budkevich, T. V., Giesebrecht, J., Behrmann, E., Loerke, J., Ramrath, D. J., Mielke, T., Ismer, J., Hildebrand, P. W., Tung, C. S., Nierhaus, K. H., Sanbonmatsu, K. Y. & Spahn, C. M. (2014). Regulation of the mammalian elongation cycle by subunit rolling: a eukaryotic-specific ribosome rearrangement. Cell 158, 121–131.Google Scholar
Bulkley, D., Innis, C. A., Blaha, G. & Steitz, T. A. (2010). Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proceedings of the National Academy of Sciences of the United States of America 107, 17158–17163.Google Scholar
Caliskan, N., Katunin, V. I., Belardinelli, R., Peske, F. & Rodnina, M. V. (2014). Programmed -1 frameshifting by kinetic partitioning during impeded translocation. Cell 157, 1619–1631.Google Scholar
Caliskan, N., Peske, F. & Rodnina, M. V. (2015). Changed in translation: mRNA recoding by -1 programmed ribosomal frameshifting. Trends in Biochemical Sciences 40, 265–274.Google Scholar
Carberry, S. E., Rhoads, R. E. & Goss, D. J. (1989). A spectroscopic study of the binding of m7GTP and m7GpppG to human protein synthesis initiation factor 4E. Biochemistry 28, 8078–8083.Google Scholar
Caruthers, J. M., Johnson, E. R. & Mckay, D. B. (2000). Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proceedings of the National Academy of Sciences of the United States of America 97, 13080–13085.Google Scholar
Castello, A., Alvarez, E. & Carrasco, L. (2006). Differential cleavage of eIF4GI and eIF4GII in mammalian cells. Effects on translation. The Journal of Biological Chemistry 281, 33206–33216.Google Scholar
Chan, C. C., Dostie, J., Diem, M. D., Feng, W., Mann, M., Rappsilber, J. & Dreyfuss, G. (2004). eIF4A3 is a novel component of the exon junction complex. RNA 10, 200–209.Google Scholar
Chapman, H. N., Fromme, P., Barty, A., White, T. A., Kirian, R. A., Aquila, A., Hunter, M. S., Schulz, J., Deponte, D. P., Weierstall, U., Doak, R. B., Maia, F. R., Martin, A. V., Schlichting, I., Lomb, L., Coppola, N., Shoeman, R. L., Epp, S. W., Hartmann, R., Rolles, D., Rudenko, A., Foucar, L., Kimmel, N., Weidenspointner, G., Holl, P., Liang, M., Barthelmess, M., Caleman, C., Boutet, S., Bogan, M. J., Krzywinski, J., Bostedt, C., Bajt, S., Gumprecht, L., Rudek, B., Erk, B., Schmidt, C., Homke, A., Reich, C., Pietschner, D., Struder, L., Hauser, G., Gorke, H., Ullrich, J., Herrmann, S., Schaller, G., Schopper, F., Soltau, H., Kuhnel, K. U., Messerschmidt, M., Bozek, J. D., Hau-Riege, S. P., Frank, M., Hampton, C. Y., Sierra, R. G., Starodub, D., Williams, G. J., Hajdu, J., Timneanu, N., Seibert, M. M., Andreasson, J., Rocker, A., Jonsson, O., Svenda, M., Stern, S., Nass, K., Andritschke, R., Schroter, C. D., Krasniqi, F., Bott, M., Schmidt, K. E., Wang, X., Grotjohann, I., Holton, J. M., Barends, T. R., Neutze, R., Marchesini, S., Fromme, R., Schorb, S., Rupp, D., Adolph, M., Gorkhover, T., Andersson, I., Hirsemann, H., Potdevin, G., Graafsma, H., Nilsson, B. & Spence, J. C. (2011). Femtosecond X-ray protein nanocrystallography. Nature 470, 73–77.Google Scholar
Chen, C., Stevens, B., Kaur, J., Cabral, D., Liu, H., Wang, Y., Zhang, H., Rosenblum, G., Smilansky, Z., Goldman, Y. E. & Cooperman, B. S. (2011a). Single-molecule fluorescence measurements of ribosomal translocation dynamics. Molecular Cell 42, 367–377.Google Scholar
Chen, C., Stevens, B., Kaur, J., Smilansky, Z., Cooperman, B. S. & Goldman, Y. E. (2011b). Allosteric vs. spontaneous exit-site (E-site) tRNA dissociation early in protein synthesis. Proceedings of the National Academy of Sciences of the United States of America 108, 16980–16985.Google Scholar
Chen, C., Zhang, H., Broitman, S. L., Reiche, M., Farrell, I., Cooperman, B. S. & Goldman, Y. E. (2013a). Dynamics of translation by single ribosomes through mRNA secondary structures. Nature Structural & Molecular Biology 20, 582–588.Google Scholar
Chen, J., Coakley, A., O'CONNOR, M., Petrov, A., O'Leary, S. E., Atkins, J. F. & Puglisi, J. D. (2015). Coupling of mRNA structure rearrangement to ribosome movement during bypassing of non-coding regions. Cell 163, 1267–1280.Google Scholar
Chen, J., Dalal, R. V., Petrov, A. N., Tsai, A., O'LEARY, S. E., Chapin, K., Cheng, J., Ewan, M., Hsiung, P. L., Lundquist, P., Turner, S. W., Hsu, D. R. & Puglisi, J. D. (2013b). High-throughput platform for real-time monitoring of biological processes by multicolor single-molecule fluorescence. Proceedings of the National Academy of Sciences of the United States of America 111, 664–669.Google Scholar
Chen, J., Petrov, A., Johansson, M., Tsai, A., O'Leary, S. E. & Puglisi, J. D. (2014). Dynamic pathways of -1 translational frameshifting. Nature 512, 328–332.Google Scholar
Chen, J., Petrov, A., Tsai, A., O'Leary, S. E. & Puglisi, J. D. (2013c). Coordinated conformational and compositional dynamics drive ribosome translocation. Nature Structural & Molecular Biology 20, 718–727.Google Scholar
Chen, J., Tsai, A., O'LEARY, S. E., Petrov, A. & Puglisi, J. D. (2012a). Unraveling the dynamics of ribosome translocation. Current Opinion in Structural Biology 22, 804–814.Google Scholar
Chen, J., Tsai, A., Petrov, A. & Puglisi, J. D. (2012b). Nonfluorescent quenchers to correlate single-molecule conformational and compositional dynamics. Journal of the American Chemical Society 134, 5734–5737.Google Scholar
Chen, Y., Potratz, J. P., Tijerina, P., Del Campo, M., Lambowitz, A. M. & Russell, R. (2008). DEAD-box proteins can completely separate an RNA duplex using a single ATP. Proceedings of the National Academy of Sciences of the United States of America 105, 20203–20208.Google Scholar
Cheng, S. & Gallie, D. R. (2007). eIF4G, eIFiso4G, and eIF4B bind the poly(A)-binding protein through overlapping sites within the RNA recognition motif domains. The Journal of Biological Chemistry 282, 25247–25258.Google Scholar
Choi, J., Ieong, K. W., Demirci, H., Chen, J., Petrov, A., Prabhakar, A., O'Leary, S. E., Dominissini, D., Rechavi, G., Soltis, S. M., Ehrenberg, M. & Puglisi, J. D. (2016). N-methyladenosine in mRNA disrupts tRNA selection and translation-elongation dynamics. Nature Structural & Molecular Biology 23, 110–115.Google Scholar
Chuang, R. Y., Weaver, P. L., Liu, Z. & Chang, T. H. (1997). Requirement of the DEAD-Box protein ded1p for messenger RNA translation. Science 275, 1468–1471.Google Scholar
Clarkson, B. K., Gilbert, W. V. & Doudna, J. A. (2010). Functional overlap between eIF4G isoforms in Saccharomyces cerevisiae . PLoS ONE 5, e9114.Google Scholar
Comstock, M. J., Ha, T. & Chemla, Y. R. (2011). Ultrahigh-resolution optical trap with single-fluorophore sensitivity. Nature Methods 8, 335–340.CrossRefGoogle ScholarPubMed
Cooper, H. L., Park, M. H., Folk, J. E., Safer, B. & Braverman, R. (1983). Identification of the hypusine-containing protein hy+ as translation initiation factor eIF-4D. Proceedings of the National Academy of Sciences of the United States of America 80, 1854–1857.Google Scholar
Cornish, P. V., Ermolenko, D. N., Noller, H. F. & Ha, T. (2008). Spontaneous intersubunit rotation in single ribosomes. Molecular Cell 30, 578–588.Google Scholar
Cornish, P. V., Ermolenko, D. N., Staple, D. W., Hoang, L., Hickerson, R. P., Noller, H. F. & Ha, T. (2009). Following movement of the L1 stalk between three functional states in single ribosomes. Proceedings of the National Academy of Sciences of the United States of America 106, 2571–2576.Google Scholar
de la Cruz, J., Iost, I., Kressler, D. & Linder, P. (1997). The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae . Proceedings of the National Academy of Sciences of the United States of America 94, 5201–5206.Google Scholar
Deardorff, J. A. & Sachs, A. B. (1997). Differential effects of aromatic and charged residue substitutions in the RNA binding domains of the yeast poly(A)-binding protein. Journal of Molecular Biology 269, 67–81.Google Scholar
Deng, X., Chen, K., Luo, G. Z., Weng, X., Ji, Q., Zhou, T. & He, C. (2015). Widespread occurrence of N6-methyladenosine in bacterial mRNA. Nucleic Acids Research 43, 6557–6567.Google Scholar
Dever, T. E. & Green, R. (2012). The elongation, termination, and recycling phases of translation in eukaryotes. Cold Spring Harbor Perspectives in Biology 4, a013706.Google Scholar
Dever, T. E., Gutierrez, E. & Shin, B. S. (2014). The hypusine-containing translation factor eIF5A. Critical Reviews in Biochemistry and Molecular Biology 49, 413–425.Google Scholar
Dhote, V., Sweeney, T. R., Kim, N., Hellen, C. U. & Pestova, T. V. (2012). Roles of individual domains in the function of DHX29, an essential factor required for translation of structured mammalian mRNAs. Proceedings of the National Academy of Sciences of the United States of America 109, E3150–E3159.Google Scholar
Doerfel, L. K., Wohlgemuth, I., Kothe, C., Peske, F., Urlaub, H. & Rodnina, M. V. (2013). EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339, 85–88.Google Scholar
Doerfel, L. K., Wohlgemuth, I., Kubyshkin, V., Starosta, A. L., Wilson, D. N., Budisa, N. & Rodnina, M. V. (2015). Entropic contribution of elongation factor P to proline positioning at the catalytic center of the Ribosome. Journal of the American Chemical Society 137, 12997–13006.Google Scholar
Dominissini, D., Moshitch-Moshkovitz, S., Schwartz, S., Salmon-Divon, M., Ungar, L., Osenberg, S., Cesarkas, K., Jacob-Hirsch, J., Amariglio, N., Kupiec, M., Sorek, R. & Rechavi, G. (2012). Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485, 201–206.Google Scholar
Dorner, S., Brunelle, J. L., Sharma, D. & Green, R. (2006). The hybrid state of tRNA binding is an authentic translation elongation intermediate. Nature Structural & Molecular Biology 13, 234–241.Google Scholar
Dorywalska, M., Blanchard, S. C., Gonzalez, R. L., Kim, H. D., Chu, S. & Puglisi, J. D. (2005). Site-specific labeling of the ribosome for single-molecule spectroscopy. Nucleic Acids Research 33, 182–189.Google Scholar
Dunkle, J. A. & Cate, J. H. (2010). Ribosome structure and dynamics during translocation and termination. Annual Review of Biophysics 39, 227–244.Google Scholar
Dunkle, J. A., Wang, L., Feldman, M. B., Pulk, A., Chen, V. B., Kapral, G. J., Noeske, J., Richardson, J. S., Blanchard, S. C. & Cate, J. H. (2011). Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332, 981–984.Google Scholar
Dunkle, J. A., Xiong, L., Mankin, A. S. & Cate, J. H. (2010). Structures of the Escherichia coli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proceedings of the National Academy of Sciences of the United States of America 107, 17152–17157.Google Scholar
Dupuis, N. F., Holmstrom, E. D. & Nesbitt, D. J. (2014). Molecular-crowding effects on single-molecule RNA folding/unfolding thermodynamics and kinetics. Proceedings of the National Academy of Sciences of the United States of America 111, 8464–8469.Google Scholar
Edelmann, P. & Gallant, J. (1977). Mistranslation in E. coli . Cell 10, 131–137.Google Scholar
Eiler, D., Lin, J., Simonetti, A., Klaholz, B. P. & Steitz, T. A. (2013). Initiation factor 2 crystal structure reveals a different domain organization from eukaryotic initiation factor 5B and mechanism among translational GTPases. Proceedings of the National Academy of Sciences of the United States of America 110, 15662–15667.Google Scholar
