1932

Abstract

Folding of polypeptides begins during their synthesis on ribosomes. This process has evolved as a means for the cell to maintain proteostasis, by mitigating the risk of protein misfolding and aggregation. The capacity to now depict this cellular feat at increasingly higher resolution is providing insight into the mechanistic determinants that promote successful folding. Emerging from these studies is the intimate interplay between protein translation and folding, and within this the ribosome particle is the key player. Its unique structural properties provide a specialized scaffold against which nascent polypeptides can begin to form structure in a highly coordinated, co-translational manner. Here, we examine how, as a macromolecular machine, the ribosome modulates the intrinsic dynamic properties of emerging nascent polypeptide chains and guides them toward their biologically active structures.

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2020-06-20
2024-06-13
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Literature Cited

  1. 1. 
    Cabrita LD, Dobson CM, Christodoulou J 2010. Protein folding on the ribosome. Curr. Opin. Struct. Biol. 20:33–45
    [Google Scholar]
  2. 2. 
    Ciryam P, Morimoto RI, Vendruscolo M, Dobson CM, O'Brien EP 2013. In vivo translation rates can substantially delay the cotranslational folding of the Escherichia coli cytosolic proteome. PNAS 110:E132–40
    [Google Scholar]
  3. 3. 
    Netzer WJ, Hartl FU. 1997. Recombination of protein domains facilitated by co-translational folding in eukaryotes. Nature 388:343–49
    [Google Scholar]
  4. 4. 
    Chiti F, Dobson CM. 2017. Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade. Annu. Rev. Biochem. 86:27–68
    [Google Scholar]
  5. 5. 
    Brandt F, Etchells SA, Ortiz JO, Elcock AH, Hartl FU, Baumeister W 2009. The native 3D organization of bacterial polysomes. Cell 136:261–71
    [Google Scholar]
  6. 6. 
    Kramer G, Shiber A, Bukau B 2019. Mechanisms of cotranslational maturation of newly synthesized proteins. Annu. Rev. Biochem. 88:337–64
    [Google Scholar]
  7. 7. 
    Hartl FU, Bracher A, Hayer-Hartl M 2011. Molecular chaperones in protein folding and proteostasis. Nature 475:324–32
    [Google Scholar]
  8. 8. 
    Duttler S, Pechmann S, Frydman J 2013. Principles of cotranslational ubiquitination and quality control at the ribosome. Mol. Cell 50:379–93
    [Google Scholar]
  9. 9. 
    Wang F, Durfee LA, Huibregtse JM 2013. A cotranslational ubiquitination pathway for quality control of misfolded proteins. Mol. Cell 50:368–78
    [Google Scholar]
  10. 10. 
    Lynch M, Marinov GK. 2015. The bioenergetic costs of a gene. PNAS 112:15690–695
    [Google Scholar]
  11. 11. 
    Lane N, Martin W. 2010. The energetics of genome complexity. Nature 467:929–34
    [Google Scholar]
  12. 12. 
    Kramer G, Boehringer D, Ban N, Bukau B 2009. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16:589–97
    [Google Scholar]
  13. 13. 
    Yang C-I, Hsieh H-H, Shan S-O 2019. Timing and specificity of cotranslational nascent protein modification in bacteria. PNAS 116:23050–60
    [Google Scholar]
  14. 14. 
    Patzelt H, Rüdiger S, Brehmer D, Kramer G, Vorderwülbecke S et al. 2001. Binding specificity of Escherichia coli trigger factor. PNAS 98:14244–49
    [Google Scholar]
  15. 15. 
    Kaiser CM, Chang H-C, Agashe VR, Lakshmipathy SK, Etchells SA et al. 2006. Real-time observation of trigger factor function on translating ribosomes. Nature 444:455–60
    [Google Scholar]
  16. 16. 
    Stein KC, Kriel A, Frydman J 2019. Nascent polypeptide domain topology and elongation rate direct the cotranslational hierarchy of Hsp70 and TRiC/CCT. Mol. Cell 75:1117–30
    [Google Scholar]
  17. 17. 
    Schibich D, Gloge F, Pöhner I, Björkholm P, Wade RC et al. 2016. Global profiling of SRP interaction with nascent polypeptides. Nature 536:219–23
    [Google Scholar]
  18. 18. 
