1932

Abstract

Stalled protein synthesis produces defective nascent chains that can harm cells. In response, cells degrade these nascent chains via a process called ribosome-associated quality control (RQC). Here, we review the irregularities in the translation process that cause ribosomes to stall as well as how cells use RQC to detect stalled ribosomes, ubiquitylate their tethered nascent chains, and deliver the ubiquitylated nascent chains to the proteasome. We additionally summarize how cells respond to RQC failure.

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2020-06-20
2024-03-29
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Literature Cited

  1. 1. 
    Keiler KC, Waller PR, Sauer RT 1996. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271:5251990–93
    [Google Scholar]
  2. 2. 
    Frischmeyer PA, van Hoof A, O'Donnell K, Guerrerio AL, Parker R, Dietz HC 2002. An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 295:55632258–61
    [Google Scholar]
  3. 3. 
    van Hoof A, Frischmeyer PA, Dietz HC, Parker R 2002. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295:55632262–64
    [Google Scholar]
  4. 4. 
    Doma MK, Parker R. 2006. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440:7083561–64
    [Google Scholar]
  5. 5. 
    Inada T, Aiba H. 2005. Translation of aberrant mRNAs lacking a termination codon or with a shortened 3′-UTR is repressed after initiation in yeast. EMBO J 24:81584–95
    [Google Scholar]
  6. 6. 
    Ito-Harashima S, Kuroha K, Tatematsu T, Inada T 2007. Translation of the poly(A) tail plays crucial roles in nonstop mRNA surveillance via translation repression and protein destabilization by proteasome in yeast. Genes Dev 21:5519–246, 7. Evidence for ribosome stalling leading to proteasomal degradation of nascent chains.
    [Google Scholar]
  7. 7. 
    Wilson MA, Meaux S, van Hoof A 2007. A genomic screen in yeast reveals novel aspects of nonstop mRNA metabolism. Genetics 177:2773–846, 7. Evidence for ribosome stalling leading to proteasomal degradation of nascent chains.
    [Google Scholar]
  8. 8. 
    Chu J, Hong NA, Masuda CA, Jenkins BV, Nelms KA et al. 2009. A mouse forward genetics screen identifies LISTERIN as an E3 ubiquitin ligase involved in neurodegeneration. PNAS 106:72097–103Evidence for disruption of RQC leading to neurodegeneration in mice (see also 112).
    [Google Scholar]
  9. 9. 
    Bengtson MH, Joazeiro CAP. 2010. Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 467:7314470–73Identification of Ltn1 as the E3 ubiquitin ligase used by RQC.
    [Google Scholar]
  10. 10. 
    Shoemaker CJ, Eyler DE, Green R 2010. Dom34:Hbs1 promotes subunit dissociation and peptidyl-tRNA drop-off to initiate no-go decay. Science 330:6002369–7210, 11. Identification of Dom34/Pelota–Hbs1 as stalled ribosome splitting factors.
    [Google Scholar]
  11. 11. 
    Pisareva VP, Skabkin MA, Hellen CUT, Pestova TV, Pisarev AV 2011. Dissociation by Pelota, Hbs1 and ABCE1 of mammalian vacant 80S ribosomes and stalled elongation complexes. EMBO J 30:91804–1710, 11. Identification of Dom34/Pelota–Hbs1 as stalled ribosome splitting factors.
    [Google Scholar]
  12. 12. 
    Shao S, von der Malsburg K, Hegde RS 2013. Listerin-dependent nascent protein ubiquitination relies on ribosome subunit dissociation. Mol. Cell 50:5637–48Demonstration of functional conservation of Ltn1 in mammals and how ribosome splitting precedes Ltn1 activity.
    [Google Scholar]
  13. 13. 
    Brandman O, Stewart-Ornstein J, Wong D, Larson A, Williams CC et al. 2012. A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 151:51042–5413, 14. Genetic screen that identifies the RQC complex in yeast.
    [Google Scholar]
  14. 14. 
    Defenouillère Q, Yao Y, Mouaikel J, Namane A, Galopier A et al. 2013. Cdc48-associated complex bound to 60S particles is required for the clearance of aberrant translation products. PNAS 110:135046–5113, 14. Genetic screen that identifies the RQC complex in yeast.
    [Google Scholar]
  15. 15. 
    Verma R, Oania RS, Kolawa NJ, Deshaies RJ 2013. Cdc48/p97 promotes degradation of aberrant nascent polypeptides bound to the ribosome. eLife 2:e00308
    [Google Scholar]
  16. 16. 
    Matsuda R, Ikeuchi K, Nomura S, Inada T 2014. Protein quality control systems associated with no-go and nonstop mRNA surveillance in yeast. Genes Cells 19:11–12
    [Google Scholar]
  17. 17. 