EL'SKAYA, A. V., Ovcharenko, G. V., Palchevskii, S. S., Petrushenko, Z. M., Triana-Alonso, F. J. & Nierhaus, K. H. (1997). Three tRNA binding sites in rabbit liver ribosomes and role of the intrinsic ATPase in 80S ribosomes from higher eukaryotes. Biochemistry 36, 10492–10497.Google Scholar
Elvekrog, M. M. & Gonzalez, R. L. Jr. (2013). Conformational selection of translation initiation factor 3 signals proper substrate selection. Nature Structural & Molecular Biology 20, 628–633.Google Scholar
Ermolenko, D. N., Majumdar, Z. K., Hickerson, R. P., Spiegel, P. C., Clegg, R. M. & Noller, H. F. (2007). Observation of intersubunit movement of the ribosome in solution using FRET. Journal of Molecular Biology 370, 530–540.Google Scholar
Ermolenko, D. N. & Noller, H. F. (2011). mRNA translocation occurs during the second step of ribosomal intersubunit rotation. Nature Structural & Molecular Biology 18, 457–462.Google Scholar
Erzberger, J. P., Stengel, F., Pellarin, R., Zhang, S., Schaefer, T., Aylett, C. H., Cimermancic, P., Boehringer, D., Sali, A., Aebersold, R. & Ban, N. (2014). Molecular architecture of the 40SeIF1eIF3 translation initiation complex. Cell 158, 1123–1135.Google Scholar
Fei, J., Bronson, J. E., Hofman, J. M., Srinivas, R. L., Wiggins, C. H. & Gonzalez, R. L. Jr. (2009). Allosteric collaboration between elongation factor G and the ribosomal L1 stalk directs tRNA movements during translation. Proceedings of the National Academy of Sciences of the United States of America 106, 15702–15707.Google Scholar
Fei, J., Kosuri, P., Macdougall, D. D. & Gonzalez, R. L. Jr. (2008). Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Molecular Cell 30, 348–359.CrossRefGoogle ScholarPubMed
Fei, J., Richard, A. C., Bronson, J. E. & Gonzalez, R. L. Jr. (2011). Transfer RNA-mediated regulation of ribosome dynamics during protein synthesis. Nature Structural & Molecular Biology 18, 1043–1051.Google Scholar
Ferguson, A., Wang, L., Altman, R. B., Terry, D. S., Juette, M. F., Burnett, B. J., Alejo, J. L., Dass, R. A., Parks, M. M., Vincent, C. T. & Blanchard, S. C. (2015). Functional dynamics within the human ribosome regulate the rate of active protein synthesis. Molecular Cell 60, 475–486.Google Scholar
Fernández, I. S., Bai, X. C., Hussain, T., Kelley, A. C., Lorsch, J. R., Ramakrishnan, V. & Scheres, S. H. (2013). Molecular architecture of a eukaryotic translational initiation complex. Science 342, 1240585.Google Scholar
Fernandez, I. S., Bai, X. C., Murshudov, G., Scheres, S. H. & Ramakrishnan, V. (2014). Initiation of translation by cricket paralysis virus IRES requires its translocation in the ribosome. Cell 157, 823–831.Google Scholar
Ferraiuolo, M. A., Lee, C. S., Ler, L. W., Hsu, J. L., Costa-Mattioli, M., Luo, M. J., Reed, R. & Sonenberg, N. (2004). A nuclear translation-like factor eIF4AIII is recruited to the mRNA during splicing and functions in nonsense-mediated decay. Proceedings of the National Academy of Sciences of the United States of America 101, 4118–4123.Google Scholar
Firczuk, H., Kannambath, S., Pahle, J., Claydon, A., Beynon, R., Duncan, J., Westerhoff, H., Mendes, P. & Mccarthy, J. E. (2013). An in vivo control map for the eukaryotic mRNA translation machinery. Molecular Systems Biology 9, 635.Google Scholar
Fischer, N., Konevega, A. L., Wintermeyer, W., Rodnina, M. V. & Stark, H. (2010). Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 466, 329–333.Google Scholar
Fischer, N., Neumann, P., Konevega, A. L., Bock, L. V., Ficner, R., Rodnina, M. V. & Stark, H. (2015). Structure of the E. coli ribosome-EF-Tu complex at <3 A resolution by Cs-corrected cryo-EM. Nature 520, 567–570.Google Scholar
Fluman, N., Navon, S., Bibi, E. & Pilpel, Y. (2014). mRNA-programmed translation pauses in the targeting of E. coli membrane proteins. eLife 3, e03440.Google Scholar
Frank, J. & Agrawal, R. K. (2000). A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406, 318–322.Google Scholar
Frank, J., Gao, H., Sengupta, J., Gao, N. & Taylor, D. J. (2007). The process of mRNA-tRNA translocation. Proceedings of the National Academy of Sciences of the United States of America 104, 19671–19678.Google Scholar
Frank, J. & Gonzalez, R. L. Jr. (2010). Structure and dynamics of a processive Brownian motor: the translating ribosome. Annual Review of Biochemistry 79, 381–412.Google Scholar
Fraser, C. S. (2015). Quantitative studies of mRNA recruitment to the eukaryotic ribosome. Biochimie 114, 58–71.Google Scholar
Freistroffer, D. V., Pavlov, M. Y., Macdougall, J., Buckingham, R. H. & Ehrenberg, M. (1997). Release factor RF3 in E.coli accelerates the dissociation of release factors RF1 and RF2 from the ribosome in a GTP-dependent manner. The EMBO Journal 16, 4126–4133.Google Scholar
Frolova, L., le Goff, X., Zhouravleva, G., Davydova, E., Philippe, M. & Kisselev, L. (1996). Eukaryotic polypeptide chain release factor eRF3 is an eRF1- and ribosome-dependent guanosine triphosphatase. RNA 2, 334–341.Google Scholar
Fronczek, D. N., Quammen, C., Wang, H., Kisker, C., Superfine, R., Taylor, R., Erie, D. A. & Tessmer, I. (2011). High accuracy FIONA-AFM hybrid imaging. Ultramicroscopy 111, 350–355.Google Scholar
Furuichi, Y. & Miura, K. (1975). A blocked structure at the 5′ terminus of mRNA from cytoplasmic polyhedrosis virus. Nature 253, 374–375.Google Scholar
Furuichi, Y., Morgan, M., Muthukrishnan, S. & Shatkin, A. J. (1975). Reovirus messenger RNA contains a methylated, blocked 5′-terminal structure: m-7G(5′)ppp(5′)G-MpCp-. Proceedings of the National Academy of Sciences of the United States of America 72, 362–366.Google Scholar
Gagnon, M. G., Lin, J., Bulkley, D. & Steitz, T. A. (2014). Ribosome structure. Crystal structure of elongation factor 4 bound to a clockwise ratcheted ribosome. Science 345, 684–687.Google Scholar
Galicia-Vázquez, G., Cencic, R., Robert, F., Agenor, A. Q. & Pelletier, J. (2012). A cellular response linking eIF4AI activity to eIF4AII transcription. RNA 18, 1373–1384.Google Scholar
Gao, H., Zhou, Z., Rawat, U., Huang, C., Bouakaz, L., Wang, C., Cheng, Z., Liu, Y., Zavialov, A., Gursky, R., Sanyal, S., Ehrenberg, M., Frank, J. & Song, H. (2007). RF3 induces ribosomal conformational changes responsible for dissociation of class I release factors. Cell 129, 929–941.Google Scholar
Gao, Y. G., Selmer, M., Dunham, C. M., Weixlbaumer, A., Kelley, A. C. & Ramakrishnan, V. (2009). The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326, 694–699.Google Scholar
García-García, C., Frieda, K. L., Feoktistova, K., Fraser, C. S. & Block, S. M. (2015). RNA BIOCHEMISTRY. Factor-dependent processivity in human eIF4A DEAD-box helicase. Science 348, 1486–1488.Google Scholar
Gosselin, P., Oulhen, N., Jam, M., Ronzca, J., Cormier, P., Czjzek, M. & Cosson, B. (2011). The translational repressor 4E-BP called to order by eIF4E: new structural insights by SAXS. Nucleic Acids Research 39, 3496–3503.Google Scholar
Goyer, C., Altmann, M., Lee, H. S., Blanc, A., Deshmukh, M., Woolford, J. L., Trachsel, H. & Sonenberg, N. (1993). TIF4631 and TIF4632: two yeast genes encoding the high-molecular-weight subunits of the cap-binding protein complex (eukaryotic initiation factor 4F) contain an RNA recognition motif-like sequence and carry out an essential function. Molecular and Cellular Biology 13, 4860–4874.Google Scholar
Goyer, C., Altmann, M., Trachsel, H. & Sonenberg, N. (1989). Identification and characterization of cap-binding proteins from yeast. The Journal of Biological Chemistry 264, 7603–7610.Google Scholar
Graber, T. E., Hebert-Seropian, S., Khoutorsky, A., David, A., Yewdell, J. W., Lacaille, J. C. & Sossin, W. S. (2013). Reactivation of stalled polyribosomes in synaptic plasticity. Proceedings of the National Academy of Sciences of the United States of America 110, 16205–16210.Google Scholar
Gradi, A., Imataka, H., Svitkin, Y. V., Rom, E., Raught, B., Morino, S. & Sonenberg, N. (1998). A novel functional human eukaryotic translation initiation factor 4G. Molecular and Cellular Biology 18, 334–342.Google Scholar
Graves, E. T., Duboc, C., Fan, J., Stransky, F., Leroux-Coyau, M. & Strick, T. R. (2015). A dynamic DNA-repair complex observed by correlative single-molecule nanomanipulation and fluorescence. Nature Structural & Molecular Biology 22, 452–457.Google Scholar
Gray, N. K., Coller, J. M., Dickson, K. S. & Wickens, M. (2000). Multiple portions of poly(A)-binding protein stimulate translation in vivo . The EMBO Journal 19, 4723–4733.Google Scholar
Grifo, J. A., Tahara, S. M., Leis, J. P., Morgan, M. A., Shatkin, A. J. & Merrick, W. C. (1982). Characterization of eukaryotic initiation factor 4A, a protein involved in ATP-dependent binding of globin mRNA. The Journal of Biological Chemistry 257, 5246–5252.Google Scholar
Grifo, J. A., Tahara, S. M., Morgan, M. A., Shatkin, A. J. & Merrick, W. C. (1983). New initiation factor activity required for globin mRNA translation. The Journal of Biological Chemistry 258, 5804–5810.Google Scholar
Groft, C. M. & Burley, S. K. (2002). Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Molecular Cell 9, 1273–1283.Google Scholar
Gromadski, K. B. & Rodnina, M. V. (2004). Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Molecular Cell 13, 191–200.Google Scholar
Gross, J. D., Moerke, N. J., von der Haar, T., Lugovskoy, A. A., Sachs, A. B., Mccarthy, J. E. & Wagner, G. (2003). Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115, 739–750.Google Scholar
Guo, Z. & Noller, H. F. (2012). Rotation of the head of the 30S ribosomal subunit during mRNA translocation. Proceedings of the National Academy of Sciences of the United States of America 109, 20391–20394.Google Scholar
Gutierrez, E., Shin, B. S., Woolstenhulme, C. J., Kim, J. R., Saini, P., Buskirk, A. R. & Dever, T. E. (2013). eIF5A promotes translation of polyproline motifs. Molecular Cell 51, 35–45.Google Scholar
Haghighat, A., Mader, S., Pause, A. & Sonenberg, N. (1995). Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E. The EMBO Journal 14, 5701–5709.Google Scholar
Hanawa-Suetsugu, K., Sekine, S., Sakai, H., Hori-Takemoto, C., Terada, T., Unzai, S., Tame, J. R., Kuramitsu, S., Shirouzu, M. & Yokoyama, S. (2004). Crystal structure of elongation factor P from Thermus thermophilus HB8. Proceedings of the National Academy of Sciences of the United States of America 101, 9595–9600.Google Scholar
Harms, U., Andreou, A. Z., Gubaev, A. & Klostermeier, D. (2014). eIF4B, eIF4G and RNA regulate eIF4A activity in translation initiation by modulating the eIF4A conformational cycle. Nucleic Acids Research 42, 7911–7922.Google Scholar
Hashem, Y., des Georges, A., Dhote, V., Langlois, R., Liao, H. Y., Grassucci, R. A., Hellen, C. U., Pestova, T. V. & Frank, J. (2013). Structure of the mammalian ribosomal 43S preinitiation complex bound to the scanning factor DHX29. Cell 153, 1108–1119.Google Scholar
He, H., von der Haar, T., Singh, C. R., Ii, M., Li, B., Hinnebusch, A. G., Mccarthy, J. E. & Asano, K. (2003). The yeast eukaryotic initiation factor 4G (eIF4G) HEAT domain interacts with eIF1 and eIF5 and is involved in stringent AUG selection. Molecular and Cellular Biology 23, 5431–5445.Google Scholar
Henderson, A. & Hershey, J. W. (2011). Eukaryotic translation initiation factor (eIF) 5A stimulates protein synthesis in Saccharomyces cerevisiae . Proceedings of the National Academy of Sciences of the United States of America 108, 6415–6419.Google Scholar
Herr, A. J., Atkins, J. F. & Gesteland, R. F. (2000a). Coupling of open reading frames by translational bypassing. Annual Review of Biochemistry 69, 343–372.Google Scholar