    Berndt U, Oellerer S, Zhang Y, Johnson AE, Rospert S 2009. A signal-anchor sequence stimulates signal recognition particle binding to ribosomes from inside the exit tunnel. PNAS 106:1398–403
    [Google Scholar]
  19. 19. 
    Brandman O, Hegde RS. 2016. Ribosome-associated protein quality control. Nat. Struct. Mol. Biol. 23:7–15
    [Google Scholar]
  20. 20. 
    Wang F, Canadeo LA, Huibregtse JM 2015. Ubiquitination of newly synthesized proteins at the ribosome. Biochimie 114:127–33
    [Google Scholar]
  21. 21. 
    Turner GC, Varshavsky A. 2000. Detecting and measuring cotranslational protein degradation in vivo. Science 289:2117–20
    [Google Scholar]
  22. 22. 
    Shiber A, Döring K, Friedrich U, Klann K, Merker D et al. 2018. Cotranslational assembly of protein complexes in eukaryotes revealed by ribosome profiling. Nature 561:268–72
    [Google Scholar]
  23. 23. 
    Shieh Y-W, Minguez P, Bork P, Auburger JJ, Guilbride DL et al. 2015. Operon structure and cotranslational subunit association direct protein assembly in bacteria. Science 350:678–80
    [Google Scholar]
  24. 24. 
    Marino J, Buholzer KJ, Zosel F, Nettels D, Schuler B 2018. Charge interactions can dominate coupled folding and binding on the ribosome. Biophys. J. 115:996–1006
    [Google Scholar]
  25. 25. 
    Borman S. 2007. Protein baby pictures. Chem. Eng. News 85:56–57
    [Google Scholar]
  26. 26. 
    Pauling L, Corey RB, Branson HR 1951. The structure of proteins: two hydrogen-bonded helical configurations of the polypeptide chain. PNAS 37:205–11
    [Google Scholar]
  27. 27. 
    Cassaignau AME, Launay HMM, Karyadi M-E, Wang X, Waudby CA et al. 2016. A strategy for co-translational folding studies of ribosome-bound nascent chain complexes using NMR spectroscopy. Nat. Protoc. 11:1492–507
    [Google Scholar]
  28. 28. 
    Ito K, Chiba S. 2013. Arrest peptides: cis-acting modulators of translation. Annu. Rev. Biochem. 82:171–202
    [Google Scholar]
  29. 29. 
    Kelkar DA, Khushoo A, Yang Z, Skach WR 2012. Kinetic analysis of ribosome-bound fluorescent proteins reveals an early, stable, cotranslational folding intermediate. J. Biol. Chem. 287:2568–78
    [Google Scholar]
  30. 30. 
    Kim SJ, Yoon JS, Shishido H, Yang Z, Rooney LA et al. 2015. Translational tuning optimizes nascent protein folding in cells. Science 348:444–48
    [Google Scholar]
  31. 31. 
    Nogales E, Scheres SHW. 2015. Cryo-EM: a unique tool for the visualization of macromolecular complexity. Mol. Cell 58:677–89
    [Google Scholar]
  32. 32. 
    Waudby CA, Launay H, Cabrita LD, Christodoulou J 2013. Protein folding on the ribosome studied using NMR spectroscopy. Prog. Nucl. Magn. Reson. Spectrosc. 74:57–75
    [Google Scholar]
  33. 33. 
    Cabrita LD, Cassaignau AME, Launay HMM, Waudby CA, Wlodarski T et al. 2016. A structural ensemble of a ribosome–nascent chain complex during cotranslational protein folding. Nat. Struct. Mol. Biol. 23:278–85
    [Google Scholar]
  34. 34. 
    Su T, Cheng J, Sohmen D, Hedman R, Berninghausen O et al. 2017. The force-sensing peptide VemP employs extreme compaction and secondary structure formation to induce ribosomal stalling. eLife 6:e25642
    [Google Scholar]
  35. 35. 
    Nilsson OB, Hedman R, Marino J, Wickles S, Bischoff L et al. 2015. Cotranslational protein folding inside the ribosome exit tunnel. Cell Rep 12:1533–40
    [Google Scholar]
  36. 36. 
    Tsalkova T, Odom OW, Kramer G, Hardesty B 1998. Different conformations of nascent peptides on ribosomes. J. Mol. Biol. 278:713–23
    [Google Scholar]
  37. 37. 