    Kuroha K, Akamatsu M, Dimitrova L, Ito T, Kato Y et al. 2010. Receptor for activated C kinase 1 stimulates nascent polypeptide‐dependent translation arrest. EMBO Rep 11:12956–61
    [Google Scholar]
  18. 18. 
    Letzring DP, Wolf AS, Brule CE, Grayhack EJ 2013. Translation of CGA codon repeats in yeast involves quality control components and ribosomal protein L1. RNA 19:91208–17
    [Google Scholar]
  19. 19. 
    Sitron CS, Park JH, Brandman O 2017. Asc1, Hel2, and Slh1 couple translation arrest to nascent chain degradation. RNA 23:5798–810
    [Google Scholar]
  20. 20. 
    Juszkiewicz S, Hegde RS. 2017. Initiation of quality control during poly(A) translation requires site-specific ribosome ubiquitination. Mol. Cell 65:4743–50.e420-22. Demonstration that Hel2/ZNF598 ubiquitylates stalled ribosomes to mark them for RQC.
    [Google Scholar]
  21. 21. 
    Sundaramoorthy E, Leonard M, Mak R, Liao J, Fulzele A, Bennett EJ 2017. ZNF598 and RACK1 regulate mammalian ribosome-associated quality control function by mediating regulatory 40S ribosomal ubiquitylation. Mol. Cell 65:4751–60.e420-22. Demonstration that Hel2/ZNF598 ubiquitylates stalled ribosomes to mark them for RQC.
    [Google Scholar]
  22. 22. 
    Matsuo Y, Ikeuchi K, Saeki Y, Iwasaki S, Schmidt C et al. 2017. Ubiquitination of stalled ribosome triggers ribosome-associated quality control. Nat. Commun. 8:15920-22. Demonstration that Hel2/ZNF598 ubiquitylates stalled ribosomes to mark them for RQC.
    [Google Scholar]
  23. 23. 
    Simms CL, Yan LL, Zaher HS 2017. Ribosome collision is critical for quality control during no-go decay. Mol. Cell 68:2361–73.e5
    [Google Scholar]
  24. 24. 
    Garzia A, Jafarnejad SM, Meyer C, Chapat C, Gogakos T et al. 2017. The E3 ubiquitin ligase and RNA-binding protein ZNF598 orchestrates ribosome quality control of premature polyadenylated mRNAs. Nat. Commun. 8:16056
    [Google Scholar]
  25. 25. 
    Saito K, Horikawa W, Ito K 2015. Inhibiting K63 polyubiquitination abolishes no-go type stalled translation surveillance in Saccharomyces cerevisiae. PLOS Genet 11:4e1005197
    [Google Scholar]
  26. 26. 
    Ikeuchi K, Tesina P, Matsuo Y, Sugiyama T, Cheng J et al. 2019. Collided ribosomes form a unique structural interface to induce Hel2‐driven quality control pathways. EMBO J 38:5e100276
    [Google Scholar]
  27. 27. 
    Higgins R, Gendron JM, Rising L, Mak R, Webb K et al. 2015. The unfolded protein response triggers site-specific regulatory ubiquitylation of 40S ribosomal proteins. Mol. Cell 59:135–49
    [Google Scholar]
  28. 28. 
    Moazed D, Noller HF. 1989. Intermediate states in the movement of transfer RNA in the ribosome. Nature 342:6246142–48
    [Google Scholar]
  29. 29. 
    Munro JB, Altman RB, O'Connor N, Blanchard SC 2007. Identification of two distinct hybrid state intermediates on the ribosome. Mol. Cell 25:4505–17
    [Google Scholar]
  30. 30. 
    Lareau LF, Hite DH, Hogan GJ, Brown PO 2014. Distinct stages of the translation elongation cycle revealed by sequencing ribosome-protected mRNA fragments. eLife 3:e01257
    [Google Scholar]
  31. 31. 
    Juszkiewicz S, Chandrasekaran V, Lin Z, Kraatz S, Ramakrishnan V, Hegde RS 2018. ZNF598 is a quality control sensor of collided ribosomes. Mol. Cell 72:3469–81.e7
    [Google Scholar]
  32. 32. 
    Winz M-L, Peil L, Turowski TW, Rappsilber J, Tollervey D 2019. Molecular interactions between Hel2 and RNA supporting ribosome-associated quality control. Nat. Commun. 10:563
    [Google Scholar]
  33. 33. 
    Kouba T, Rutkai E, Karásková M, Valášek LS 2012. The eIF3c/NIP1 PCI domain interacts with RNA and RACK1/ASC1 and promotes assembly of translation preinitiation complexes. Nucleic Acids Res 40:62683–99
    [Google Scholar]
  34. 34. 
    Wolf AS, Grayhack EJ. 2015. Asc1, homolog of human RACK1, prevents frameshifting in yeast by ribosomes stalled at CGA codon repeats. RNA 21:5935–45
    [Google Scholar]
  35. 35. 