Herr, A. J., Gesteland, R. F. & Atkins, J. F. (2000b). One protein from two open reading frames: mechanism of a 50 nt translational bypass. The EMBO Journal 19, 2671–2680.Google Scholar
Herr, A. J., Wills, N. M., Nelson, C. C., Gesteland, R. F. & Atkins, J. F. (2004). Factors that influence selection of coding resumption sites in translational bypassing: minimal conventional peptidyl-tRNA:mRNA pairing can suffice. The Journal of Biological Chemistry 279, 11081–11087.Google Scholar
Hershey, J. W., Smit-Mcbride, Z. & Schnier, J. (1990). The role of mammalian initiation factor eIF-4D and its hypusine modification in translation. Biochimica et Biophysica Acta 1050, 160–162.Google Scholar
Hershey, P. E., Mcwhirter, S. M., Gross, J. D., Wagner, G., Alber, T. & Sachs, A. B. (1999). The Cap-binding protein eIF4E promotes folding of a functional domain of yeast translation initiation factor eIF4G1. The Journal of Biological Chemistry 274, 21297–21304.Google Scholar
Hilbert, M., Kebbel, F., Gubaev, A. & Klostermeier, D. (2011). eIF4G stimulates the activity of the DEAD box protein eIF4A by a conformational guidance mechanism. Nucleic Acids Research 39, 2260–2270.Google Scholar
Hilliker, A., Gao, Z., Jankowsky, E. & Parker, R. (2011). The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F-mRNA complex. Molecular Cell 43, 962–972.Google Scholar
Hinnebusch, A. G. (2005). Translational regulation of GCN4 and the general amino acid control of yeast. Annual Review of Microbiology 59, 407–450.Google Scholar
Hinnebusch, A. G. (2006). eIF3: a versatile scaffold for translation initiation complexes. Trends in Biochemical Sciences 31, 553–562.CrossRefGoogle ScholarPubMed
Hinnebusch, A. G. (2011). Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiology and Molecular Biology Reviews 75, 434–467, first page of table of contents.Google Scholar
Hinnebusch, A. G. & Lorsch, J. R. (2012). The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harbor Perspectives in Biology 4.Google Scholar
Hinton, T. M., Coldwell, M. J., Carpenter, G. A., Morley, S. J. & Pain, V. M. (2007). Functional analysis of individual binding activities of the scaffold protein eIF4G. The Journal of Biological Chemistry 282, 1695–1708.Google Scholar
Hirokawa, G., Nijman, R. M., Raj, V. S., Kaji, H., Igarashi, K. & Kaji, A. (2005). The role of ribosome recycling factor in dissociation of 70S ribosomes into subunits. RNA 11, 1317–1328.CrossRefGoogle ScholarPubMed
Hofmann, W., Reichart, B., Ewald, A., Muller, E., Schmitt, I., Stauber, R. H., Lottspeich, F., Jockusch, B. M., Scheer, U., Hauber, J. & Dabauvalle, M. C. (2001). Cofactor requirements for nuclear export of Rev response element (RRE)- and constitutive transport element (CTE)-containing retroviral RNAs. An unexpected role for actin. The Journal of Cell Biology 152, 895–910.CrossRefGoogle ScholarPubMed
Holtkamp, W., Wintermeyer, W. & Rodnina, M. V. (2014). Synchronous tRNA movements during translocation on the ribosome are orchestrated by elongation factor G and GTP hydrolysis. Bioessays 36, 908–918.Google Scholar
Hopfield, J. J. (1974). Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proceedings of the National Academy of Sciences of the United States of America 71, 4135–4139.Google Scholar
Horan, L. H. & Noller, H. F. (2007). Intersubunit movement is required for ribosomal translocation. Proceedings of the National Academy of Sciences of the United States of America 104, 4881–4885.Google Scholar
Huang, W. M., Ao, S. Z., Casjens, S., Orlandi, R., Zeikus, R., Weiss, R., Winge, D. & Fang, M. (1988). A persistent untranslated sequence within bacteriophage T4 DNA topoisomerase gene 60. Science 239, 1005–1012.CrossRefGoogle ScholarPubMed
Hussain, T., Llácer, J. L., Fernández, I. S., Munoz, A., Martin-Marcos, P., Savva, C. G., Lorsch, J. R., Hinnebusch, A. G. & Ramakrishnan, V. (2014). Structural changes enable start codon recognition by the eukaryotic translation initiation complex. Cell 159, 597–607.Google Scholar
Imataka, H., Gradi, A. & Sonenberg, N. (1998). A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. The EMBO Journal 17, 7480–7489.Google Scholar
Imataka, H. & Sonenberg, N. (1997). Human eukaryotic translation initiation factor 4G (eIF4G) possesses two separate and independent binding sites for eIF4A. Molecular and Cellular Biology 17, 6940–6947.Google Scholar
Ingolia, N. T., Ghaemmaghami, S., Newman, J. R. & Weissman, J. S. (2009). Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324, 218–223.Google Scholar
Ingolia, N. T., Lareau, L. F. & Weissman, J. S. (2011). Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147, 789–802.Google Scholar
Ito, K. & Chiba, S. (2013). Arrest peptides: cis-acting modulators of translation. Annual Review of Biochemistry 82, 171–202.Google Scholar
Ito, K., Ebihara, K. & Nakamura, Y. (1998). The stretch of C-terminal acidic amino acids of translational release factor eRF1 is a primary binding site for eRF3 of fission yeast. RNA 4, 958–972.Google Scholar
Ito, K., Ebihara, K., Uno, M. & Nakamura, Y. (1996). Conserved motifs in prokaryotic and eukaryotic polypeptide release factors: tRNA-protein mimicry hypothesis. Proceedings of the National Academy of Sciences of the United States of America 93, 5443–5448.Google Scholar
Jacks, T., Madhani, H. D., Masiarz, F. R. & Varmus, H. E. (1988a). Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell 55, 447–458.Google Scholar
Jacks, T., Power, M. D., Masiarz, F. R., Luciw, P. A., Barr, P. J. & Varmus, H. E. (1988b). Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 331, 280–283.Google Scholar
Jackson, R. J. (2013). The current status of vertebrate cellular mRNA IRESs. Cold Spring Harbor Perspectives in Biology 5.Google Scholar
Jackson, R. J., Hellen, C. U. & Pestova, T. V. (2010). The mechanism of eukaryotic translation initiation and principles of its regulation. Nature Reviews. Molecular Cell Biology 11, 113–127.Google Scholar
Jackson, R. J., Hellen, C. U. & Pestova, T. V. (2012). Termination and post-termination events in eukaryotic translation. Advances in Protein Chemistry and Structural Biology 86, 45–93.Google Scholar
Jao, D. L. & Chen, K. Y. (2006). Tandem affinity purification revealed the hypusine-dependent binding of eukaryotic initiation factor 5A to the translating 80S ribosomal complex. Journal of Cellular Biochemistry 97, 583–598.Google Scholar
Jenner, L. B., Demeshkina, N., Yusupova, G. & Yusupov, M. (2010). Structural aspects of messenger RNA reading frame maintenance by the ribosome. Nature Structural & Molecular Biology 17, 555–560.Google Scholar
Johansson, M., Bouakaz, E., Lovmar, M. & Ehrenberg, M. (2008). The kinetics of ribosomal peptidyl transfer revisited. Molecular Cell 30, 589–598.Google Scholar
Johansson, M., Chen, J., Tsai, A., Kornberg, G. & Puglisi, J. D. (2014). Sequence-dependent elongation dynamics on macrolide-bound ribosomes. Cell Reports 7, 1534–1546.Google Scholar
Johansson, M., Zhang, J. & Ehrenberg, M. (2012). Genetic code translation displays a linear trade-off between efficiency and accuracy of tRNA selection. Proceedings of the National Academy of Sciences of the United States of America 109, 131–136.Google Scholar
Kahvejian, A., Roy, G. & Sonenberg, N. (2001). The mRNA closed-loop model: the function of PABP and PABP-interacting proteins in mRNA translation. Cold Spring Harbor Symposia on Quantitative Biology 66, 293–300.Google Scholar
Kahvejian, A., Svitkin, Y. V., Sukarieh, R., M'Boutchou, M. N. & Sonenberg, N. (2005). Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes & Development 19, 104–113.Google Scholar
Kang, H. A. & Hershey, J. W. (1994). Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae . The Journal of Biological Chemistry 269, 3934–3940.Google Scholar
Kannan, K., Kanabar, P., Schryer, D., Florin, T., Oh, E., Bahroos, N., Tenson, T., Weissman, J. S. & Mankin, A. S. (2014). The general mode of translation inhibition by macrolide antibiotics. Proceedings of the National Academy of Sciences of the United States of America 111, 15958–15963.Google Scholar
Karaskova, M., Gunisova, S., Herrmannova, A., Wagner, S., Munzarova, V. & Valasek, L. (2012). Functional characterization of the role of the N-terminal domain of the c/Nip1 subunit of eukaryotic initiation factor 3 (eIF3) in AUG recognition. The Journal of Biological Chemistry 287, 28420–28434.Google Scholar
Karim, M. M., Svitkin, Y. V., Kahvejian, A., de Crescenzo, G., Costa-Mattioli, M. & Sonenberg, N. (2006). A mechanism of translational repression by competition of Paip2 with eIF4G for poly(A) binding protein (PABP) binding. Proceedings of the National Academy of Sciences of the United States of America 103, 9494–9499.Google Scholar
Karimi, R., Pavlov, M. Y., Buckingham, R. H. & Ehrenberg, M. (1999). Novel roles for classical factors at the interface between translation termination and initiation. Molecular Cell 3, 601–609.Google Scholar
Kaye, N. M., Emmett, K. J., Merrick, W. C. & Jankowsky, E. (2009). Intrinsic RNA binding by the eukaryotic initiation factor 4F depends on a minimal RNA length but not on the m7G cap. The Journal of Biological Chemistry 284, 17742–17750.Google Scholar
Keiler, K. C., Waller, P. R. & Sauer, R. T. (1996). Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271, 990–993.Google Scholar
Kemper, W. M., Berry, K. W. & Merrick, W. C. (1976). Purification and properties of rabbit reticulocyte protein synthesis initiation factors M2Balpha and M2Bbeta. The Journal of Biological Chemistry 251, 5551–5557.Google Scholar
Khoshnevis, S., Gunisova, S., Vlckova, V., Kouba, T., Neumann, P., Beznoskova, P., Ficner, R. & Valasek, L. S. (2014). Structural integrity of the PCI domain of eIF3a/TIF32 is required for mRNA recruitment to the 43S pre-initiation complexes. Nucleic Acids Research 42, 4123–4139.Google Scholar
Kiel, M. C., Aoki, H. & Ganoza, M. C. (1999). Identification of a ribosomal ATPase in Escherichia coli cells. Biochimie 81, 1097–1108.Google Scholar
Kiel, M. C. & Ganoza, M. C. (2001). Functional interactions of an Escherichia coli ribosomal ATPase. European Journal of Biochemistry 268, 278–286.Google Scholar
Kim, H. D., Puglisi, J. D. & Chu, S. (2007). Fluctuations of transfer RNAs between classical and hybrid states. Biophysical Journal 93, 3575–3582.Google Scholar
Kim, H. K., Liu, F., Fei, J., Bustamante, C., Gonzalez, R. L. Jr. & Tinoco, I. Jr. (2014). A frameshifting stimulatory stem loop destabilizes the hybrid state and impedes ribosomal translocation. Proceedings of the National Academy of Sciences of the United States of America 111, 5538–5543.Google Scholar
Kim, H. S., Wilce, M. C., Yoga, Y. M., Pendini, N. R., Gunzburg, M. J., Cowieson, N. P., Wilson, G. M., Williams, B. R., Gorospe, M. & Wilce, J. A. (2011). Different modes of interaction by TIAR and HuR with target RNA and DNA. Nucleic Acids Research 39, 1117–1130.Google Scholar
Knoops, K., Schoehn, G. & Schaffitzel, C. (2012). Cryo-electron microscopy of ribosomal complexes in cotranslational folding, targeting, and translocation. Wiley Interdisciplinary Reviews, RNA 3, 429–441.Google Scholar
Koh, C. S., Brilot, A. F., Grigorieff, N. & Korostelev, A. A. (2014). Taura syndrome virus IRES initiates translation by binding its tRNA–mRNA-like structural element in the ribosomal decoding center. Proceedings of the National Academy of Sciences of the United States of America 111, 9139–9144.Google Scholar