    Kleizen B, van Vlijmen T, de Jonge HR, Braakman I 2005. Folding of CFTR is predominantly cotranslational. Mol. Cell 20:277–87
    [Google Scholar]
  38. 38. 
    Samelson AJ, Jensen MK, Soto RA, Cate JHD, Marqusee S 2016. Quantitative determination of ribosome nascent chain stability. PNAS 113:13402–7
    [Google Scholar]
  39. 39. 
    Samelson AJ, Bolin E, Costello SM, Sharma AK, O'Brien EP et al. 2018. Kinetic and structural comparison of a protein's cotranslational folding and refolding pathways. Sci. Adv. 4:eaas9098
    [Google Scholar]
  40. 40. 
    Holtkamp W, Kokic G, Jäger M, Mittelstaet J, Komar AA et al. 2015. Cotranslational protein folding on the ribosome monitored in real time. Science 350:1104–7
    [Google Scholar]
  41. 41. 
    Dao Duc K, Batra SS, Bhattacharya N, Cate JHD, Song YS 2019. Differences in the path to exit the ribosome across the three domains of life. Nucleic Acids Res 47:4198–210
    [Google Scholar]
  42. 42. 
    Voss NR, Gerstein M, Steitz TA, Moore PB 2006. The geometry of the ribosomal polypeptide exit tunnel. J. Mol. Biol. 360:893–906
    [Google Scholar]
  43. 43. 
    Ziv G, Haran G, Thirumalai D 2005. Ribosome exit tunnel can entropically stabilize α-helices. PNAS 102:18956–61
    [Google Scholar]
  44. 44. 
    Lu J, Deutsch C. 2005. Folding zones inside the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 12:1123–29
    [Google Scholar]
  45. 45. 
    Woolhead CA, McCormick PJ, Johnson AE 2004. Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 116:725–36
    [Google Scholar]
  46. 46. 
    Bhushan S, Gartmann M, Halic M, Armache J-P, Jarasch A et al. 2010. α-Helical nascent polypeptide chains visualized within distinct regions of the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 17:313–17
    [Google Scholar]
  47. 47. 
    Bañó-Polo M, Baeza-Delgado C, Tamborero S, Hazel A, Grau B et al. 2018. Transmembrane but not soluble helices fold inside the ribosome tunnel. Nat. Commun. 9:5246
    [Google Scholar]
  48. 48. 
    O'Brien EP, Hsu S-TD, Christodoulou J, Vendruscolo M, Dobson CM 2010. Transient tertiary structure formation within the ribosome exit port. J. Am. Chem. Soc. 132:16928–37
    [Google Scholar]
  49. 49. 
    Kosolapov A, Deutsch C. 2009. Tertiary interactions within the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 16:405–11
    [Google Scholar]
  50. 50. 
    Goldman DH, Kaiser CM, Milin A, Righini M, Tinoco I Jr et al. 2015. Mechanical force releases nascent chain–mediated ribosome arrest in vitro and in vivo. Science 348:457–60
    [Google Scholar]
  51. 51. 
    Farías-Rico JA, Ruud Selin F, Myronidi I, Frühauf M, von Heijne G 2018. Effects of protein size, thermodynamic stability, and net charge on cotranslational folding on the ribosome. PNAS 115:E9280–87
    [Google Scholar]
  52. 52. 
    Kemp G, Kudva R, de la Rosa A, von Heijne G 2019. Force-profile analysis of the cotranslational folding of HemK and filamin domains: comparison of biochemical and biophysical folding assays. J. Mol. Biol. 431:1308–14
    [Google Scholar]
  53. 53. 
    Notari L, Martínez-Carranza M, Farías-Rico JA, Stenmark P, von Heijne G 2018. Cotranslational folding of a pentarepeat β-helix protein. J. Mol. Biol. 430:5196–206
    [Google Scholar]
  54. 53a. 
    Jensen MK, Samelson AJ, Steward A, Clarke J, Marqusee S 2020. The folding and unfolding behavior of ribonuclease H on the ribosome. bioRxiv 2020.04.16.044867 https://doi.org/10.1101/2020.04.16.044867
    [Crossref]
  55. 54. 
