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Regulation of Ribosomal Protein Synthesis in Prokaryotes

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Abstract

Protein synthesis on ribosomes is considered the main process in cell life. Regulation of ribosomal protein gene expression plays an important role in the balanced synthesis of proteins and RNA in ribosomal biogenesis. This review is focused on some features of autoregulation of ribosomal protein synthesis in prokaryotes. Inhibition of the synthesis of ribosomal proteins encoded by 12 operons by mechanisms of competition , “entrapment”, and retroregulation are discussed. Examples of regulation of protein synthesis by individual ribosomal proteins and their complexes are presented.

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REFERENCES

  1. Zengel J.M., Lindahl L. 1994. Diverse mechanisms for regulating ribosomal protein synthesis in Escherichia coli. Prog. Nucleic Acids Res. Mol. Biol. 47, 331–370.

    CAS  Google Scholar 

  2. Zengel J.M., Mueckl D., Lindahl L. 1980. Protein L4 of the E. coli ribosome regulates an eleven gene r protein operon. Cell. 21 (2), 523–535.

    CAS  PubMed  Google Scholar 

  3. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., Cate J.H. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science. 310 (5749), 827–834.

    CAS  PubMed  Google Scholar 

  4. Li X., Lindahl L., Zengel J.M. 1996. Ribosomal protein L4 from Escherichia coli utilizes nonidentical determinants for its structural and regulatory functions. RNA. 2 (1), 24–37.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Stelzl U., Zengel J.M., Tovbina M., Walker M., Nierhaus K.H., Lindahl L., Patel D.J. 2003. RNA-structural mimicry in Escherichia coli ribosomal protein L4-dependent regulation of the S10 operon. J. Biol. Chem. 278 (30), 28237–28245.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Stelzl U., Nierhaus K.H. 2001. A short fragment of 23S rRNA containing the binding sites for two ribosomal proteins, L24 and L4, is a key element for rRNA folding during early assembly. RNA. 7 (4), 598–609.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Freedman L.P., Zengel J.M., Archer R.H., Lindahl L. 1987. Autogenous control of the S10 ribosomal protein operon of Escherichia coli: Genetic dissection of transcriptional and posttranscriptional regulation. Proc. Natl. Acad. Sci. U. S. A. 84 (18), 6516–6520.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Zengel J.M., Lindahl L. 1990. Escherichia coli ribosomal protein L4 stimulates transcription termination at a specific site in the leader of the S10 operon independent of L4-mediated inhibition of translation. J. Mol. Biol. 213 (1), 67–78.

    CAS  PubMed  Google Scholar 

  9. Zengel J.M., Lindahl L. 1996. A hairpin structure upstream of the terminator hairpin required for ribosomal protein L4-mediated attenuation control of the S10 operon of Escherichia coli J. Bacteriol. 178 (8), 2383–2387.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Sha Y., Lindahl L., Zengel J.M. 1995. RNA determinants required for L4-mediated attenuation control of the S10 r-protein operon of Escherichia coli. J. Mol. Biol. 245 (5), 486–498.

    CAS  PubMed  Google Scholar 

  11. Fu Y., Deiorio-Haggar K., Anthony J., Meyer M.M. 2013. Most RNAs regulating ribosomal protein biosynthesis in Escherichia coli are narrowly distributed to Gammaproteobacteria. Nucleic Acids Res. 41 (6), 3491–3503.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Zengel J.M., Sha Y., Lindahl L. 2002. Surprising flexibility of leader RNA determinants for r-protein L4-mediated transcription termination in the Escherichia coli S10 operon. RNA. 8 (5), 572–578.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Zengel J.M., Lindahl L. 1990. Ribosomal protein L4 stimulates in vitro termination of transcription at a NusA-dependent terminator in the S10 operon leader. Proc. Natl. Acad. Sci. U. S. A. 87 (7), 2675–2679.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Zengel J.M., Lindahl L. 1992. Ribosomal protein L4 and transcription factor NusA have separable roles in mediating terminating of transcription within the leader of the S10 operon of Escherichia coli. Genes Dev. 6 (12B), 2655–2662.

    CAS  PubMed  Google Scholar 

  15. Sha Y., Lindahl L., Zengel J.M. 1995. Role of NusA in L4-mediated attenuation control of the S10 r-protein operon of Escherichia coli. J. Mol. Biol. 245 (5), 474–485.

    CAS  PubMed  Google Scholar 

  16. Mikhailina A.O., Kostareva O.S., Sarskikh A.V., Fedorov R.V., Pindl V., Garber M.B., Tishchenko S.V. 2014. Investigation of the regulatory function of archaeal ribosomal protein L4. Biochemistry (Moscow). 79 (1), 69–76.