Kolupaeva, V. G., Unbehaun, A., Lomakin, I. B., Hellen, C. U. & Pestova, T. V. (2005). Binding of eukaryotic initiation factor 3 to ribosomal 40S subunits and its role in ribosomal dissociation and anti-association. RNA 11, 470–486.Google Scholar
Korostelev, A., Asahara, H., Lancaster, L., Laurberg, M., Hirschi, A., Zhu, J., Trakhanov, S., Scott, W. G. & Noller, H. F. (2008). Crystal structure of a translation termination complex formed with release factor RF2. Proceedings of the National Academy of Sciences of the United States of America 105, 19684–19689.Google Scholar
Koutmou, K. S., Mcdonald, M. E., Brunelle, J. L. & Green, R. (2014). RF3:GTP promotes rapid dissociation of the class 1 termination factor. RNA 20, 609–620.Google Scholar
Kozak, M. (2002). Pushing the limits of the scanning mechanism for initiation of translation. Gene 299, 1–34.Google Scholar
Kuhle, B. & Ficner, R. (2014a). eIF5B employs a novel domain release mechanism to catalyze ribosomal subunit joining. The EMBO Journal 33, 1177–1191.Google Scholar
Kuhle, B. & Ficner, R. (2014b). Structural insight into the recognition of amino-acylated initiator tRNA by eIF5B in the 80S initiation complex. BMC Structural Biology 14, 20.Google Scholar
Lamphear, B. J., Kirchweger, R., Skern, T. & Rhoads, R. E. (1995). Mapping of functional domains in eukaryotic protein synthesis initiation factor 4 G (eIF4G) with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. The Journal of Biological Chemistry 270, 21975–21983.Google Scholar
Lang, B. F., Jakubkova, M., Hegedusova, E., Daoud, R., Forget, L., Brejova, B., Vinar, T., Kosa, P., Fricova, D., Nebohacova, M., Griac, P., Tomaska, L., Burger, G. & Nosek, J. (2014). Massive programmed translational jumping in mitochondria. Proceedings of the National Academy of Sciences of the United States of America 111, 5926–5931.Google Scholar
Lang, M. J., Fordyce, P. M., Engh, A. M., Neuman, K. C. & Block, S. M. (2004). Simultaneous, coincident optical trapping and single-molecule fluorescence. Nature Methods 1, 133–139.Google Scholar
Laurberg, M., Asahara, H., Korostelev, A., Zhu, J., Trakhanov, S. & Noller, H. F. (2008). Structural basis for translation termination on the 70S ribosome. Nature 454, 852–857.Google Scholar
Lax, S., Fritz, W., Browning, K. & Ravel, J. (1985). Isolation and characterization of factors from wheat germ that exhibit eukaryotic initiation factor 4B activity and overcome 7-methylguanosine 5′-triphosphate inhibition of polypeptide synthesis. Proceedings of the National Academy of Sciences of the United States of America 82, 330–333.Google Scholar
Lee, A. S., Burdeinick-Kerr, R. & Whelan, S. P. (2013). A ribosome-specialized translation initiation pathway is required for cap-dependent translation of vesicular stomatitis virus mRNAs. Proceedings of the National Academy of Sciences of the United States of America 110, 324–329.Google Scholar
Lefebvre, A. K., Korneeva, N. L., Trutschl, M., Cvek, U., Duzan, R. D., Bradley, C. A., Hershey, J. W. & Rhoads, R. E. (2006). Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. The Journal of Biological Chemistry 281, 22917–22932.Google Scholar
Levene, M. J., Korlach, J., Turner, S. W., Foquet, M., Craighead, H. G. & Webb, W. W. (2003). Zero-mode waveguides for single-molecule analysis at high concentrations. Science 299, 682–686.Google Scholar
Li, G. W., Oh, E. & Weissman, J. S. (2012). The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484, 538–541.Google Scholar
Li, W., Ross-Smith, N., Proud, C. G. & Belsham, G. J. (2001). Cleavage of translation initiation factor 4AI (eIF4AI) but not eIF4AII by foot-and-mouth disease virus 3C protease: identification of the eIF4AI cleavage site. FEBS Letters 507, 1–5.Google Scholar
Lin, J., Fabian, M., Sonenberg, N. & Meller, A. (2012). Nanopore detachment kinetics of poly(A) binding proteins from RNA molecules reveals the critical role of C-terminus interactions. Biophysical Journal 102, 1427–1434.Google Scholar
Linder, P. & Jankowsky, E. (2011). From unwinding to clamping - the DEAD box RNA helicase family. Nature Reviews. Molecular Cell Biology 12, 505–516.Google Scholar
Liu, C. Y., Qureshi, M. T. & Lee, T. H. (2011). Interaction strengths between the ribosome and tRNA at various steps of translocation. Biophysical Journal 100, 2201–2208.Google Scholar
Liu, F., Putnam, A. & Jankowsky, E. (2008). ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proceedings of the National Academy of Sciences of the United States of America 105, 20209–20214.Google Scholar
Liu, T., Kaplan, A., Alexander, L., Yan, S., Wen, J. D., Lancaster, L., Wickersham, C. E., Fredrik, K., Noller, H., Tinoco, I. & Bustamante, C. J. (2014a). Direct measurement of the mechanical work during translocation by the ribosome. eLife 3, e03406.Google Scholar
Liu, Y., Neumann, P., Kuhle, B., Monecke, T., Schell, S., Chari, A. & Ficner, R. (2014b). Translation initiation factor eIF3b contains a nine-bladed beta-propeller and interacts with the 40S ribosomal subunit. Structure 22, 923–930.Google Scholar
Lomakin, I. B. & Steitz, T. A. (2013). The initiation of mammalian protein synthesis and mRNA scanning mechanism. Nature 500, 307–311.Google Scholar
Lorsch, J. R. & Herschlag, D. (1998a). The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry 37, 2180–2193.CrossRefGoogle ScholarPubMed
Lorsch, J. R. & Herschlag, D. (1998b). The DEAD box protein eIF4A. 2. A cycle of nucleotide and RNA-dependent conformational changes. Biochemistry 37, 2194–2206.Google Scholar
Lucic, V., Rigort, A. & Baumeister, W. (2013). Cryo-electron tomography: the challenge of doing structural biology in situ. The Journal of Cell Biology 202, 407–419.Google Scholar
Maag, D., Algire, M. A. & Lorsch, J. R. (2006). Communication between eukaryotic translation initiation factors 5 and 1A within the ribosomal pre-initiation complex plays a role in start site selection. Journal of Molecular Biology 356, 724–737.Google Scholar
Maag, D., Fekete, C. A., Gryczynski, Z. & Lorsch, J. R. (2005). A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon. Molecular Cell 17, 265–275.Google Scholar
Maag, D. & Lorsch, J. R. (2003). Communication between eukaryotic translation initiation factors 1 and 1A on the yeast small ribosomal subunit. Journal of Molecular Biology 330, 917–924.CrossRefGoogle ScholarPubMed
MacDougall, D. D. & Gonzalez, R. L. (2011). Exploring the structural dynamics of the translational machinery using single-molecule fluorescence resonance energy transfer. Ribosomes: Structure, Function, and Dynamics, 273–293.Google Scholar
Mader, S., Lee, H., Pause, A. & Sonenberg, N. (1995). The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Molecular and Cellular Biology 15, 4990–4997.Google Scholar
Mallam, A. L., Del Campo, M., Gilman, B., Sidote, D. J. & Lambowitz, A. M. (2012). Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature 490, 121–125.Google Scholar
Mandal, A., Mandal, S. & Park, M. H. (2014). Genome-wide analyses and functional classification of proline repeat-rich proteins: potential role of eIF5A in eukaryotic evolution. PLoS ONE 9, e111800.Google Scholar
Mao, Y., Liu, H., Liu, Y. & Tao, S. (2014). Deciphering the rules by which dynamics of mRNA secondary structure affect translation efficiency in Saccharomyces cerevisiae . Nucleic Acids Research 42, 4813–4822.Google Scholar
Marcinkiewicz, C., Gajko, A. & Galasinski, W. (1991). Purification and properties of the heterogeneous subunits of elongation factor EF-1 from Guerin epithelioma cells. Acta Biochimica Polonica 38, 129–134.Google Scholar
Marcotrigiano, J., Gingras, A. C., Sonenberg, N. & Burley, S. K. (1997). Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89, 951–961.Google Scholar
Marcotrigiano, J., Gingras, A. C., Sonenberg, N. & Burley, S. K. (1999). Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Molecular Cell 3, 707–716.Google Scholar
Marintchev, A., Edmonds, K. A., Marintcheva, B., Hendrickson, E., Oberer, M., Suzuki, C., Herdy, B., Sonenberg, N. & Wagner, G. (2009). Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 136, 447–460.Google Scholar
Marintchev, A. & Wagner, G. (2004). Translation initiation: structures, mechanisms and evolution. Quarterly Reviews of Biophysics 37, 197–284.Google Scholar
Marquez, V., Wilson, D. N., Tate, W. P., Triana-Alonso, F. & Nierhaus, K. H. (2004). Maintaining the ribosomal reading frame: the influence of the E site during translational regulation of release factor 2. Cell 118, 45–55.Google Scholar
Marsden, S., Nardelli, M., Linder, P. & Mccarthy, J. E. (2006). Unwinding single RNA molecules using helicases involved in eukaryotic translation initiation. Journal of Molecular Biology 361, 327–335.Google Scholar
Marshall, R. A., Aitken, C. E. & Puglisi, J. D. (2009). GTP hydrolysis by IF2 guides progression of the ribosome into elongation. Molecular Cell 35, 37–47.Google Scholar
Marshall, R. A., Dorywalska, M. & Puglisi, J. D. (2008). Irreversible chemical steps control intersubunit dynamics during translation. Proceedings of the National Academy of Sciences of the United States of America 105, 15364–15369.Google Scholar
Marzi, S., Myasnikov, A. G., Serganov, A., Ehresmann, C., Romby, P., Yusupov, M. & Klaholz, B. P. (2007). Structured mRNAs regulate translation initiation by binding to the platform of the ribosome. Cell 130, 1019–1031.Google Scholar
Masuda, T., Petrov, A. N., Iizuka, R., Funatsu, T., Puglisi, J. D. & Uemura, S. (2012). Initiation factor 2, tRNA, and 50S subunits cooperatively stabilize mRNAs on the ribosome during initiation. Proceedings of the National Academy of Sciences of the United States of America 109, 4881–4885.Google Scholar
Mathews, M. B. & Hershey, J. W. (2015). The translation factor eIF5A and human cancer. Biochimica et Biophysica Acta 1849, 836–844.Google Scholar
Matsuo, H., Li, H., Mcguire, A. M., Fletcher, C. M., Gingras, A. C., Sonenberg, N. & Wagner, G. (1997). Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nature Structural Biology 4, 717–724.Google Scholar
Mccarthy, J. E. (1998). Posttranscriptional control of gene expression in yeast. Microbiology and Molecular Biology Reviews 62, 1492–1553.Google Scholar
Melnikov, S., Ben-Shem, A., Garreau de Loubresse, N., Jenner, L., Yusupova, G. & Yusupov, M. (2012). One core, two shells: bacterial and eukaryotic ribosomes. Nature Structural & Molecular Biology 19, 560–567.Google Scholar
Merrick, W. C. (2015). eIF4F: a retrospective. The Journal of Biological Chemistry 290, 24091–24099.Google Scholar
Meyer, K. D., Saletore, Y., Zumbo, P., Elemento, O., Mason, C. E. & Jaffrey, S. R. (2012). Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell 149, 1635–1646.Google Scholar
Milon, P., Maracci, C., Filonava, L., Gualerzi, C. O. & Rodnina, M. V. (2012). Real-time assembly landscape of bacterial 30S translation initiation complex. Nature Structural & Molecular Biology 19, 609–615.Google Scholar
Milon, P. & Rodnina, M. V. (2012). Kinetic control of translation initiation in bacteria. Critical Reviews in Biochemistry and Molecular Biology 47, 334–348.Google Scholar
Mitarai, N., Sneppen, K. & Pedersen, S. (2008). Ribosome collisions and translation efficiency: optimization by codon usage and mRNA destabilization. Journal of Molecular Biology 382, 236–245.Google Scholar