    Wang J, Zhou J, Yang Q, Grayhack EJ 2018. Multi-protein bridging factor 1 (Mbf1), Rps3 and Asc1 prevent stalled ribosomes from frameshifting. eLife 7:e39637
    [Google Scholar]
  36. 36. 
    Nilsson J, Sengupta J, Frank J, Nissen P 2004. Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep 5:121137–41
    [Google Scholar]
  37. 37. 
    Gallo S, Manfrini N. 2015. Working hard at the nexus between cell signaling and the ribosomal machinery: an insight into the roles of RACK1 in translational regulation. Translation 3:2e1120382
    [Google Scholar]
  38. 38. 
    Zeller CE, Parnell SC, Dohlman HG 2007. The RACK1 ortholog Asc1 functions as a G-protein β subunit coupled to glucose responsiveness in yeast. J. Biol. Chem. 282:3425168–76
    [Google Scholar]
  39. 39. 
    Ron D, Chen CH, Caldwell J, Jamieson L, Orr E, Mochly-Rosen D 1994. Cloning of an intracellular receptor for protein kinase C: a homolog of the β subunit of G proteins. PNAS 91:3839–43
    [Google Scholar]
  40. 40. 
    Becker T, Armache J-P, Jarasch A, Anger AM, Villa E et al. 2011. Structure of the no-go mRNA decay complex Dom34-Hbs1 bound to a stalled 80S ribosome. Nat. Struct. Mol. Biol. 18:715–20
    [Google Scholar]
  41. 41. 
    Becker T, Franckenberg S, Wickles S, Shoemaker CJ, Anger AM et al. 2012. Structural basis of highly conserved ribosome recycling in eukaryotes and archaea. Nature 482:7386501–6
    [Google Scholar]
  42. 42. 
    Chavatte L, Seit-Nebi A, Dubovaya V, Favre A 2002. The invariant uridine of stop codons contacts the conserved NIKSR loop of human eRF1 in the ribosome. EMBO J 21:195302–11
    [Google Scholar]
  43. 43. 
    Taylor D, Unbehaun A, Li W, Das S, Lei J et al. 2012. Cryo-EM structure of the mammalian eukaryotic release factor eRF1-eRF3-associated termination complex. PNAS 109:4518413–18
    [Google Scholar]
  44. 44. 
    Muhs M, Hilal T, Mielke T, Skabkin MA, Sanbonmatsu KY et al. 2015. Cryo-EM of ribosomal 80S complexes with termination factors reveals the translocated cricket paralysis virus IRES. Mol. Cell 57:3422–32
    [Google Scholar]
  45. 45. 
    Brown A, Shao S, Murray J, Hegde RS, Ramakrishnan V 2015. Structural basis for stop codon recognition in eukaryotes. Nature 524:7566493–96
    [Google Scholar]
  46. 46. 
    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 2:4334–41
    [Google Scholar]
  47. 47. 
    Song H, Mugnier P, Das AK, Webb HM, Evans DR et al. 2000. The crystal structure of human eukaryotic release factor eRF1—mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100:3311–21
    [Google Scholar]
  48. 48. 
    Pisarev AV, Skabkin MA, Pisareva VP, Skabkina OV, Rakotondrafara AM et al. 2010. The role of ABCE1 in eukaryotic posttermination ribosomal recycling. Mol. Cell 37:2196–210
    [Google Scholar]
  49. 49. 
    Shoemaker CJ, Green R. 2011. Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast. PNAS 108:51E1392–98
    [Google Scholar]
  50. 50. 
    Graille M, Chaillet M, van Tilbeurgh H 2008. Structure of yeast Dom34: a protein related to translation termination factor Erf1 and involved in no-go decay. J. Biol. Chem. 283:117145–54
    [Google Scholar]
  51. 51. 
    Lee HH, Kim Y-S, Kim KH, Heo I, Kim SK et al. 2007. Structural and functional insights into Dom34, a key component of no-go mRNA decay. Mol. Cell 27:6938–50
    [Google Scholar]
  52. 52. 
    Guydosh NR, Green R. 2014. Dom34 rescues ribosomes in 3′ untranslated regions. Cell 156:5950–62
    [Google Scholar]
  53. 53. 
    Kobayashi K, Kikuno I, Kuroha K, Saito K, Ito K et al. 2010. Structural basis for mRNA surveillance by archaeal Pelota and GTP-bound EF1α complex. PNAS 107:4117575–79
    [Google Scholar]
  54. 54. 
    Ikeuchi K, Inada T. 2016. Ribosome-associated Asc1/RACK1 is required for endonucleolytic cleavage induced by stalled ribosome at the 3′ end of nonstop mRNA. Sci. Rep. 6:28234
    [Google Scholar]
  55. 55. 