    Google Scholar 

  17. Williams K.P. 2008. Strong mimicry of an rRNA binding site for two proteins by the mRNA encoding both proteins. RNA Biol. 5 (3), 145–148.

    CAS  PubMed  Google Scholar 

  18. Yates J.L., Arfsten A.E., Nomura M. 1980. In vitro expression of Escherichia coli ribosomal protein genes: Autogenous inhibition of translation. Proc. Natl. Acad. Sci. U. S. A. 77 (4), 1837–1841.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Dean D., Nomura M. 1980. Feedback regulation of ribosomal protein gene expression in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 77 (6), 3590–3594.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Brot N., Caldwell P., Weissbach H. 1981. Regulation of synthesis of Escherichia coli ribosomal proteins L1 and L11. Arch. Biochem. Biophys. 206 (1), 51–53.

    CAS  PubMed  Google Scholar 

  21. Kohrer C., Mayer C., Neumair O., Grobner P., Piendl W. 1998. Interaction of ribosomal L1 proteins from mesophilic and thermophilic archaea and bacteria with specific L1-binding sites on 23S rRNA and mRNA. Eur. J. Biochem. 256 (1), 97–105.

    CAS  PubMed  Google Scholar 

  22. Hanner M., Mayer C., Köhrer C., Golderer G., Gröbner P., Piendl W. 1994. Autogenous translational regulation of the ribosomal MvaL1 operon in the archaebacterium Methanococcus vannielii. J. Bacteriol. 176 (2), 409–418.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Yates J.L., Dean D., Strycharz W.A., Nomura M. 1981. E. coli ribosomal protein L10 inhibits translation of L10 and L7/L12 mRNAs by acting at a single site. Nature. 294 (5837), 190–192.

    CAS  PubMed  Google Scholar 

  24. Baughman G., Nomura M. 1983. Localization of the target site for translational regulation of the L11 operon and direct evidence for translational coupling in Escherichia coli. Cell. 34 (3), 979–988.

    CAS  PubMed  Google Scholar 

  25. Mayer C., Kohrer C., Grobner P., Piendel W. 1998. MvaL1 autoregulates the synthesis of the three ribosomal proteins encoded on the MvaL1 operon of the archaeon Methanococcus vannielii by inhibiting its own translation before or at the formation of the first peptide bond. Mol. Microbiol. 27 (2), 455–468.

    CAS  PubMed  Google Scholar 

  26. Mikhailina A.O., Kostareva O.S., Nikonova E.Yu., Garber M.B., Tishchenko S.V. 2018. Identification of L1-binding sites in Thermus thermophilus and Thermotoga maritime mRNAs. Mol. Biol. (Moscow). 52 (1), 84–90.

  27. Zimmermann R.A., Thurlow D.L., Finn R.S., Marsch T.L., Ferret L.K. 1980. Genetics and evolution of RNA polymerase, tRNA and ribosomes. Univ. Tokyo Press, Tokyo. 1, 569–584.

  28. Gourse R.L., Thurlow D.L., Gerbi S.A., Zimmermenn R.A. 1981. Specific binding of a procaryot ribosomal protein to an eukaryotic ribosomal RNA: Implications for evolution and autoregulation. Proc. Natl. Acad. Sci. U. S. A. 78 (5), 2722–2726.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Draper D.E. 1989. How do proteins recognize specific RNA sites? New clues from autogenously regulated ribosomal proteins. Trends Biochem. Sci. 14 (8), 335–338.

    CAS  PubMed  Google Scholar 

  30. Baier G., Hohenwarter O., Hofbauer C., Hummel H., Stoffler-Mailicke M., Stoffler G. 1989. Structural and functional equivalence between ribosomal proteins of Escherichia coli L1 and Methanococcus vannielii L6. Syst. Appl. Microbiol. 12, 119–126.

    CAS  Google Scholar 

  31. Korepanov A.P., Kostareva O.S., Bazhenova M.V., Bubunenko M.G., Garber M.B., Tishchenko S.V. 2015. Studying the properties of domain I of the ribosomal protein L1: incorporation into ribosome and regulation of the L1 operon expression. Protein J. 34 (2), 103–110.

    CAS  PubMed  Google Scholar 

  32. Nevskaya N., Tishchenko S., Volchkov S., Kljastorny V., Nikonova E., Nikonov O., Nikulin A., Kohrer C., Piendl W., Zimmermann R., Stockley, P., Garber, M., Nikonov S. 2006. New insights into the interaction of ribosomal protein L1 with RNA. J. Mol. Biol. 355 (4), 747–759.