Mitchell, S. F., Walker, S. E., Algire, M. A., Park, E. H., Hinnebusch, A. G. & Lorsch, J. R. (2010). The 5′−7-methylguanosine cap on eukaryotic mRNAs serves both to stimulate canonical translation initiation and to block an alternative pathway. Molecular Cell 39, 950–962.Google Scholar
Mittermaier, A. & Kay, L. E. (2006). New tools provide new insights in NMR studies of protein dynamics. Science 312, 224–228.Google Scholar
Moerke, N. J., Aktas, H., Chen, H., Cantel, S., Reibarkh, M. Y., Fahmy, A., Gross, J. D., Degterev, A., Yuan, J., Chorev, M., Halperin, J. A. & Wagner, G. (2007). Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128, 257–267.Google Scholar
Moll, I., Grill, S., Gualerzi, C. O. & Blasi, U. (2002). Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Molecular Microbiology 43, 239–246.Google Scholar
Moore, S. D. & Sauer, R. T. (2007). The tmRNA system for translational surveillance and ribosome rescue. Annual Review of Biochemistry 76, 101–124.Google Scholar
Morino, S., Imataka, H., Svitkin, Y. V., Pestova, T. V. & Sonenberg, N. (2000). Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Molecular and Cellular Biology 20, 468–477.Google Scholar
Muhs, M., Hilal, T., Mielke, T., Skabkin, M. A., Sanbonmatsu, K. Y., Pestova, T. V. & Spahn, C. M. (2015). Cryo-EM of ribosomal 80S complexes with termination factors reveals the translocated cricket paralysis virus IRES. Molecular Cell 57, 422–432.Google Scholar
Munro, J. B., Altman, R. B., O'CONNOR, N. & Blanchard, S. C. (2007). Identification of two distinct hybrid state intermediates on the ribosome. Molecular Cell 25, 505–517.Google Scholar
Munro, J. B., Altman, R. B., Tung, C. S., Sanbonmatsu, K. Y. & Blanchard, S. C. (2010a). A fast dynamic mode of the EF-G-bound ribosome. The EMBO Journal 29, 770–781.Google Scholar
Munro, J. B., Sanbonmatsu, K. Y., Spahn, C. M. & Blanchard, S. C. (2009). Navigating the ribosome's metastable energy landscape. Trends in Biochemical Sciences 34, 390–400.Google Scholar
Munro, J. B., Wasserman, M. R., Altman, R. B., Wang, L. & Blanchard, S. C. (2010b). Correlated conformational events in EF-G and the ribosome regulate translocation. Nature Structural & Molecular Biology 17, 1470–1477.Google Scholar
Myasnikov, A. G., Afonina, Z. A., Menetret, J. F., Shirokov, V. A., Spirin, A. S. & Klaholz, B. P. (2014). The molecular structure of the left-handed supra-molecular helix of eukaryotic polyribosomes. Nat Communications 5, 5294.Google Scholar
Nakamura, Y., Ito, K. & Isaksson, L. A. (1996). Emerging understanding of translation termination. Cell 87, 147–150.Google Scholar
Namy, O., Moran, S. J., Stuart, D. I., Gilbert, R. J. & Brierley, I. (2006). A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting. Nature 441, 244–247.Google Scholar
Nanda, J. S., Saini, A. K., Munoz, A. M., Hinnebusch, A. G. & Lorsch, J. R. (2013). Coordinated movements of eukaryotic translation initiation factors eIF1, eIF1A, and eIF5 trigger phosphate release from eIF2 in response to start codon recognition by the ribosomal preinitiation complex. The Journal of Biological Chemistry 288, 5316–5329.Google Scholar
Neff, C. L. & Sachs, A. B. (1999). Eukaryotic translation initiation factors 4 G and 4A from Saccharomyces cerevisiae interact physically and functionally. Molecular and Cellular Biology 19, 5557–5564.Google Scholar
Niederberger, N., Trachsel, H. & Altmann, M. (1998). The RNA recognition motif of yeast translation initiation factor Tif3/eIF4B is required but not sufficient for RNA strand-exchange and translational activity. RNA 4, 1259–1267.CrossRefGoogle Scholar
Niedzwiecka, A., Marcotrigiano, J., Stepinski, J., Jankowska-Anyszka, M., Wyslouch-Cieszynska, A., Dadlez, M., Gingras, A. C., Mak, P., Darzynkiewicz, E., Sonenberg, N., Burley, S. K. & Stolarski, R. (2002). Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 5′ cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins. Journal of Molecular Biology 319, 615–635.Google Scholar
Nierhaus, K. H. (1990). The allosteric three-site model for the ribosomal elongation cycle: features and future. Biochemistry 29, 4997–5008.Google Scholar
Nilsen, T. W. (2014). Molecular biology. Internal mRNA methylation finally finds functions. Science 343, 1207–1208.Google Scholar
Ninio, J. (1975). Kinetic amplification of enzyme discrimination. Biochimie 57, 587–595.Google Scholar
Niu, Y., Zhao, X., Wu, Y. S., Li, M. M., Wang, X. J. & Yang, Y. G. (2013). N6-methyl-adenosine (m6A) in RNA: an old modification with a novel epigenetic function. Genomics, Proteomics & Bioinformatics 11, 8–17.Google Scholar
Noriega, T. R., Chen, J., Walter, P. & Puglisi, J. D. (2014a). Real-time observation of signal recognition particle binding to actively translating ribosomes. eLife 3, e04418.Google Scholar
Noriega, T. R., Tsai, A., Elvekrog, M. M., Petrov, A., Neher, S. B., Chen, J., Bradshaw, N., Puglisi, J. D. & Walter, P. (2014b). Signal recognition particle-ribosome binding is sensitive to nascent chain length. The Journal of Biological Chemistry 289, 19294–19305.Google Scholar
Nosek, J., Tomaska, L., Burger, G. & Lang, B. F. (2015). Programmed translational bypassing elements in mitochondria: structure, mobility, and evolutionary origin. Trends in Genetics 31, 187–194.Google Scholar
O'Leary, S. E., Petrov, A., Chen, J. & Puglisi, J. D. (2013). Dynamic recognition of the mRNA cap by Saccharomyces cerevisiae eIF4E. Structure 21, 2197–2207.Google Scholar
Oberer, M., Marintchev, A. & Wagner, G. (2005). Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes & Development 19, 2212–2223.Google Scholar
Ogle, J. M., Brodersen, D. E., Clemons, W. M. Jr., Tarry, M. J., Carter, A. P. & Ramakrishnan, V. (2001). Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292, 897–902.Google Scholar
Oliveira, C. C., van den Heuvel, J. J. & Mccarthy, J. E. (1993). Inhibition of translational initiation in Saccharomyces cerevisiae by secondary structure: the roles of the stability and position of stem-loops in the mRNA leader. Molecular Microbiology 9, 521–532.Google Scholar
Otero, L. J., Ashe, M. P. & Sachs, A. B. (1999). The yeast poly(A)-binding protein Pab1p stimulates in vitro poly(A)-dependent and cap-dependent translation by distinct mechanisms. The EMBO Journal 18, 3153–3163.Google Scholar
Ozes, A. R., Feoktistova, K., Avanzino, B. C. & Fraser, C. S. (2011). Duplex unwinding and ATPase activities of the DEAD-box helicase eIF4A are coupled by eIF4G and eIF4B. Journal of Molecular Biology 412, 674–687.Google Scholar
Palmer, A. G. III (2014). Chemical exchange in biomacromolecules: past, present, and future. Journal of Magnetic Resonance 241, 3–17.Google Scholar
Pan, C., Potratz, J. P., Cannon, B., Simpson, Z. B., Ziehr, J. L., Tijerina, P. & Russell, R. (2014). DEAD-box helicase proteins disrupt RNA tertiary structure through helix capture. PLoS Biology 12, e1001981.Google Scholar
Papadopoulos, E., Jenni, S., Kabha, E., Takrouri, K. J., Yi, T., Salvi, N., Luna, R. E., Gavathiotis, E., Mahalingam, P., Arthanari, H., Rodriguez-Mias, R., Yefidoff-Freedman, R., Aktas, B. H., Chorev, M., Halperin, J. A. & Wagner, G. (2014). Structure of the eukaryotic translation initiation factor eIF4E in complex with 4EGI-1 reveals an allosteric mechanism for dissociating eIF4G. Proceedings of the National Academy of Sciences of the United States of America 111, E3187–3195.Google ScholarPubMed
Pape, T., Wintermeyer, W. & Rodnina, M. V. (1998). Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E. coli ribosome. The EMBO Journal 17, 7490–7497.Google Scholar
Park, E. H., Walker, S. E., Lee, J. M., Rothenburg, S., Lorsch, J. R. & Hinnebusch, A. G. (2011). Multiple elements in the eIF4G1 N-terminus promote assembly of eIF4G1•PABP mRNPs in vivo . The EMBO Journal 30, 302–316.Google Scholar
Park, E. H., Walker, S. E., Zhou, F., Lee, J. M., Rajagopal, V., Lorsch, J. R. & Hinnebusch, A. G. (2013). Yeast eukaryotic initiation factor 4B (eIF4B) enhances complex assembly between eIF4A and eIF4G in vivo . The Journal of Biological Chemistry 288, 2340–2354.CrossRefGoogle ScholarPubMed
Park, M. H., Nishimura, K., Zanelli, C. F. & Valentini, S. R. (2010). Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 38, 491–500.Google Scholar
Park, S., Myszka, D. G., Yu, M., Littler, S. J. & Laird-Offringa, I. A. (2000). HuD RNA recognition motifs play distinct roles in the formation of a stable complex with AU-rich RNA. Molecular and Cellular Biology 20, 4765–4772.Google Scholar
Parker, J. (1989). Errors and alternatives in reading the universal genetic code. Microbiological Reviews 53, 273–298.Google Scholar
Parsyan, A., Shahbazian, D., Martineau, Y., Petroulakis, E., Alain, T., Larsson, O., Mathonnet, G., Tettweiler, G., Hellen, C. U., Pestova, T. V., Svitkin, Y. V. & Sonenberg, N. (2009). The helicase protein DHX29 promotes translation initiation, cell proliferation, and tumorigenesis. Proceedings of the National Academy of Sciences of the United States of America 106, 22217–22222.Google Scholar
Parsyan, A., Svitkin, Y., Shahbazian, D., Gkogkas, C., Lasko, P., Merrick, W. C. & Sonenberg, N. (2011). mRNA helicases: the tacticians of translational control. Nature Reviews. Molecular Cell Biology 12, 235–245.Google Scholar
Passmore, L. A., Schmeing, T. M., Maag, D., Applefield, D. J., Acker, M. G., Algire, M. A., Lorsch, J. R. & Ramakrishnan, V. (2007). The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Molecular Cell 26, 41–50.Google Scholar
Pech, M., Karim, Z., Yamamoto, H., Kitakawa, M., Qin, Y. & Nierhaus, K. H. (2011). Elongation factor 4 (EF4/LepA) accelerates protein synthesis at increased Mg2+ concentrations. Proceedings of the National Academy of Sciences of the United States of America 108, 3199–3203.Google Scholar
Peil, L., Starosta, A. L., Lassak, J., Atkinson, G. C., Virumae, K., Spitzer, M., Tenson, T., Jung, K., Remme, J. & Wilson, D. N. (2013). Distinct XPPX sequence motifs induce ribosome stalling, which is rescued by the translation elongation factor EF-P. Proceedings of the National Academy of Sciences of the United States of America 110, 15265–15270.Google Scholar
Pelletier, J., Graff, J., Ruggero, D. & Sonenberg, N. (2015). Targeting the eIF4F translation initiation complex: a critical nexus for cancer development. Cancer Research 75, 250–263.Google Scholar
Perez, C. E. & Gonzalez, R. L. JR. (2011). In vitro and in vivo single-molecule fluorescence imaging of ribosome-catalyzed protein synthesis. Current Opinion in Chemical Biology 15, 853–863.Google Scholar
Peske, F., Kuhlenkoetter, S., Rodnina, M. V. & Wintermeyer, W. (2014). Timing of GTP binding and hydrolysis by translation termination factor RF3. Nucleic Acids Research 42, 1812–1820.Google Scholar
Peske, F., Rodnina, M. V. & Wintermeyer, W. (2005). Sequence of steps in ribosome recycling as defined by kinetic analysis. Molecular Cell 18, 403–412.Google Scholar
Pestova, T. V., Borukhov, S. I. & Hellen, C. U. (1998). Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394, 854–859.Google Scholar
Pestova, T. V., Lomakin, I. B., Lee, J. H., Choi, S. K., Dever, T. E. & Hellen, C. U. (2000). The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403, 332–335.Google Scholar
Petropoulos, A. D. & Green, R. (2012). Further in vitro exploration fails to support the “allosteric three-site model”. The Journal of Biological Chemistry 287, 11642–11648.Google Scholar