    Chen L, Muhlrad D, Hauryliuk V, Cheng Z, Lim MK et al. 2010. Structure of the Dom34-Hbs1 complex and implications for its role in no-go decay. Nat. Struct. Mol. Biol. 17:101233–40
    [Google Scholar]
  56. 56. 
    Chiabudini M, Tais A, Zhang Y, Hayashi S, Wölfle T et al. 2014. Release factor eRF3 mediates premature translation termination on polylysine-stalled ribosomes in Saccharomyces cerevisiae. Mol. Cell. Biol 34:214062–76
    [Google Scholar]
  57. 57. 
    Shcherbik N, Chernova TA, Chernoff YO, Pestov DG 2016. Distinct types of translation termination generate substrates for ribosome-associated quality control. Nucleic Acids Res 44:146840–52
    [Google Scholar]
  58. 58. 
    D'Orazio KN, Wu CC-C, Sinha N, Loll-Krippleber R, Brown GW, Green R 2019. The endonuclease Cue2 cleaves mRNAs at stalled ribosomes during no go decay. eLife 8:e49117
    [Google Scholar]
  59. 59. 
    Sugiyama T, Li S, Kato M, Ikeuchi K, Ichimura A et al. 2019. Sequential ubiquitination of ribosomal protein uS3 triggers the degradation of non-functional 18S rRNA. Cell Rep 26:123400–15.e7
    [Google Scholar]
  60. 60. 
    Lyumkis D, dos Passos DO, Tahara EB, Webb K, Bennett EJ et al. 2014. Structural basis for translational surveillance by the large ribosomal subunit-associated protein quality control complex. PNAS 111:4515981–86
    [Google Scholar]
  61. 61. 
    Shen PS, Park J, Qin Y, Li X, Parsawar K et al. 2015. Rqc2p and 60S ribosomal subunits mediate mRNA-independent elongation of nascent chains. Science 347:621775–78Discovery of CAT tails and a cryo–electron microscopy structure of Rqc2- and Ltn1-bound 60S subunit.
    [Google Scholar]
  62. 62. 
    Shao S, Brown A, Santhanam B, Hegde RS 2015. Structure and assembly pathway of the ribosome quality control complex. Mol. Cell 57:3433–44
    [Google Scholar]
  63. 63. 
    Doamekpor SK, Lee J-W, Hepowit NL, Wu C, Charenton C et al. 2016. Structure and function of the yeast listerin (Ltn1) conserved N-terminal domain in binding to stalled 60S ribosomal subunits. PNAS 113:29E4151–60
    [Google Scholar]
  64. 64. 
    Shao S, Hegde RS. 2014. Reconstitution of a minimal ribosome-associated ubiquitination pathway with purified factors. Mol. Cell 55:6880–90
    [Google Scholar]
  65. 65. 
    Nameki N, Yoneyama M, Koshiba S, Tochio N, Inoue M et al. 2004. Solution structure of the RWD domain of the mouse GCN2 protein. Protein Sci 13:82089–100
    [Google Scholar]
  66. 66. 
    Deshaies RJ, Joazeiro CAP. 2009. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78:399–434
    [Google Scholar]
  67. 67. 
    Kostova KK, Hickey KL, Osuna BA, Hussmann JA, Frost A et al. 2017. CAT-tailing as a fail-safe mechanism for efficient degradation of stalled nascent polypeptides. Science 357:6349414–17
    [Google Scholar]
  68. 68. 
    Osuna BA, Howard CJ, Subheksha KC, Frost A, Weinberg DE 2017. In vitro analysis of RQC activities provides insights into the mechanism and function of CAT tailing. eLife 6:e27949
    [Google Scholar]
  69. 69. 
    Burroughs AM, Aravind L. 2014. A highly conserved family of domains related to the DNA-glycosylase fold helps predict multiple novel pathways for RNA modifications. RNA Biol 11:4360–72
    [Google Scholar]
  70. 70. 
    Lytvynenko I, Paternoga H, Thrun A, Balke A, Müller TA et al. 2019. Alanine tails signal proteolysis in bacterial ribosome-associated quality control. Cell 178:176–90.e22
    [Google Scholar]
  71. 71. 
    Wu Z, Tantray I, Lim J, Chen S, Li Y et al. 2019. MISTERMINATE mechanistically links mitochondrial dysfunction with proteostasis failure. Mol. Cell 75:4835–48
    [Google Scholar]
  72. 72. 
    Monro RE. 1969. Uncoupling of polymerization from template control. Nature 223:5209903–5
    [Google Scholar]
  73. 73. 
    Sitron CS, Brandman O. 2019. CAT tails drive degradation of stalled polypeptides on and off the ribosome. Nat. Struct. Mol. Biol. 26:6450–59Characterization of yeast CAT tails as degrons (also shown for prokaryotes in 70).