    CAS  PubMed  Google Scholar 

  33. Tishchenko S., Gabdulkhakov A., Nevskaya N., Sarskikh A., Kostareva O., Nikonova E., Sycheva A., Moshkovskii S., Garber M., Nikonov S. 2012. High-resolution crystal structure of the isolated ribosomal L1 stalk. Acta Crystallogr. D. 68 (8), 1051–1057.

    CAS  PubMed  Google Scholar 

  34. Gabdulkhakov A., Tishchenko S., Mikhaylina A., Garber M., Nevskaya N., Nikonov S. 2017. Crystal structure of the 23S rRNA fragment specific to r-protein L1 and designed model of the ribosomal L1 stalk from Haloarcula marismortui. Crystals. 7 (2), 37.

    Google Scholar 

  35. Boni I.V., Artamonova V.S., Tzareva N.V., Dreyfus M. 2001. Non-canonical mechanism for translational control in bacteria: synthesis of ribosomal protein S1. EMBO J. 20 (15), 4222–4232.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Boni I.V., Artamonova V.S., Dreyfus M. 2000. The last RNA binding repeat of the Escherichia coli ribosomal protein S1 is specifically involved in autogenous control. J. Bacteriol. 182 (20), 5872–5879.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Sengupta J., Agrawal R.K., Frank J. 2001. Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA. Proc. Natl. Acad. Sci. U. S. A. 98 (21), 11991–11996.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Byrgazov K., Manoharadas S., Kaberdina A.C., Vesper O., Moll I. 2012. Direct interaction of the N-terminal domain of ribosomal protein S1 with protein S2 in Escherichia coli. PLoS One. 7, e32702. https://doi.org/10.1371journal.pone.0032702

  39. Sukhodolets M.V., Garges S., Adhya S. 2006. Ribosomal protein S1 promotes transcriptional cycling. RNA. 12 (8), 1505–1513.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Demo G., Rasouly A., Vasilyev N., Svetlov V., Loveland A.B., Diaz-Avalos R., Grigorieff N., Nudler E., Korostelev A.A. 2017. Structure of RNA polymerase bound to ribosomal 30S subunit. eLife. 6, e28560. https://doi.org/10.7554/eLife.28560

    Article  PubMed  PubMed Central  Google Scholar 

  41. Sorensen M.A., Fricke J., Pedersen S. 1998. Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. J. Mol. Biol. 280 (4), 561–569.

    CAS  PubMed  Google Scholar 

  42. Duval M., Korepanov A., Fuchsbauer O., Fechter P., Haller A., Fabbretti A., Choulier L., Micura R., Klaholz B.P., Romby P. 2013. Escherichia coli ribosomal protein S1 unfolds structured mRNAs onto the ribosome for active translation initiation. PLoS Biol. 11 (12), e1001731.

    PubMed  PubMed Central  Google Scholar 

  43. Lu Y., Lim L., Song J. 2017. NMR studies reveal that protein dynamics critically mediate aggregation of the well-folded and very soluble E. coli S1 ribosomal protein. bioRXiv. https://doi.org/10.1101/178459

  44. Hajnsdorf E., Boni I.V. 2012. Multiple activities of RNA-binding proteins S1 and Hfq. Biochimie. 94 (7), 1544–1553.

    CAS  PubMed  Google Scholar 

  45. Dunn J.J., Buzash-Pollert E., Studier F.W. 1978. Mutations of bacteriophage T7 that affect initiation of synthesis of the gene 0.3 protein. Proc. Natl. Acad. Sci. U. S. A. 75 (6), 2741–2745.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Aseev L.V., Levandovskaya A.A., Tchufistova L.S., Skaptsova N.V., Boni I.V. 2008. A new regulatory circuit in ribosomal protein operons: S2-mediated control of the rpsB’tsf expression in vivo. RNA. 14 (9), 1882–1894.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Yusupova G., Jenner L., Rees B., Moras D., Yusupov M. 2006. Structural basis for messenger RNA movement on the ribosome. Nature. 444 (7117), 391–394.

    CAS  PubMed  Google Scholar 

  48. Brodersen D.E., Clemons W.M., Jr., Carter A.P., Wimberly B.T., Ramakrishnan V. 2002. Crystal structure of the 30S ribosomal subunit from Thermus thermophilus: Structure of the proteins and their interactions with 16S RNA. J. Mol. Biol. 316 (3), 725–768.

    CAS  PubMed  Google Scholar 

  49. Aseev L.V., Koledinskaya L.S., Bomi I.V. 2014. Dissecting the extended “–10” Escherichia coli rpsB promoter activity and regulation in vivo. Biochemistry (Moscow). 79 (8), 776–784.