Petrov, A., Chen, J., O'Leary, S., Tsai, A. & Puglisi, J. D. (2012). Single-molecule analysis of translational dynamics. Cold Spring Harbor Perspectives in Biology 4, a011551.Google Scholar
Pisarev, A. V., Hellen, C. U. & Pestova, T. V. (2007). Recycling of eukaryotic posttermination ribosomal complexes. Cell 131, 286–299.Google Scholar
Pisarev, A. V., Kolupaeva, V. G., Yusupov, M. M., Hellen, C. U. & Pestova, T. V. (2008). Ribosomal position and contacts of mRNA in eukaryotic translation initiation complexes. The EMBO Journal 27, 1609–1621.Google Scholar
Pisarev, A. V., Skabkin, M. A., Pisareva, V. P., Skabkina, O. V., Rakotondrafara, A. M., Hentze, M. W., Hellen, C. U. & Pestova, T. V. (2010). The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Molecular Cell 37, 196–210.Google Scholar
Pisareva, V. P., Pisarev, A. V., Komar, A. A., Hellen, C. U. & Pestova, T. V. (2008). Translation initiation on mammalian mRNAs with structured 5′UTRs requires DExH-box protein DHX29. Cell 135, 1237–1250.Google Scholar
Prat, A., Schmid, S. R., Buser, P., Blum, S., Trachsel, H., Nielsen, P. J. & Linder, P. (1990). Expression of translation initiation factor 4A from yeast and mouse in Saccharomyces cerevisiae . Biochimica et Biophysica Acta 1050, 140–145.Google Scholar
Precup, J., Ulrich, A. K., Roopnarine, O. & Parker, J. (1989). Context specific misreading of phenylalanine codons. Molecular and General Genetics 218, 397–401.Google Scholar
Ptushkina, M., von der Haar, T., Karim, M. M., Hughes, J. M. & Mccarthy, J. E. (1999). Repressor binding to a dorsal regulatory site traps human eIF4E in a high cap-affinity state. The EMBO Journal 18, 4068–4075.Google Scholar
Ptushkina, M., von der Haar, T., Vasilescu, S., Frank, R., Birkenhager, R. & Mccarthy, J. E. (1998). Cooperative modulation by eIF4G of eIF4E-binding to the mRNA 5′ cap in yeast involves a site partially shared by p20. The EMBO Journal 17, 4798–4808.Google Scholar
Pulk, A. & Cate, J. H. (2013). Control of ribosomal subunit rotation by elongation factor G. Science 340, 1235970.Google Scholar
Qin, P., Yu, D., Zuo, X. & Cornish, P. V. (2014). Structured mRNA induces the ribosome into a hyper-rotated state. EMBO Reports 15, 185–190.Google Scholar
Qu, X., Wen, J. D., Lancaster, L., Noller, H. F., Bustamante, C. & Tinoco, I. Jr. (2011). The ribosome uses two active mechanisms to unwind messenger RNA during translation. Nature 475, 118–121.Google Scholar
Rabl, J., Leibundgut, M., Ataide, S. F., Haag, A. & Ban, N. (2011). Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science 331, 730–736.Google Scholar
Rajagopal, V., Park, E. H., Hinnebusch, A. G. & Lorsch, J. R. (2012). Specific domains in yeast translation initiation factor eIF4G strongly bias RNA unwinding activity of the eIF4F complex toward duplexes with 5′-overhangs. The Journal of Biological Chemistry 287, 20301–20312.Google Scholar
Ramrath, D. J., Yamamoto, H., Rother, K., Wittek, D., Pech, M., Mielke, T., Loerke, J., Scheerer, P., Ivanov, P., Teraoka, Y., Shpanchenko, O., Nierhaus, K. H. & Spahn, C. M. (2012). The complex of tmRNA-SmpB and EF-G on translocating ribosomes. Nature 485, 526–529.Google Scholar
Ratje, A. H., Loerke, J., Mikolajka, A., Brunner, M., Hildebrand, P. W., Starosta, A. L., Donhofer, A., Connell, S. R., Fucini, P., Mielke, T., Whitford, P. C., Onuchic, J. N., Yu, Y., Sanbonmatsu, K. Y., Hartmann, R. K., Penczek, P. A., Wilson, D. N. & Spahn, C. M. (2010). Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature 468, 713–716.Google Scholar
Ravera, E., Salmon, L., Fragai, M., Parigi, G., Al-Hashimi, H. & Luchinat, C. (2014). Insights into domain-domain motions in proteins and RNA from solution NMR. Accounts of Chemical Research 47, 3118–3126.Google Scholar
Ray, B. K., Lawson, T. G., Kramer, J. C., Cladaras, M. H., Grifo, J. A., Abramson, R. D., Merrick, W. C. & Thach, R. E. (1985). ATP-dependent unwinding of messenger RNA structure by eukaryotic initiation factors. The Journal of Biological Chemistry 260, 7651–7658.Google Scholar
Richman, N. & Bodley, J. W. (1972). Ribosomes cannot interact simultaneously with elongation factors EF Tu and EF G. Proceedings of the National Academy of Sciences of the United States of America 69, 686–689.Google Scholar
Richter, J. D. & Sonenberg, N. (2005). Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433, 477–480.Google Scholar
Richter, N. J., Rogers, G. W., Hensold, J. O. & Merrick, W. C. (1999). Further biochemical and kinetic characterization of human eukaryotic initiation factor 4H. The Journal of Biological Chemistry 274, 35415–35424.Google Scholar
Richter-Cook, N. J., Dever, T. E., Hensold, J. O. & Merrick, W. C. (1998). Purification and characterization of a new eukaryotic protein translation factor. Eukaryotic initiation factor 4H. The Journal of Biological Chemistry 273, 7579–7587.Google Scholar
Rodnina, M. V. (2012). Quality control of mRNA decoding on the bacterial ribosome. Advances in Protein Chemistry and Structural Biology 86, 95–128.Google Scholar
Rodnina, M. V. (2013). The ribosome as a versatile catalyst: reactions at the peptidyl transferase center. Current Opinion in Structural Biology 23, 595–602.Google Scholar
Rodnina, M. V., Savelsbergh, A., Katunin, V. I. & Wintermeyer, W. (1997). Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385, 37–41.Google Scholar
Rodnina, M. V., Serebryanik, A. I., Ovcharenko, G. V. & El'Skaya, A. V. (1994). ATPase strongly bound to higher eukaryotic ribosomes. European Journal of Biochemistry 225, 305–310.Google Scholar
Rodnina, M. V. & Wintermeyer, W. (2001a). Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms. Annual Review of Biochemistry 70, 415–435.Google Scholar
Rodnina, M. V. & Wintermeyer, W. (2001b). Ribosome fidelity: tRNA discrimination, proofreading and induced fit. Trends in Biochemical Sciences 26, 124–130.Google Scholar
Rogers, G. W., Lima, W. F. & Merrick, W. C. (2001a). Further characterization of the helicase activity of eIF4A. Substrate specificity. The Journal of Biological Chemistry 276, 12598–12608.Google Scholar
Rogers, G. W., Richter, N. J., Lima, W. F. & Merrick, W. C. (2001b). Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. The Journal of Biological Chemistry 276, 30914–30922.Google Scholar
Rogers, G. W., Richter, N. J. & Merrick, W. C. (1999). Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. The Journal of Biological Chemistry 274, 12236–12244.Google Scholar
Roll-Mecak, A., Cao, C., Dever, T. E. & Burley, S. K. (2000). X-ray structures of the universal translation initiation factor IF2/eIF5B: conformational changes on GDP and GTP binding. Cell 103, 781–792.Google Scholar
Roost, C., Lynch, S. R., Batista, P. J., Qu, K., Chang, H. Y. & Kool, E. T. (2015). Structure and thermodynamics of N6-methyladenosine in RNA: a spring-loaded base modification. Journal of the American Chemical Society 137, 2107–2115.Google Scholar
Rosenblum, G., Chen, C., Kaur, J., Cui, X., Zhang, H., Asahara, H., Chong, S., Smilansky, Z., Goldman, Y. E. & Cooperman, B. S. (2013). Quantifying elongation rhythm during full-length protein synthesis. Journal of the American Chemical Society 135, 11322–11329.Google Scholar
Rossi, D., Kuroshu, R., Zanelli, C. F. & Valentini, S. R. (2014). eIF5A and EF-P: two unique translation factors are now traveling the same road. Wiley Interdisciplinary Reviews, RNA 5, 209–222.Google Scholar
Roy, R., Hohng, S. & Ha, T. (2008). A practical guide to single-molecule FRET. Nature Methods 5, 507–516.Google Scholar
Rozen, F., Edery, I., Meerovitch, K., Dever, T. E., Merrick, W. C. & Sonenberg, N. (1990). Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Molecular and Cellular Biology 10, 1134–1144.Google Scholar
Rozovsky, N., Butterworth, A. C. & Moore, M. J. (2008). Interactions between eIF4AI and its accessory factors eIF4B and eIF4H. RNA 14, 2136–2148.Google Scholar
Saini, A. K., Nanda, J. S., Lorsch, J. R. & Hinnebusch, A. G. (2010). Regulatory elements in eIF1A control the fidelity of start codon selection by modulating tRNA(i)(Met) binding to the ribosome. Genes & Development 24, 97–110.Google Scholar
Saini, P., Eyler, D. E., Green, R. & Dever, T. E. (2009). Hypusine-containing protein eIF5A promotes translation elongation. Nature 459, 118–121.Google Scholar
Salmon, L., Yang, S. & Al-Hashimi, H. M. (2014). Advances in the determination of nucleic acid conformational ensembles. Annual Review of Physical Chemistry 65, 293–316.CrossRefGoogle ScholarPubMed
Samatova, E., Konevega, A. L., Wills, N. M., Atkins, J. F. & Rodnina, M. V. (2014). High-efficiency translational bypassing of non-coding nucleotides specified by mRNA structure and nascent peptide. Nature Communications 5, 4459.Google Scholar
Sander, G. (1983). Ribosomal protein L1 from Escherichia coli. Its role in the binding of tRNA to the ribosome and in elongation factor g-dependent GTP hydrolysis. The Journal of Biological Chemistry 258, 10098–10103.Google Scholar
Sarnow, P., Cevallos, R. C. & Jan, E. (2005). Takeover of host ribosomes by divergent IRES elements. Biochemical Society Transactions 33(Pt 6), 1479–1482.Google Scholar
Sartori, A., Gatz, R., Beck, F., Rigort, A., Baumeister, W. & Plitzko, J. M. (2007). Correlative microscopy: bridging the gap between fluorescence light microscopy and cryo-electron tomography. Journal of Structural Biology 160, 135–145.Google Scholar
Savelsbergh, A., Katunin, V. I., Mohr, D., Peske, F., Rodnina, M. V. & Wintermeyer, W. (2003). An elongation factor G-induced ribosome rearrangement precedes tRNA–mRNA translocation. Molecular Cell 11, 1517–1523.Google Scholar
Scheper, G. C., van Kollenburg, B., Hu, J., Luo, Y., Goss, D. J. & Proud, C. G. (2002). Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA. The Journal of Biological Chemistry 277, 3303–3309.Google Scholar
Schmeing, T. M. & Ramakrishnan, V. (2009). What recent ribosome structures have revealed about the mechanism of translation. Nature 461, 1234–1242.Google Scholar
Schmeing, T. M., Voorhees, R. M., Kelley, A. C., Gao, Y. G., Murphy, F. V. T., Weir, J. R. & Ramakrishnan, V. (2009). The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326, 688–694.Google Scholar
Schreier, M. H., Erni, B. & Staehelin, T. (1977). Initiation of mammalian protein synthesis. I. Purification and characterization of seven initiation factors. Journal of Molecular Biology 116, 727–753.Google Scholar
Schutz, P., Bumann, M., Oberholzer, A. E., Bieniossek, C., Trachsel, H., Altmann, M. & Baumann, U. (2008). Crystal structure of the yeast eIF4A–eIF4G complex: an RNA-helicase controlled by protein–protein interactions. Proceedings of the National Academy of Sciences of the United States of America 105, 9564–9569.Google Scholar
Seidelt, B., Innis, C. A., Wilson, D. N., Gartmann, M., Armache, J. P., Villa, E., Trabuco, L. G., Becker, T., Mielke, T., Schulten, K., Steitz, T. A. & Beckmann, R. (2009). Structural insight into nascent polypeptide chain-mediated translational stalling. Science 326, 1412–1415.Google Scholar
Sekiyama, N., Arthanari, H., Papadopoulos, E., Rodriguez-Mias, R. A., Wagner, G. & Léger-Abraham, M. (2015). Molecular mechanism of the dual activity of 4EGI-1: dissociating eIF4G from eIF4E but stabilizing the binding of unphosphorylated 4E-BP1. Proceedings of the National Academy of Sciences of the United States of America 112, E4036–E4045.Google Scholar