    [Google Scholar]
  74. 74. 
    Alamgir M, Erukova V, Jessulat M, Azizi A, Golshani A 2010. Chemical-genetic profile analysis of five inhibitory compounds in yeast. BMC Chem. Biol. 10:6
    [Google Scholar]
  75. 75. 
    Choe Y-J, Park S-H, Hassemer T, Körner R, Vincenz-Donnelly L et al. 2016. Failure of RQC machinery causes protein aggregation and proteotoxic stress. Nature 531:7593191–95Demonstration of how CAT tails can aggregate after RQC failure (see also 81, 82).
    [Google Scholar]
  76. 76. 
    Moore SD, Sauer RT. 2007. The tmRNA system for translational surveillance and ribosome rescue. Annu. Rev. Biochem. 76:101–24
    [Google Scholar]
  77. 77. 
    Mirkin BG, Fenner TI, Galperin MY, Koonin EV 2003. Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. BMC Evol. Biol. 3:2
    [Google Scholar]
  78. 78. 
    Kuroha K, Zinoviev A, Hellen CUT, Pestova TV 2018. Release of ubiquitinated and non-ubiquitinated nascent chains from stalled mammalian ribosomal complexes by ANKZF1 and Ptrh1. Mol. Cell 72:2286–302.e8
    [Google Scholar]
  79. 79. 
    Tsuchiya H, Ohtake F, Arai N, Kaiho A, Yasuda S et al. 2017. In vivo ubiquitin linkage-type analysis reveals that the Cdc48-Rad23/Dsk2 axis contributes to K48-linked chain specificity of the proteasome. Mol. Cell 66:4488–502.e7
    [Google Scholar]
  80. 80. 
    Stewart MD, Ritterhoff T, Klevit RE, Brzovic PS 2016. E2 enzymes: more than just middle men. Cell Res 26:4423–40
    [Google Scholar]
  81. 81. 
    Yonashiro R, Tahara EB, Bengtson MH, Khokhrina M, Lorenz H et al. 2016. The Rqc2/Tae2 subunit of the ribosome-associated quality control (RQC) complex marks ribosome-stalled nascent polypeptide chains for aggregation. eLife 5:e11794
    [Google Scholar]
  82. 82. 
    Defenouillère Q, Zhang E, Namane A, Mouaikel J, Jacquier A, Fromont-Racine M 2016. Rqc1 and Ltn1 prevent CAT-tail induced protein aggregation by efficient recruitment of Cdc48 on stalled 60S subunits. J. Biol. Chem. 291:2312245–53
    [Google Scholar]
  83. 83. 
    Hänzelmann P, Schindelin H. 2011. The structural and functional basis of the p97/valosin-containing protein (VCP)-interacting motif (VIM): mutually exclusive binding of cofactors to the N-terminal domain of p97. J. Biol. Chem. 286:4438679–90
    [Google Scholar]
  84. 84. 
    Stapf C, Cartwright E, Bycroft M, Hofmann K, Buchberger A 2011. The general definition of the p97/valosin-containing protein (VCP)-interacting motif (VIM) delineates a new family of p97 cofactors. J. Biol. Chem. 286:4438670–78
    [Google Scholar]
  85. 85. 
    Izawa T, Park S-H, Zhao L, Hartl FU, Neupert W 2017. Cytosolic protein Vms1 links ribosome quality control to mitochondrial and cellular homeostasis. Cell 171:4890–903.e18
    [Google Scholar]
  86. 86. 
    Nielson JR, Fredrickson EK, Cameron Waller T, Rendón OZ, Schubert HL et al. 2017. Sterol oxidation mediates stress-responsive Vms1 translocation to mitochondria. Mol. Cell 68:4673–85.e6
    [Google Scholar]
  87. 87. 
    Verma R, Reichermeier KM, Burroughs AM, Oania RS, Reitsma JM et al. 2018. Vms1 and ANKZF1 peptidyl-tRNA hydrolases release nascent chains from stalled ribosomes. Nature 557:7705446–51
    [Google Scholar]
  88. 88. 
    Rendón OZ, Fredrickson EK, Howard CJ, Van Vranken J, Fogarty S et al. 2018. Vms1p is a release factor for the ribosome-associated quality control complex. Nat. Commun. 9:2197
    [Google Scholar]
  89. 89. 
    Yip MCJ, Keszei AFA, Feng Q, Chu V, McKenna MJ, Shao S 2019. Mechanism for recycling tRNAs on stalled ribosomes. Nat. Struct. Mol. Biol. 26:5343–49
    [Google Scholar]
  90. 90. 
    Su T, Izawa T, Thoms M, Yamashita Y, Cheng J et al. 2019. Structure and function of Vms1 and Arb1 in RQC and mitochondrial proteome homeostasis. Nature 570:7762538–42
    [Google Scholar]
  91. 91. 