    CAS  PubMed  Google Scholar 

  50. An G., Bendiak D.S., Mamelak L.A., Friesen J.D. 1981. Organization and nucleotide sequence of a new ribosomal operon in Escherichia coli containing the genes for ribosomal protein S2 and elongation factor Ts. Nucleic Acids Res. 9 (16), 4163–4172.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Bendiak D.S., Friesen J.D. 1981. Organization of genes in the four minute region of the Escherichia coli chromosome: Evidence that rpsB and tsf are co-transcribed. Mol. Gen. Genet. 181 (3), 356–362.

    CAS  PubMed  Google Scholar 

  52. Merino E., Yanofsky C. 2005. Regulation by termination-antitermination: A genomic approach. Trends Genet. 21 (5), 260–264.

    CAS  PubMed  Google Scholar 

  53. Lesage P., Chiaruttini C., Graffe M., Dondon J., Milet M., Springer M. 1992. Messenger RNA secondary structure and translational coupling in the Escherichia coli operon encoding translation initiation factor IF3 and the ribosomal proteins, L35 and L20. J. Mol. Biol. 228 (2), 366–386.

    CAS  PubMed  Google Scholar 

  54. Spillmann S., Dohme F., Nierhaus K.H. 1977. Assembly in vitro of the 50S subunit from Escherichia coli ribosomes: Proteins essential for the first heat dependent conformational change. J. Mol. Biol. 115 (3), 513–523.

    CAS  PubMed  Google Scholar 

  55. Chiaruttini C., Milet M., Springer M. 1996. A long-range RNA-RNA interaction forms a pseudoknot required for translational control of the IF3-L35-L20 ribosomal protein operon in Escherichia coli. EMBO J. 15 (16), 4402–4413.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Allemand F., Haentjens J., Chiaruttini C., Royer C., Springer M. 2007. Escherichia coli ribosomal protein L20 binds as a single monomer to its own mRNA bearing two potential binding sites. Nucleic Acids Res. 35 (9), 3016–3031.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., Bartels H., Franceschi F., Yonath A. 2001. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell. 107 (5), 679–688.

    CAS  PubMed  Google Scholar 

  58. Guillier M., Allemand F., Raibaud S., Dardel F., Springer M., Chiaruttini C. 2002. Translational feedback regulation of the gene for L35 in Escherichia coli requires binding of ribosomal protein L20 to two sites in its leader mRNA: A possible case of ribosomal RNA-messenger RNA molecular mimicry. RNA. 8 (7), 878–889.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Haentjens-Sitri J., Allemand F., Springer M., Chiaruttini C. 2008. A competition mechanism regulates the translation of the Escherichia coli operon encoding ribosomal proteins L35 and L20. J. Mol. Biol. 375 (3), 612–625.

    CAS  PubMed  Google Scholar 

  60. Choonee N., Even S., Zig L., Putzer H. 2007. Ribosomal protein L20 controls expression of the Bacillus subtilis infC operon via a transcription attenuation mechanism. Nucleic Acids Res. 35 (5), 1578–1588.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Isono K., Kitakawa M. 1978. Cluster of ribosomal protein genes in Escherichia coli containing gene for proteins S6, S18, and L9. Proc. Natl. Acad. Sci. U. S. A. 75 (12), 6163–6167.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Held W., Ballou B., Mizushima S., Nomura M. 1974. Assembly mapping of 30 S ribosomal proteins from Escherichia coli. J. Biol. Chem. 249, 3103–3111.

    CAS  PubMed  Google Scholar 

  63. Agalarov S.C., Sridhar Prasad G., Funke P.M., Stout C.D., Williamson J.R. 2000. Structure of the S15, S6, S18-rRNA complex: Assembly of the 30S ribosome central domain. Science. 288 (5463), 107–113.

    CAS  PubMed  Google Scholar 

  64. Recht M.I., Williamson J.R. 2001. Central domain assembly: Thermodynamics and kinetics of S6 and S18 binding to an S15-RNA complex. J. Mol. Biol. 313 (1), 35–48.

    CAS  PubMed  Google Scholar 

  65. Matelska D., Purta E., Panek S., Boniecki M.J., Bujnicki J.M., Dunin-Horkawicz S. 2013. S6:S18 ribosomal protein complex interacts with a structural motif present in its own mRNA. RNA. 19 (10), 1341–1348.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Fu Y., Deiorio-Haggar K., Soo M.W., Meyer M.M. 2014. Bacterial RNA motif in the 5′ UTR of rpsF interacts with an S6:S18 complex. RNA. 20 (2), 168–176.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Babina A.M., Soo M.W., Fu Y., Meyer M.M. 2015. An S6:S18 complex inhibits translation of E. coli rpsF. RNA. 21 (12), 2039–2046.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Dennis P.P., Fiil N.P. 1979. Transcriptional and post-transcriptional control of RNA polymerase and ribosomal protein genes cloned on composite ColE1 plasmids in the bacterium Escherichia coli. J. Biol. Chem. 254 (16), 7540–7547.