Selmer, M., Dunham, C. M., Murphy, F. V. T., Weixlbaumer, A., Petry, S., Kelley, A. C., Weir, J. R. & Ramakrishnan, V. (2006). Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313, 1935–1942.Google Scholar
Senissar, M., Saux, A. L., Belgareh-Touze, N., Adam, C., Banroques, J. & Tanner, N. K. (2014). The DEAD-box helicase Ded1 from yeast is an mRNP cap-associated protein that shuttles between the cytoplasm and nucleus. Nucleic Acids Research 42, 10005–10022.Google Scholar
Shah, P., Ding, Y., Niemczyk, M., Kudla, G. & Plotkin, J. B. (2013). Rate-limiting steps in yeast protein translation. Cell 153, 1589–1601.Google Scholar
Sharma, D. & Jankowsky, E. (2014). The Ded1/DDX3 subfamily of DEAD-box RNA helicases. Critical Reviews in Biochemistry and Molecular Biology 49, 343–360.Google Scholar
Shatkin, A. J. (1976). Capping of eucaryotic mRNAs. Cell 9(4 Pt 2), 645–653.Google Scholar
Shen, K., Arslan, S., Akopian, D., Ha, T. & Shan, S. O. (2012). Activated GTPase movement on an RNA scaffold drives co-translational protein targeting. Nature 492, 271–275.Google Scholar
Shiba, T., Mizote, H., Kaneko, T., Nakajima, T. & Kakimoto, Y. (1971). Hypusine, a new amino acid occurring in bovine brain. Isolation and structural determination. Biochimica et Biophysica Acta 244, 523–531.Google Scholar
Shih, J. W., Wang, W. T., Tsai, T. Y., Kuo, C. Y., Li, H. K. & Wu Lee, Y. H. (2012). Critical roles of RNA helicase DDX3 and its interactions with eIF4E/PABP1 in stress granule assembly and stress response. The Biochemical Journal 441, 119–129.Google Scholar
Shoemaker, C. J. & Green, R. (2011). Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast. Proceedings of the National Academy of Sciences of the United States of America 108, E1392–E1398.Google Scholar
Siddiqui, N., Tempel, W., Nedyalkova, L., Volpon, L., Wernimont, A. K., Osborne, M. J., Park, H. W. & Borden, K. L. (2012). Structural insights into the allosteric effects of 4EBP1 on the eukaryotic translation initiation factor eIF4E. Journal of Molecular Biology 415, 781–792.Google Scholar
Singh, C. R., Watanabe, R., Chowdhury, W., Hiraishi, H., Murai, M. J., Yamamoto, Y., Miles, D., Ikeda, Y., Asano, M. & Asano, K. (2012). Sequential eukaryotic translation initiation factor 5 (eIF5) binding to the charged disordered segments of eIF4G and eIF2β stabilizes the 48S preinitiation complex and promotes its shift to the initiation mode. Molecular and Cellular Biology 32, 3978–3989.Google Scholar
Siwiak, M. & Zielenkiewicz, P. (2010). A comprehensive, quantitative, and genome-wide model of translation. PLoS Computational Biology 6, e1000865.Google Scholar
Skabkin, M. A., Skabkina, O. V., Hellen, C. U. & Pestova, T. V. (2013). Reinitiation and other unconventional posttermination events during eukaryotic translation. Molecular Cell 51, 249–264.Google Scholar
Slepenkov, S. V., Darzynkiewicz, E. & Rhoads, R. E. (2006). Stopped-flow kinetic analysis of eIF4E and phosphorylated eIF4E binding to cap analogs and capped oligoribonucleotides: evidence for a one-step binding mechanism. The Journal of Biological Chemistry 281, 14927–14938.Google Scholar
Slepenkov, S. V., Korneeva, N. L. & Rhoads, R. E. (2008). Kinetic mechanism for assembly of the m7GpppG.eIF4E.eIF4G complex. The Journal of Biological Chemistry 283, 25227–25237.Google Scholar
Sokabe, M. & Fraser, C. S. (2014). Human eukaryotic initiation factor 2 (eIF2)–GTP–Met-tRNAi ternary complex and eIF3 stabilize the 43 S preinitiation complex. The Journal of Biological Chemistry 289, 31827–31836.Google Scholar
Sonenberg, N. (2008). eIF4E, the mRNA cap-binding protein: from basic discovery to translational research. Biochemistry and Cell Biology 86, 178–183.Google Scholar
Sonenberg, N., Morgan, M. A., Merrick, W. C. & Shatkin, A. J. (1978). A polypeptide in eukaryotic initiation factors that crosslinks specifically to the 5′-terminal cap in mRNA. Proceedings of the National Academy of Sciences of the United States of America 75, 4843–4847.Google Scholar
Song, H., Mugnier, P., Das, A. K., Webb, H. M., Evans, D. R., Tuite, M. F., Hemmings, B. A. & Barford, D. (2000). The crystal structure of human eukaryotic release factor eRF1 – mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100, 311–321.Google Scholar
Soto-Rifo, R., Rubilar, P. S., Limousin, T., de Breyne, S., Décimo, D. & Ohlmann, T. (2012). DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs. The EMBO Journal 31, 3745–3756.Google Scholar
Spirin, A. S. (1969). A model of the functioning ribosome: locking and unlocking of the ribosome subparticles. Cold Spring Harbor Symposia on Quantitative Biology 34, 197–207.Google Scholar
Spirin, A. S. (2009). How does a scanning ribosomal particle move along the 5′-untranslated region of eukaryotic mRNA? Brownian Ratchet model. Biochemistry 48, 10688–10692.Google Scholar
Stark, H., Rodnina, M. V., Wieden, H. J., van Heel, M. & Wintermeyer, W. (2000). Large-scale movement of elongation factor G and extensive conformational change of the ribosome during translocation. Cell 100, 301–309.Google Scholar
Sternberg, S. H., Fei, J., Prywes, N., Mcgrath, K. A. & Gonzalez, R. L. Jr. (2009). Translation factors direct intrinsic ribosome dynamics during translation termination and ribosome recycling. Nature Structural & Molecular Biology 16, 861–868.Google Scholar
Sun, Y., Atas, E., Lindqvist, L., Sonenberg, N., Pelletier, J. & Meller, A. (2012). The eukaryotic initiation factor eIF4H facilitates loop-binding, repetitive RNA unwinding by the eIF4A DEAD-box helicase. Nucleic Acids Research 40, 6199–6207.Google Scholar
Sun, Y., Atas, E., Lindqvist, L. M., Sonenberg, N., Pelletier, J. & Meller, A. (2014). Single-molecule kinetics of the eukaryotic initiation factor 4AI upon RNA unwinding. Structure 22, 941–948.Google Scholar
Svidritskiy, E., Brilot, A. F., Koh, C. S., Grigorieff, N. & Korostelev, A. A. (2014). Structures of yeast 80S ribosome-tRNA complexes in the rotated and nonrotated conformations. Structure 22, 1210–1218.Google Scholar
Svitkin, Y. V., Pause, A., Haghighat, A., Pyronnet, S., Witherell, G., Belsham, G. J. & Sonenberg, N. (2001). The requirement for eukaryotic initiation factor 4A (elF4A) in translation is in direct proportion to the degree of mRNA 5′ secondary structure. RNA 7, 382–394.Google Scholar
Tait, S., Dutta, K., Cowburn, D., Warwicker, J., Doig, A. J. & Mccarthy, J. E. (2010). Local control of a disorder–order transition in 4E-BP1 underpins regulation of translation via eIF4E. Proceedings of the National Academy of Sciences of the United States of America 107, 17627–17632.Google Scholar
Takyar, S., Hickerson, R. P. & Noller, H. F. (2005). mRNA helicase activity of the ribosome. Cell 120, 49–58.Google Scholar
Tang, M., Comellas, G. & Rienstra, C. M. (2013). Advanced solid-state NMR approaches for structure determination of membrane proteins and amyloid fibrils. Accounts of Chemical Research 46, 2080–2088.Google Scholar
Tarn, W. Y. & Chang, T. H. (2009). The current understanding of Ded1p/DDX3 homologs from yeast to human. RNA Biology 6, 17–20.Google Scholar
Tarun, S. Z. & Sachs, A. B. (1996). Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. The EMBO Journal 15, 7168–7177.Google Scholar
Taylor, D., Unbehaun, A., Li, W., Das, S., Lei, J., Liao, H. Y., Grassucci, R. A., Pestova, T. V. & Frank, J. (2012). Cryo-EM structure of the mammalian eukaryotic release factor eRF1–eRF3-associated termination complex. Proceedings of the National Academy of Sciences of the United States of America 109, 18413–18418.Google Scholar
Taylor, D. J., Nilsson, J., Merrill, A. R., Andersen, G. R., Nissen, P. & Frank, J. (2007). Structures of modified eEF2 80S ribosome complexes reveal the role of GTP hydrolysis in translocation. The EMBO Journal 26, 2421–2431.Google Scholar
Thomas, A., Goumans, H., Voorma, H. O. & Benne, R. (1980a). The mechanism of action of eukaryotic initiation factor 4C in protein synthesis. European Journal of Biochemistry 107, 39–45.Google Scholar
Thomas, A., Spaan, W., van Steeg, H., Voorma, H. O. & Benne, R. (1980b). Mode of action of protein synthesis initiation factor eIF-1 from rabbit reticulocytes. FEBS Letters 116, 67–71.Google Scholar
Tinoco, I. Jr. Kim, H. K. & Yan, S. (2013). Frameshifting dynamics. Biopolymers 99, 1147–1166.Google Scholar
Todd, G. C. & Walter, N. G. (2013). Secondary structure of bacteriophage T4 gene 60 mRNA: implications for translational bypassing. RNA 19, 685–700.Google Scholar
Tomoo, K., Matsushita, Y., Fujisaki, H., Abiko, F., Shen, X., Taniguchi, T., Miyagawa, H., Kitamura, K., Miura, K. & Ishida, T. (2005). Structural basis for mRNA Cap-Binding regulation of eukaryotic initiation factor 4E by 4E-binding protein, studied by spectroscopic, X-ray crystal structural, and molecular dynamics simulation methods. Biochimica et Biophysica Acta 1753, 191–208.Google Scholar
Tomoo, K., Shen, X., Okabe, K., Nozoe, Y., Fukuhara, S., Morino, S., Ishida, T., Taniguchi, T., Hasegawa, H., Terashima, A., Sasaki, M., Katsuya, Y., Kitamura, K., Miyoshi, H., Ishikawa, M. & Miura, K. (2002). Crystal structures of 7-methylguanosine 5′-triphosphate (m(7)GTP)- and P(1)-7-methylguanosine-P(3)-adenosine-5′,5′-triphosphate (m(7)GpppA)-bound human full-length eukaryotic initiation factor 4E: biological importance of the C-terminal flexible region. The Biochemical Journal 362(Pt 3), 539–544.Google Scholar
Tong, Y., Park, I., Hong, B. S., Nedyalkova, L., Tempel, W. & Park, H. W. (2009). Crystal structure of human eIF5A1: insight into functional similarity of human eIF5A1 and eIF5A2. Proteins 75, 1040–1045.Google Scholar
Topisirovic, I., Svitkin, Y. V., Sonenberg, N. & Shatkin, A. J. (2011). Cap and cap-binding proteins in the control of gene expression. Wiley Interdisciplinary Reviews, RNA 2, 277–298.Google Scholar
Toprak, E., Kural, C. & Selvin, P. R. (2010). Super-accuracy and super-resolution getting around the diffraction limit. Methods Enzymol 475, 1–26.Google Scholar
Tourigny, D. S., Fernandez, I. S., Kelley, A. C. & Ramakrishnan, V. (2013). Elongation factor G bound to the ribosome in an intermediate state of translocation. Science 340, 1235490.Google Scholar
Trabuco, L. G., Harrison, C. B., Schreiner, E. & Schulten, K. (2010). Recognition of the regulatory nascent chain TnaC by the ribosome. Structure 18, 627–637.Google Scholar
Triana-Alonso, F. J., Chakraburtty, K. & Nierhaus, K. H. (1995). The elongation factor 3 unique in higher fungi and essential for protein biosynthesis is an E site factor. The Journal of Biological Chemistry 270, 20473–20478.Google Scholar
Tsai, A., Kornberg, G., Johansson, M., Chen, J. & Puglisi, J. D. (2014). The dynamics of SecM-induced translational stalling. Cell Reports 7, 1521–1533.Google Scholar
Tsai, A., Petrov, A., Marshall, R. A., Korlach, J., Uemura, S. & Puglisi, J. D. (2012). Heterogeneous pathways and timing of factor departure during translation initiation. Nature 487, 390–393.Google Scholar
Tsai, A., Uemura, S., Johansson, M., Puglisi, E. V., Marshall, R. A., Aitken, C. E., Korlach, J., Ehrenberg, M. & Puglisi, J. D. (2013). The impact of aminoglycosides on the dynamics of translation elongation. Cell Reports 3, 497–508.Google Scholar
Tu, D., Blaha, G., Moore, P. B. & Steitz, T. A. (2005). Structures of MLSBK antibiotics bound to mutated large ribosomal subunits provide a structural explanation for resistance. Cell 121, 257–270.Google Scholar