    Ye Y, Tang WK, Zhang T, Xia D 2017. A mighty “protein extractor” of the cell: structure and function of the p97/CDC48 ATPase. Front. Mol. Biosci. 4:39
    [Google Scholar]
  92. 92. 
    Bodnar NO, Rapoport TA. 2017. Molecular mechanism of substrate processing by the Cdc48 ATPase complex. Cell 169:4722–35.e9
    [Google Scholar]
  93. 93. 
    Blythe EE, Olson KC, Chau V, Deshaies RJ 2017. Ubiquitin- and ATP-dependent unfoldase activity of P97/VCP•NPLOC4•UFD1L is enhanced by a mutation that causes multisystem proteinopathy. PNAS 114:22E4380–88
    [Google Scholar]
  94. 94. 
    Beskow A, Grimberg KB, Bott LC, Salomons FA, Dantuma NP, Young P 2009. A conserved unfoldase activity for the p97 AAA-ATPase in proteasomal degradation. J. Mol. Biol. 394:4732–46
    [Google Scholar]
  95. 95. 
    Olszewski MM, Williams C, Dong KC, Martin A 2019. The Cdc48 unfoldase prepares well-folded protein substrates for degradation by the 26S proteasome. Commun. Biol. 2:29
    [Google Scholar]
  96. 96. 
    Defenouillère Q, Namane A, Mouaikel J, Jacquier A, Fromont-Racine M 2017. The ribosome-bound quality control complex remains associated to aberrant peptides during their proteasomal targeting and interacts with Tom1 to limit protein aggregation. Mol. Biol. Cell 28:91165–76
    [Google Scholar]
  97. 97. 
    Izawa T, Tsuboi T, Kuroha K, Inada T, Nishikawa S-I, Endo T 2012. Roles of Dom34:Hbs1 in nonstop protein clearance from translocators for normal organelle protein influx. Cell Rep 2:3447–53
    [Google Scholar]
  98. 98. 
    Crowder JJ, Geigges M, Gibson RT, Fults ES, Buchanan BW et al. 2015. Rkr1/Ltn1 ubiquitin ligase-mediated degradation of translationally stalled endoplasmic reticulum proteins. J. Biol. Chem. 290:3018454–66
    [Google Scholar]
  99. 99. 
    Arakawa S, Yunoki K, Izawa T, Tamura Y, Nishikawa S-I, Endo T 2016. Quality control of nonstop membrane proteins at the ER membrane and in the cytosol. Sci. Rep. 6:30795
    [Google Scholar]
  100. 100. 
    von der Malsburg K, Shao S, Hegde RS 2015. The ribosome quality control pathway can access nascent polypeptides stalled at the Sec61 translocon. Mol. Biol. Cell 26:122168–80
    [Google Scholar]
  101. 101. 
    Lakshminarayan R, Phillips BP, Binnian IL, Gomez-Navarro N, Escudero-Urquijo N et al. 2020. Pre-emptive quality control of a misfolded membrane protein by ribosome-driven effects. Curr. Biol. 30:85464.e5
    [Google Scholar]
  102. 102. 
    Trentini DB, Pecoraro M, Tiwary S, Cox J, Mann M et al. 2020. Role for ribosome-associated quality control in sampling proteins for MHC class I-mediated antigen presentation. PNAS 117:84099–108
    [Google Scholar]
  103. 103. 
    Sitron CS, Park JH, Giafaglione JM, Brandman O 2020. Aggregation of CAT tails blocks their degradation and causes proteotoxicity in S. cerevisiae. PLOS ONE 15:1e0227841
    [Google Scholar]
  104. 104. 
    Fändrich M, Dobson CM. 2002. The behaviour of polyamino acids reveals an inverse side chain effect in amyloid structure formation. EMBO J 21:215682–90
    [Google Scholar]
  105. 105. 
    Shinchuk LM, Sharma D, Blondelle SE, Reixach N, Inouye H, Kirschner DA 2005. Poly-(l-alanine) expansions form core β-sheets that nucleate amyloid assembly. Proteins 61:3579–89
    [Google Scholar]
  106. 106. 
    Abravaya K, Myers MP, Murphy SP, Morimoto RI 1992. The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev 6:71153–64
    [Google Scholar]
  107. 107. 
    Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R 1998. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94:4471–80
    [Google Scholar]
  108. 108. 
    Neef DW, Jaeger AM, Gomez-Pastor R, Willmund F, Frydman J, Thiele DJ 2014. A direct regulatory interaction between chaperonin TRiC and stress-responsive transcription factor HSF1. Cell Rep 9:3955–66
    [Google Scholar]
  109. 109. 
    Zheng X, Krakowiak J, Patel N, Beyzavi A, Ezike J et al. 2016. Dynamic control of Hsf1 during heat shock by a chaperone switch and phosphorylation. eLife 5:e18638
    [Google Scholar]
  110. 110. 