    CAS  PubMed  Google Scholar 

  69. Fukuda R. 1980. Autogenous regulation of the synthesis of ribosomal proteins, L10 and L7/12, in Escherichia coli. Mol. Gen. Genet. 178 (2), 483–486.

    CAS  PubMed  Google Scholar 

  70. Brot N., Caldwell P., Weissbach H. 1980. Autogenous control of Escherichia coli ribosomal protein L10 synthesis in vitro. Proc. Natl. Acad. Sci. U. S. A. 77 (5), 2592–2595.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Holowachuk E.W., Friesen J.D., Fiil N.P. 1980. Bacteriophage lambda vehicle for the direct cloning of Escherichia coli promoter DNA sequences: Feedback regulation of the rplJL–rpoBC operon. Proc. Natl. Acad. Sci. U. S. A. 77 (4), 2124–2128.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Friesen J.I., Tropak M., An C. 1983. Mutations in the rplJ leader of Escherichia coli that abolish feedback regulation. Cell. 32 (2), 361–369.

    CAS  PubMed  Google Scholar 

  73. Shimmin L.C., Dennis P.P. 1989. Characterization of the L11, L1, L10 and L12 equivalent ribosomal protein gene cluster of the halophilic archaebacterium Halobacterium cutirubrum. EMBO J. 8 (4), 1252–1235.

    Google Scholar 

  74. Johnsen M., Christensen T., Dennis P.P., Fiil N.P. 1982. Autogenous control: ribosomal protein L10-L12 complex binds to the leader sequence of its mRNA. EMBO J. 1 (8), 999–1004.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Diaconu M., Kothe U., Schlünzen F., Fischer N., Harms J.M., Tonevitsky, Stark H., Rodnina M.V., Wahl M.C. 2005. Structural basis for the function of the ribosomal L7/L12 stalk in factor binding and GTPase activation. Cell. 121 (7), 991–1004.

    CAS  PubMed  Google Scholar 

  76. Gordiyenko Y., Videler H., Zhou M., McKay A.R., Fucini P., Biegel E., Müller V., Robinson C.V. 2010. Mass spectrometry defines the stoichiometry of ribosomal stalk complexes across the phylogenetic tree. Mol. Cell Prot. 9 (8), 1774–1783.

    CAS  Google Scholar 

  77. Ilag L.L., Videler H., McKay A.R., Sobott F., Fucini P., Nierhaus K.H., Robinson, C.V. 2005. Heptameric (L12)6/L10 rather than canonical pentameric complexes are found by tandem MS of intact ribosomes from thermophilic bacteria. Proc. Natl. Acad. Sci. U. S. A. 102 (23), 8192–8197.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Klein D.J., Schmeing T.M., Moore P.B., Steitz T.A. 2001. The kink-turn: A new RNA secondary structure motif. EMBO J. 20 (15), 4214–4221.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Iben J.R., Draper D.E. 2008. Specific interactions of the L10(L12)4 ribosomal protein complex with mRNA, rRNA, and L11. Biochemistry. 47 (9), 2721–2731.

    CAS  PubMed  Google Scholar 

  80. Climie S.C., Friesen J.D. 1987. Feedback regulation of the rplJL-rpoBC ribosomal protein operon of Escherichia coli requires a region of mRNA secondary structure. J. Mol. Biol. 198 (3), 371–381.

    CAS  PubMed  Google Scholar 

  81. Babitzke P., Baker C.S., Romeo T. 2009. Regulation of translation initiation by RNA binding proteins. Annu. Rev. Microbiol. 63, 27–44.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Peattie D.A., Douthwaite S., Garrett R.A., Noller H.F. 1981. A “bulged” double helix in a RNA-protein contact site. Proc. Natl. Acad. Sci. U. S. A. 7 (6), 1697–1701.

    Google Scholar 

  83. Douthwaite S., Christensen A., Garrett R.A. 1982. Binding site of ribosomal proteins on prokaryotic 5S ribonucleic acids: a study with ribonucleases. Biochemistry. 21 (10), 2313–2320.