Ude, S., Lassak, J., Starosta, A. L., Kraxenberger, T., Wilson, D. N. & Jung, K. (2013). Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science 339, 82–85.Google Scholar
Uemura, S., Aitken, C. E., Korlach, J., Flusberg, B. A., Turner, S. W. & Puglisi, J. D. (2010). Real-time tRNA transit on single translating ribosomes at codon resolution. Nature 464, 1012–1017.Google Scholar
Uemura, S., Dorywalska, M., Lee, T. H., Kim, H. D., Puglisi, J. D. & Chu, S. (2007). Peptide bond formation destabilizes Shine-Dalgarno interaction on the ribosome. Nature 446, 454–457.Google Scholar
Uemura, S., Iizuka, R., Ueno, T., Shimizu, Y., Taguchi, H., Ueda, T., Puglisi, J. D. & Funatsu, T. (2008). Single-molecule imaging of full protein synthesis by immobilized ribosomes. Nucleic Acids Research 36, e70.Google Scholar
Valásek, L. S. (2012). ‘Ribozoomin’–translation initiation from the perspective of the ribosome-bound eukaryotic initiation factors (eIFs). Current Protein & Peptide Science 13, 305–330.Google Scholar
Valiente-Echeverría, F., Hermoso, M. A. & Soto-Rifo, R. (2015). RNA helicase DDX3: at the crossroad of viral replication and antiviral immunity. Reviews in Medical Virology 25, 286–299.Google Scholar
Valle, M., Zavialov, A., Sengupta, J., Rawat, U., Ehrenberg, M. & Frank, J. (2003). Locking and unlocking of ribosomal motions. Cell 114, 123–134.Google Scholar
Vassilenko, K. S., Alekhina, O. M., Dmitriev, S. E., Shatsky, I. N. & Spirin, A. S. (2011). Unidirectional constant rate motion of the ribosomal scanning particle during eukaryotic translation initiation. Nucleic Acids Research 39, 5555–5567.Google Scholar
Vazquez-Laslop, N., Thum, C. & Mankin, A. S. (2008). Molecular mechanism of drug-dependent ribosome stalling. Molecular Cell 30, 190–202.Google Scholar
Vega Laso, M. R., Zhu, D., Sagliocco, F., Brown, A. J., Tuite, M. F. & Mccarthy, J. E. (1993). Inhibition of translational initiation in the yeast Saccharomyces cerevisiae as a function of the stability and position of hairpin structures in the mRNA leader. The Journal of Biological Chemistry 268, 6453–6462.Google Scholar
Vesper, O., Amitai, S., Belitsky, M., Byrgazov, K., Kaberdina, A. C., Engelberg-Kulka, H. & Moll, I. (2011). Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli . Cell 147, 147–157.Google Scholar
Vestergaard, B., Van, L. B., Andersen, G. R., Nyborg, J., Buckingham, R. H. & Kjeldgaard, M. (2001). Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Molecular Cell 8, 1375–1382.Google Scholar
Villa, N., Do, A., Hershey, J. W. & Fraser, C. S. (2013). Human eukaryotic initiation factor 4 G (eIF4G) protein binds to eIF3c, -d, and -e to promote mRNA recruitment to the ribosome. The Journal of Biological Chemistry 288, 32932–32940.Google Scholar
Volpon, L., Osborne, M. J., Topisirovic, I., Siddiqui, N. & Borden, K. L. (2006). Cap-free structure of eIF4E suggests a basis for conformational regulation by its ligands. The EMBO Journal 25, 5138–5149.Google Scholar
von der Haar, T., Ball, P. D. & Mccarthy, J. E. (2000). Stabilization of eukaryotic initiation factor 4E binding to the mRNA 5′-cap by domains of eIF4G. The Journal of Biological Chemistry 275, 30551–30555.Google Scholar
von der Haar, T., Oku, Y., Ptushkina, M., Moerke, N., Wagner, G., Gross, J. D. & Mccarthy, J. E. (2006). Folding transitions during assembly of the eukaryotic mRNA cap-binding complex. Journal of Molecular Biology 356, 982–992.Google Scholar
Wakiyama, M., Imataka, H. & Sonenberg, N. (2000). Interaction of eIF4 G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation. Current Biology 10, 1147–1150.Google Scholar
Walker, S. E., Zhou, F., Mitchell, S. F., Larson, V. S., Valasek, L., Hinnebusch, A. G. & Lorsch, J. R. (2013). Yeast eIF4B binds to the head of the 40S ribosomal subunit and promotes mRNA recruitment through its N-terminal and internal repeat domains. RNA 19, 191–207.Google Scholar
Wang, Y., Rader, A. J., Bahar, I. & Jernigan, R. L. (2004). Global ribosome motions revealed with elastic network model. Journal of Structural Biology 147, 302–314.Google Scholar
Weiss, R. B., Huang, W. M. & Dunn, D. M. (1990). A nascent peptide is required for ribosomal bypass of the coding gap in bacteriophage T4 gene 60. Cell 62, 117–126.Google Scholar
Weisser, M., Voigts-Hoffmann, F., Rabl, J., Leibundgut, M. & Ban, N. (2013). The crystal structure of the eukaryotic 40S ribosomal subunit in complex with eIF1 and eIF1A. Nature Structural & Molecular Biology 20, 1015–1017.Google Scholar
Weixlbaumer, A., Jin, H., Neubauer, C., Voorhees, R. M., Petry, S., Kelley, A. C. & Ramakrishnan, V. (2008). Insights into translational termination from the structure of RF2 bound to the ribosome. Science 322, 953–956.Google Scholar
Wells, S. E., Hillner, P. E., Vale, R. D. & Sachs, A. B. (1998). Circularization of mRNA by eukaryotic translation initiation factors. Molecular Cell 2, 135–140.Google Scholar
Wen, J. D., Lancaster, L., Hodges, C., Zeri, A. C., Yoshimura, S. H., Noller, H. F., Bustamante, C. & Tinoco, I. (2008). Following translation by single ribosomes one codon at a time. Nature 452, 598–603.Google Scholar
Wills, N. M., O'CONNOR, M., Nelson, C. C., Rettberg, C. C., Huang, W. M., Gesteland, R. F. & Atkins, J. F. (2008). Translational bypassing without peptidyl-tRNA anticodon scanning of coding gap mRNA. The EMBO Journal 27, 2533–2544.Google Scholar
Wilson, D. N. & Doudna Cate, J. H. (2012). The structure and function of the eukaryotic ribosome. Cold Spring Harbor Perspectives in Biology 4.Google Scholar
Wimberly, B. T., Brodersen, D. E., Clemons, W. M. Jr. Morgan-Warren, R. J., Carter, A. P., Vonrhein, C., Hartsch, T. & Ramakrishnan, V. (2000). Structure of the 30S ribosomal subunit. Nature 407, 327–339.Google Scholar
Woolstenhulme, C. J., Parajuli, S., Healey, D. W., Valverde, D. P., Petersen, E. N., Starosta, A. L., Guydosh, N. R., Johnson, W. E., Wilson, D. N. & Buskirk, A. R. (2013). Nascent peptides that block protein synthesis in bacteria. Proceedings of the National Academy of Sciences of the United States of America 110, E878–E887.Google Scholar
Xue, S. & Barna, M. (2012). Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nature Reviews. Molecular Cell Biology 13, 355–369.Google Scholar
Yamamoto, H., Collier, M., Loerke, J., Ismer, J., Schmidt, A., Hilal, T., Sprink, T., Yamamoto, K., Mielke, T., Bürger, J., Shaikh, T. R., Dabrowski, M., Hildebrand, P. W., Scheerer, P. & Spahn, C. M. (2015). Molecular architecture of the ribosome-bound Hepatitis C virus internal ribosomal entry site RNA. The EMBO Journal 34, 3042–3058.Google Scholar
Yamamoto, H., Unbehaun, A., Loerke, J., Behrmann, E., Collier, M., Bürger, J., Mielke, T. & Spahn, C. M. (2014). Structure of the mammalian 80S initiation complex with initiation factor 5B on HCV-IRES RNA. Nature Structural & Molecular Biology 21, 721–727.Google Scholar
Yanagiya, A., Svitkin, Y. V., Shibata, S., Mikami, S., Imataka, H. & Sonenberg, N. (2009). Requirement of RNA binding of mammalian eukaryotic translation initiation factor 4GI (eIF4GI) for efficient interaction of eIF4E with the mRNA cap. Molecular and Cellular Biology 29, 1661–1669.Google Scholar
Yang, J. R., Chen, X. & Zhang, J. (2014). Codon-by-codon modulation of translational speed and accuracy via mRNA folding. PLoS Biology 12, e1001910.Google Scholar
Yang, Q., del Campo, M., Lambowitz, A. M. & Jankowsky, E. (2007). DEAD-box proteins unwind duplexes by local strand separation. Molecular Cell 28, 253–263.Google Scholar
Yang, Q. & Jankowsky, E. (2006). The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases. Nature Structural & Molecular Biology 13, 981–986.Google Scholar
Yao, L., Li, Y., Tsai, T. W., Xu, S. & Wang, Y. (2013). Noninvasive measurement of the mechanical force generated by motor protein EF-G during ribosome translocation. Angewandte Chemie (International ed. in English) 52, 14041–14044.Google Scholar
Yildiz, A., Forkey, J. N., Mckinney, S. A., Ha, T., Goldman, Y. E. & Selvin, P. R. (2003). Myosin V walks hand-over-hand: single fluorophore imaging with 1·5-nm localization. Science 300, 2061–2065.Google Scholar
Young, R. & Bremer, H. (1976). Polypeptide-chain-elongation rate in Escherichia coli B/r as a function of growth rate. The Biochemical Journal 160, 185–194.Google Scholar
Yu, Y., Marintchev, A., Kolupaeva, V. G., Unbehaun, A., Veryasova, T., Lai, S. C., Hong, P., Wagner, G., Hellen, C. U. & Pestova, T. V. (2009). Position of eukaryotic translation initiation factor eIF1A on the 40S ribosomal subunit mapped by directed hydroxyl radical probing. Nucleic Acids Research 37, 5167–5182.Google Scholar
Yusupov, M. M., Yusupova, G. Z., Baucom, A., Lieberman, K., Earnest, T. N., Cate, J. H. & Noller, H. F. (2001). Crystal structure of the ribosome at 5·5 A resolution. Science 292, 883–896.Google Scholar
Yusupova, G. Z., Yusupov, M. M., Cate, J. H. & Noller, H. F. (2001). The path of messenger RNA through the ribosome. Cell 106, 233–241.Google Scholar
Zaher, H. S. & Green, R. (2009). Fidelity at the molecular level: lessons from protein synthesis. Cell 136, 746–762.Google Scholar
Zanelli, C. F., Maragno, A. L., Gregio, A. P., Komili, S., Pandolfi, J. R., Mestriner, C. A., Lustri, W. R. & Valentini, S. R. (2006). eIF5A binds to translational machinery components and affects translation in yeast. Biochemical and Biophysical Research Communications 348, 1358–1366.Google Scholar
Zavialov, A. V., Buckingham, R. H. & Ehrenberg, M. (2001). A posttermination ribosomal complex is the guanine nucleotide exchange factor for peptide release factor RF3. Cell 107, 115–124.Google Scholar
Zavialov, A. V. & Ehrenberg, M. (2003). Peptidyl-tRNA regulates the GTPase activity of translation factors. Cell 114, 113–122.Google Scholar
Zavialov, A. V., Mora, L., Buckingham, R. H. & Ehrenberg, M. (2002). Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3. Molecular Cell 10, 789–798.Google Scholar
Zeng, X., Chugh, J., Casiano-Negroni, A., Al-Hashimi, H. M. & Brooks, C. L. III (2014). Flipping of the ribosomal A-site adenines provides a basis for tRNA selection. Journal of Molecular Biology 426, 3201–3213.Google Scholar
Zhang, F., Saini, A. K., Shin, B. S., Nanda, J. & Hinnebusch, A. G. (2015). Conformational changes in the P site and mRNA entry channel evoked by AUG recognition in yeast translation preinitiation complexes. Nucleic Acids Research 43, 2293–2312.Google Scholar
Zhang, W., Dunkle, J. A. & Cate, J. H. (2009). Structures of the ribosome in intermediate states of ratcheting. Science 325, 1014–1017.Google Scholar
Zhou, F., Walker, S. E., Mitchell, S. F., Lorsch, J. R. & Hinnebusch, A. G. (2014). Identification and characterization of functionally critical, conserved motifs in the internal repeats and N-terminal domain of yeast translation initiation factor 4B (yeIF4B). The Journal of Biological Chemistry 289, 1704–1722.Google Scholar
Zhou, J., Lancaster, L., Donohue, J. P. & Noller, H. F. (2013). Crystal structures of EF-G-ribosome complexes trapped in intermediate states of translocation. Science 340, 1236086.Google Scholar
Zhouravleva, G., Frolova, L., le Goff, X., le Guellec, R., Inge-Vechtomov, S., Kisselev, L. & Philippe, M. (1995). Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. The EMBO Journal 14, 4065–4072.Google Scholar
Zuk, D. & Jacobson, A. (1998). A single amino acid substitution in yeast eIF-5A results in mRNA stabilization. The EMBO Journal 17, 2914–2925.Google Scholar