    Krakowiak J, Zheng X, Patel N, Feder ZA, Anandhakumar J et al. 2018. Hsf1 and Hsp70 constitute a two-component feedback loop that regulates the yeast heat shock response. eLife 7:e31668
    [Google Scholar]
  111. 111. 
    Farah CA, Abi Farah C, Nguyen MD, Julien JP, Leclerc N 2003. Altered levels and distribution of microtubule-associated proteins before disease onset in a mouse model of amyotrophic lateral sclerosis. J. Neurochem. 84:177–86
    [Google Scholar]
  112. 112. 
    Ishimura R, Nagy G, Dotu I, Zhou H-L, Yang X et al. 2014. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. Science 345:6195455–59
    [Google Scholar]
  113. 113. 
    Roman C, Cohn L, Calame K 1991. A dominant negative form of transcription activator mTFE3 created by differential splicing. Science 254:502894–97
    [Google Scholar]
  114. 114. 
    Davis ZH, Mediani L, Vinet J, Alberti S, Holehouse AS et al. 2019. Protein products of non-stop mRNA disrupt nucleolar homeostasis. bioRxiv 851741. https://doi.org/10.1101/851741
    [Crossref]
  115. 115. 
    Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:5924218–23
    [Google Scholar]
  116. 116. 
    Charneski CA, Hurst LD. 2013. Positively charged residues are the major determinants of ribosomal velocity. PLOS Biol 11:3e1001508
    [Google Scholar]
  117. 117. 
    Requião RD, de Souza HJA, Rossetto S, Domitrovic T, Palhano FL 2016. Increased ribosome density associated to positively charged residues is evident in ribosome profiling experiments performed in the absence of translation inhibitors. RNA Biol 13:6561–68
    [Google Scholar]
  118. 118. 
    Weinberg DE, Shah P, Eichhorn SW, Hussmann JA, Plotkin JB, Bartel DP 2016. Improved ribosome-footprint and mRNA measurements provide insights into dynamics and regulation of yeast translation. Cell Rep 14:71787–99
    [Google Scholar]
  119. 119. 
    Lu J, Deutsch C. 2008. Electrostatics in the ribosomal tunnel modulate chain elongation rates. J. Mol. Biol. 384:173–86
    [Google Scholar]
  120. 120. 
    Dimitrova LN, Kuroha K, Tatematsu T, Inada T 2009. Nascent peptide-dependent translation arrest leads to Not4p-mediated protein degradation by the proteasome. J. Biol. Chem. 284:1610343–52
    [Google Scholar]
  121. 121. 
    Letzring DP, Dean KM, Grayhack EJ 2010. Control of translation efficiency in yeast by codon-anticodon interactions. RNA 16:122516–28
    [Google Scholar]
  122. 122. 
    Stadler M, Fire A. 2011. Wobble base-pairing slows in vivo translation elongation in metazoans. RNA 17:122063–73
    [Google Scholar]
  123. 123. 
    Gamble CE, Brule CE, Dean KM, Fields S, Grayhack EJ 2016. Adjacent codons act in concert to modulate translation efficiency in yeast. Cell 166:3679–90
    [Google Scholar]
  124. 124. 
    Simms CL, Hudson BH, Mosior JW, Rangwala AS, Zaher HS 2014. An active role for the ribosome in determining the fate of oxidized mRNA. Cell Rep 9:41256–64
    [Google Scholar]
  125. 125. 
    Arthur L, Pavlovic-Djuranovic S, Smith-Koutmou K, Green R, Szczesny P, Djuranovic S 2015. Translational control by lysine-encoding A-rich sequences. Sci. Adv. 1:6e1500154
    [Google Scholar]
  126. 126. 
    Tang TTL, Stowell JAW, Hill CH, Passmore LA 2019. The intrinsic structure of poly(A) RNA determines the specificity of Pan2 and Caf1 deadenylases. Nat. Struct. Mol. Biol. 26:6433–42
    [Google Scholar]
  127. 127. 
    Chandrasekaran V, Juszkiewicz S, Choi J, Puglisi JD, Brown A et al. 2019. Mechanism of ribosome stalling during translation of a poly(A) tail. Nat. Struct. Mol. Biol. 26:121132–40
    [Google Scholar]
  128. 128. 
    Bonetti B, Fu L, Moon J, Bedwell DM 1995. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J. Mol. Biol 251:3334–45
    [Google Scholar]
  129. 129. 
    Namy O, Duchateau-Nguyen G, Rousset J-P 2002. Translational readthrough of the PDE2 stop codon modulates cAMP levels in Saccharomyces cerevisiae. Mol. Microbiol 43:3641–52
    [Google Scholar]
  130. 130. 