    CAS  PubMed  Google Scholar 

  84. Thurlow D.L., Ehresmann C., Ehresmann B. 1983. Nucleotides in 16S rRNA that are required in unmodified form for features recognized by ribosomal protein S8. Nucleic Acids Res. 11 (19), 6787–6802.

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Gregory R.J., Zeller M.L., Thurlow D.L., Gourse R.L., Stark M. J.R., Dahlberg A.E., Zimmermann R.A. 1984. Interaction of ribosomal proteins S6, S8, S15 and S18 with the central domain of 16S ribosomal RNA from Escherichia coli. J. Mol. Biol. 178 (2), 287–302.

    CAS  PubMed  Google Scholar 

  86. Stern S., Wilson R.C., Noller H.F. 1986. Localization of the binding site for protein S4 on 16S ribosomal RNA by chemical and enzymatic probing and primer extension. J. Mol. Biol. 192 (1), 101–110.

    CAS  PubMed  Google Scholar 

  87. Climie S.C., Friesen J.D. 1988. In vivo and in vitro structural analysis of the rplJ mRNA leader of Escherichia coli. Protection by bound L10–L7/L12. J. Biol. Chem. 263 (29), 15166–15175.

    CAS  PubMed  Google Scholar 

  88. Christensen T., Johnsen M., Fiil N.P., Friesen J.D. 1984. RNA secondary structure and translation inhibition: analysis of mutants in the rplJ leader. EMBO J. 3 (7), 1609–1612.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Yakhnin H., Yakhnin A.V., Babitzke P. 2015. Ribosomal protein L10(L12)4 autoregulates expression of the Bacillus subtilis rplJL operon by a transcription attenuation mechanism. Nucleic Acids Res. 43 (14), 7032–7043.

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Merino E., Yanofsky C. 2002. Regulation by termination-antitermination: A genomic approach. In Bacillus subtilis and Its Closest Relatives: From Genes to Cells. Washington DC: ASM Press, vol. 1, pp. 323–336.

    Google Scholar 

  91. Draper D.E., Gluick T.C., Schlax P.J. 1998. Pseudoknots, RNA folding, and translational regulation. In RNA Structure and Function. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press, vol. 1, pp. 415–436.

    Google Scholar 

  92. Régnier P., Portier C. 1986. Initiation, attenuation and RNase III processing of transcripts from the Escherichia coli operon encoding ribosomal protein S15 and polynucleotide phosphorylase. J. Mol. Biol. 187 (1), 23–32.

    PubMed  Google Scholar 

  93. Jarrige A.C., Mathy N., Portier C. 2001. PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader. EMBO J. 20 (23), 6845–6855.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Slinger B.L., Newman H., Lee Y., Pei S., Meyer M.M. 2015. Co-evolution of bacterial ribosomal protein S15 with diverse mRNA regulatory structures. PLoS Genet. 11 (12), e1005720.

    PubMed  PubMed Central  Google Scholar 

  95. Serganov A., Polonskaia A., Ehresmann B., Ehresmann C., Patel D.J. 2003. Ribosomal protein S15 represses its own translation via adaptation of an rRNA-like fold within its mRNA. EMBO J. 22 (8), 1898–1908.

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Mathy N., Pellegrini O., Serganov A., Patel D.J., Ehresmann C., Portier C. 2004. Specific recognition of rpsO mRNA and 16S rRNA by Escherichia coli ribosomal protein S15 relies on both mimicry and site differentiation. Mol. Microbiol. 52 (3), 661–675.

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Philippe C., Eyermann F., Bénard L., Portier C., Ehresmann B., Ehresmann C. 1993. Ribosomal protein S15 from Escherichia coli modulates its own translation by trapping the ribosome on the mRNA initiation loading site. Proc. Natl. Acad. Sci. U. S. A. 90 (10), 4394–4398.

    CAS  PubMed  PubMed Central  Google Scholar 

  98. 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 (6), 1019–1031.

    CAS  PubMed  Google Scholar 

  99. Ehresmann C., Ehresmann B., Ennifar E., Dumas P., Garber M., Mathy N., Nikulin A., Portier C., Patel D., Serganov A. 2004. Molecular mimicry in translational regulation: the case of ribosomal protein S15. RNA Biol. 1 (1), 66–73.

    CAS  PubMed  Google Scholar 

  100. Jinks-Robertson S., Nomura M. 1982. Ribosomal protein S4 acts in trans as a translational repressor to regulate expression of the alpha operon in Escherichia coli. Bacteriol. 151 (1), 193–202.

    CAS  Google Scholar 

  101. Thomas M., Bedwell D.M., Nomura M. 1987. Regulation of alpha operon gene expression in Escherichia coli. A novel form of translational coupling. J. Mol. Biol. 196 (2), 333–345.