    Firth AE, Wills NM, Gesteland RF, Atkins JF 2011. Stimulation of stop codon readthrough: frequent presence of an extended 3′ RNA structural element. Nucleic Acids Res 39:156679–91
    [Google Scholar]
  131. 131. 
    Napthine S, Yek C, Powell ML, Brown TDK, Brierley I 2012. Characterization of the stop codon readthrough signal of Colorado tick fever virus segment 9 RNA. RNA 18:2241–52
    [Google Scholar]
  132. 132. 
    Dunn JG, Foo CK, Belletier NG, Gavis ER, Weissman JS 2013. Ribosome profiling reveals pervasive and regulated stop codon readthrough in Drosophila melanogaster. eLife 2:e01179
    [Google Scholar]
  133. 133. 
    Wickner RB, Masison DC, Edskes HK 1995. [PSI] and [URE3] as yeast prions. Yeast 11:161671–85
    [Google Scholar]
  134. 134. 
    Manuvakhova M, Keeling K, Bedwell DM 2000. Aminoglycoside antibiotics mediate context-dependent suppression of termination codons in a mammalian translation system. RNA 6:71044–55
    [Google Scholar]
  135. 135. 
    Wilson MA, Meaux S, Parker R, van Hoof A 2005. Genetic interactions between [PSI+] and nonstop mRNA decay affect phenotypic variation. PNAS 102:2910244–49
    [Google Scholar]
  136. 136. 
    Pelechano V, Wei W, Steinmetz LM 2013. Extensive transcriptional heterogeneity revealed by isoform profiling. Nature 497:7447127–31
    [Google Scholar]
  137. 137. 
    Ozsolak F, Kapranov P, Foissac S, Kim SW, Fishilevich E et al. 2010. Comprehensive polyadenylation site maps in yeast and human reveal pervasive alternative polyadenylation. Cell 143:61018–29
    [Google Scholar]
  138. 138. 
    Sparks KA, Mayer SA, Dieckmann CL 1997. Premature 3′-end formation of CBP1 mRNA results in the downregulation of cytochrome b mRNA during the induction of respiration in Saccharomyces cerevisiae. Mol. Cell. Biol 17:84199–207
    [Google Scholar]
  139. 139. 
    Meaux S, Van Hoof A 2006. Yeast transcripts cleaved by an internal ribozyme provide new insight into the role of the cap and poly(A) tail in translation and mRNA decay. RNA 12:71323–37
    [Google Scholar]
  140. 140. 
    Tsuboi T, Kuroha K, Kudo K, Makino S, Inoue E et al. 2012. Dom34:Hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3′ end of aberrant mRNA. Mol. Cell 46:4518–29
    [Google Scholar]
  141. 141. 
    Guydosh NR, Kimmig P, Walter P, Green R 2017. Regulated Ire1-dependent mRNA decay requires no-go mRNA degradation to maintain endoplasmic reticulum homeostasis in S. pombe. eLife 6:e29216
    [Google Scholar]
  142. 142. 
    Cesaratto F, Sasset L, Myers MP, Re A, Petris G, Burrone OR 2019. BiP/GRP78 mediates ERAD targeting of proteins produced by membrane-bound ribosomes stalled at the STOP-codon. J. Mol. Biol. 431:2123–41
    [Google Scholar]
  143. 143. 
    Cole SE, LaRiviere FJ, Merrikh CN, Moore MJ 2009. A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Mol. Cell 34:4440–50
    [Google Scholar]
  144. 144. 
    Sarkar A, Thoms M, Barrio-Garcia C, Thomson E, Flemming D et al. 2017. Preribosomes escaping from the nucleus are caught during translation by cytoplasmic quality control. Nat. Struct. Mol. Biol. 24:121107–15
    [Google Scholar]
  145. 145. 
    Jung Y, Kim HD, Yang HW, Kim HJ, Jang C-Y, Kim J 2017. Modulating cellular balance of Rps3 mono-ubiquitination by both Hel2 E3 ligase and Ubp3 deubiquitinase regulates protein quality control. Exp. Mol. Med. 49:e390
    [Google Scholar]
  146. 146. 
    Garshott DM, Sundaramoorthy E, Leonard M, Bennett EJ 2018. USP21 and OTUD3 antagonize regulatory ribosomal ubiquitylation and ribosome-associated quality control. bioRxiv 407726. https://doi.org/10.1101/407726
    [Crossref]
  147. 147. 
    Maupin-Furlow JA. 2013. Ubiquitin-like proteins and their roles in archaea. Trends Microbiol 21:131–38
    [Google Scholar]
  148. 148. 
    Ishimura R, Nagy G, Dotu I, Chuang JH, Ackerman SL 2016. Activation of GCN2 kinase by ribosome stalling links translation elongation with translation initiation. eLife 5:e14295
    [Google Scholar]
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