    CAS  PubMed  Google Scholar 

  102. Nomura M., Held W.A. 1974. Reconstitution of ribosomes: Studies of ribosome structure, function and assembly. In Ribosomes. Cold Spring Harbor, New York: Cold Spring Harbor Lab. Press, vol. 1, pp. 193–224.

    Google Scholar 

  103. Nowotny V., Nierhaus K.H. 1988. Assembly of the 30S subunit from Escherichia coli ribosomes occurs via two assembly domains which are initiated by S4 and S7. Biochemistry. 27 (18), 7051–7055.

    CAS  PubMed  Google Scholar 

  104. Schluenzen F., Tocilj A., Zarivach R., Harms J., Gluehmann M., Janell D., Bashan A., Bartels H., Agmon I., Franceschi F., Yonath, A. 2000. Structure of functionally activated small ribosomal subunit at 3.3 Å resolution. Cell. 102 (5), 615–623.

    CAS  PubMed  Google Scholar 

  105. Wimberly B.T., Brodersen D.E., Clemons Jr. W.M., Morgan-Warren R.J., Carter A.P., Vonrhein C., Hartsch T., Ramakrishnan V. 2000. Structure of the 30S ribosomal subunit. Nature. 407 (6802), 327–339.

    CAS  PubMed  Google Scholar 

  106. Bellur D.L., Woodson S.A. 2009. A minimized rRNA binding site for ribosomal protein S4 and its implications for 30S assembly. Nucleic Acids Res. 37 (6), 1886–1896.

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Baker A., Draper D. 1995. Messenger RNA recognition by fragments of ribosomal protein S4. J. Biol. Chem. 270 (39), 22939–22945.

    CAS  PubMed  Google Scholar 

  108. Tang C.K., Draper D.E. 1989. Unusual mRNA pseudoknot structure is recognized by a protein translational repressor. Cell. 57 (4), 531–536.

    CAS  PubMed  Google Scholar 

  109. Spedding G.S., Gluick T.C., Draper D.E. 1993. Ribosome initiation complex formation with the pseudoknotted alpha operon messenger RNA. J. Mol. Biol. 229 (3), 609–622.

    CAS  PubMed  Google Scholar 

  110. Tang C.K., Draper D.E. 1990. Evidence for allosteric coupling between the ribosome and repressor binding sites of a translationally regulated mRNA. Biochemistry. 29 (18), 4434–4439.

    CAS  PubMed  Google Scholar 

  111. Schlax P.J., Xavier K.A., Gluick T.C., Draper D.E. 2001. Translational repression of the Escherichia coli alpha operon mRNA: importance of an mRNA conformational switch and a ternary entrapment complex. J. Biol. Chem. 276 (42), 38494–38501.

    CAS  PubMed  Google Scholar 

  112. Spedding G.S., Draper D.E. 1993. Allosteric mechanism for translational repression in the Escherichia coli alpha operon. Proc. Natl. Acad. Sci. U. S. A. 90 (10), 4399–4403.

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Deckman I.C., Draper D.E., Thomas M.S. 1987. S4-alpha mRNA translation repression complex: 1. Thermodynamics of formation. J. Mol. Biol. 196 (2), 313–322.

    CAS  PubMed  Google Scholar 

  114. Vartikar J.V., Draper D.E. 1989. S4-16 S ribosomal RNA complex. Binding constant measurements and specific recognition of a 460-nucleotide region. J. Mol. Biol. 209 (2), 221–234.

    CAS  PubMed  Google Scholar 

  115. Grundy F.J., Henkin T.M. 1991. The rpsD gene, encoding ribosomal protein S4, is autogeneously regulated in Bacillus subtilis. J. Bacteriol. 173 (15), 4595–4602.

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Torres M., Condon C., Balada J.M., Squires C., Squires C.L. 2001. Ribosomal protein S4 is a transcription factor with properties remarkably similar to NusA, a protein involved in both nonribosomal and ribosomal RNA termination. EMBO J. 20 (14), 3811–3820.

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Merianos H.J., Wang J., Moore P.B. 2004. The structure of a ribosomal protein S8/spc-operon mRNA complex. RNA. 10 (6), 954–964.

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Zimmermann R.A., Alimov A., Uma K., Wu H., Wower I., Nikonowicz E.P., Drygin D., Dong P., Jiang L. 2000. How proteins and RNA recognize one another. In The Ribosome: Structure, Function, Antibiotics, and Cellular Interactions. Eds. Garrett R.A., Dowthwaite S.A., Liljas A., Marbeson A.T., Moore P.B., Noller H. Washington, DC: ASM Press, vol. 1, pp. 93–104.

    Google Scholar 

  119. Cerretti D.P., Mattheakis L.C., Kearney K.R., Vu L., Nomura M. 1988. Translational regulation of the spc operon in Escherichia coli: Identification and structural analysis of the target site for S8 repressor protein. J. Mol. Biol. 204 (2), 309–329.

    CAS  PubMed  Google Scholar 

  120. Gregory R.J., Cahill P.B., Thurlow D.L., Zimmermann R.A. 1988. Interaction of Escherichia coli ribosomal protein S8 with its binding sites in ribosomal RNA and messenger RNA. J. Mol. Biol. 204 (2), 295–307.

    CAS  PubMed  Google Scholar 

  121. Mattheakis L., Nomura M. 1988. Feedback regulation of the spc operon in Escherichia coli: Translational coupling and mRNA processing. J. Bacteriol. 170 (10), 4482–4492.

    Google Scholar 

  122. Mattheakis L., Vu L., Sor F., Nomura M. 1989. Retroregulation of the synthesis of ribosomal proteins L14 and L24 by feedback repressor S8 in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 86 (2), 448–452.

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Dean D., Yates J.L., Nomura M. 1981. Identification of ribosomal protein S7 as a repressor of translation within the str operon of E. coli. Cell. 24 (2), 413–419.

    CAS  PubMed  Google Scholar 

  124. Saito K., Mattheakis L.C., Nomura M. 1994. Post-transcriptional regulation of the str operon in Escherichia coli. Ribosomal protein S7 inhibits coupled translation of S7 but not its independent translation. J. Mol. Biol. 235 (1), 111–124.

    CAS  PubMed  Google Scholar 

  125. Dragon F., Brakier-Gingras L. 1993. Interaction of Escherichia coli ribosomal protein S7 with 16S rRNA. Nucleic Acids Res. 21 (5), 1199–1203.

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Robert F., Brakier-Gingras L. 2001. Ribosomal protein S7 from Escherichia coli uses the same determinants to bind 16S ribosomal RNA and its messenger RNA. Nucleic Acids Res. 29 (3), 677–682.

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Golovin A., Spiridonova V., Kopylov A. 2006. Mapping contacts of the S12–S7 intercistronic region of str-operon mRNA with ribosomal protein S7 of E. coli. FEBS Lett. 580 (25), 5858–5862.

    CAS  PubMed  Google Scholar 

  128. Burgos H.L., O’Connor K., SanchezVazquez P., Gourse R.L. 2017. Roles of transcriptional and translational control mechanisms in regulation of ribosomal protein synthesis in Escherichia coli. J. Bacteriol. 199, e00407–17.

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Hendrick E.G., Hill W.E. 2010. Protein S20 binds two 16S rRNA sites as assembly is initiated. J. Mol. Biol. 401, 493–502.

    Google Scholar 

  130. Tobin C., Mandava C.S., Ehrenberg M., Andersson D.I., Sanyal S. 2010. Ribosomes lacking protein S20 are defective in mRNA binding and subunit association. J. Mol. Biol. 397, 767–776.

    CAS  PubMed  Google Scholar 

  131. Parsons G.D., Mackie G.A. 1983. Expression of the gene for ribosomal protein S20: effects of gene dosage. J. Bacteriol. 154, 152–160.

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Mackie G.A. 1981. Nucleotide sequence of the gene for ribosomal protein S20 and its flanking regions. J. Biol. Chem. 256, 8177–8182.

    CAS  PubMed  Google Scholar 

  133. Parsons G.D., Donly B.C., Mackie G.A. 1988. Mutations in the leader sequence and initiation codon of the gene for ribosomal protein S20 (rpsT) affect both translational efficiency and autoregulation. J. Bacteriol. 170, 2485–2492.

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Donly B.C., Mackie G.A. 1988. Affinities of ribosomal protein S20 and C-tenninal deletion mutants for 16S rRNA and S20 mRNA. Nucleic Acids Res. 16 (3), 997–1010.

    CAS  PubMed  PubMed Central  Google Scholar 

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The work was supported by the Russian Foundation for Basic Research, project no. 19-14-50124.

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Correspondence to A. O. Mikhaylina.

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Translated by E. Puchkov

Abbreviations: 5'-UTR, 5'-untranslated region; r-proteins, ribosomal proteins; SD, the Shin–Dalgarno sequence.

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Mikhaylina, A.O., Nikonova, E.Y., Kostareva, O.S. et al. Regulation of Ribosomal Protein Synthesis in Prokaryotes. Mol Biol 55, 16–36 (2021). https://doi.org/10.1134/S0026893321010118

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