    Ismail N, Hedman R, Lindén M, von Heijne G 2015. Charge-driven dynamics of nascent-chain movement through the SecYEG translocon. Nat. Struct. Mol. Biol. 22:145–49
    [Google Scholar]
  56. 55. 
    Yap M-N, Bernstein HD. 2011. The translational regulatory function of SecM requires the precise timing of membrane targeting. Mol. Microbiol. 81:540–53
    [Google Scholar]
  57. 56. 
    Evans MS, Sander IM, Clark PL 2008. Cotranslational folding promotes β-helix formation and avoids aggregation in vivo. J. Mol. Biol. 383:683–92
    [Google Scholar]
  58. 57. 
    Nilsson OB, Nickson AA, Hollins JJ, Wickles S, Steward A et al. 2017. Cotranslational folding of spectrin domains via partially structured states. Nat. Struct. Mol. Biol. 24:221–25
    [Google Scholar]
  59. 58. 
    Kaiser CM, Goldman DH, Chodera JD, Tinoco I, Bustamante C 2011. The ribosome modulates nascent protein folding. Science 334:1723–27
    [Google Scholar]
  60. 59. 
    Alexander LM, Goldman DH, Wee LM, Bustamante C 2019. Non-equilibrium dynamics of a nascent polypeptide during translation suppress its misfolding. Nat. Commun. 10:2709
    [Google Scholar]
  61. 60. 
    Ban N, Nissen P, Hansen J, Moore PB, Steitz TA 2000. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289:905–20
    [Google Scholar]
  62. 61. 
    Schluenzen F, Tocilj A, Zarivach R, Harms J, Gluehmann M et al. 2000. Structure of functionally activated small ribosomal subunit at 3.3 Å resolution. Cell 102:615–23
    [Google Scholar]
  63. 62. 
    Brown A, Shao S. 2018. Ribosomes and cryo-EM: a duet. Curr. Opin. Struct. Biol. 52:1–7
    [Google Scholar]
  64. 63. 
    Serber Z, Corsini L, Durst F, Dötsch V 2005. In-cell NMR spectroscopy. Meth. Enzymol. 394:17–41
    [Google Scholar]
  65. 64. 
    Deckert A, Waudby CA, Wlodarski T, Wentink AS, Wang X et al. 2016. Structural characterization of the interaction of α-synuclein nascent chains with the ribosomal surface and trigger factor. PNAS 113:5012–17
    [Google Scholar]
  66. 65. 
    Lange S, Franks WT, Rajagopalan N, Döring K, Geiger MA et al. 2016. Structural analysis of a signal peptide inside the ribosome tunnel by DNP MAS NMR. Sci. Adv. 2:e1600379
    [Google Scholar]
  67. 66. 
    Tian P, Steward A, Kudva R, Su T, Shilling PJ et al. 2018. Folding pathway of an Ig domain is conserved on and off the ribosome. PNAS 115:E11284–93
    [Google Scholar]
  68. 67. 
    Deeng J, Chan KY, van der Sluis EO 2016. Dynamic behavior of trigger factor on the ribosome. J. Mol. Biol. 428:3588–602
    [Google Scholar]
  69. 68. 
    Zhang Y, Ma C, Yuan Y, Zhu J, Li N et al. 2014. Structural basis for interaction of a cotranslational chaperone with the eukaryotic ribosome. Nat. Struct. Mol. Biol. 21:1042–46
    [Google Scholar]
  70. 69. 
    Schaffitzel C, Oswald M, Berger I, Ishikawa T 2006. Structure of the E. coli signal recognition particle bound to a translating ribosome. Nature 444:503–6
    [Google Scholar]
  71. 70. 
    Becker T, Bhushan S, Jarasch A, Armache J-P, Funes S et al. 2009. Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 326:1369–73
    [Google Scholar]
  72. 71. 
    Frauenfeld J, Gumbart J, van der Sluis EO, Funes S, Gartmann M et al. 2011. Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nat. Struct. Mol. Biol. 18:614–21
    [Google Scholar]
  73. 72. 
    Voorhees RM, Fernandez IS, Scheres SHW, Hegde RS 2014. Structure of the mammalian ribosome-Sec61 complex to 3.4 Å resolution. Cell 157:1632–43
    [Google Scholar]
  74. 73. 
    Gogala M, Becker T, Beatrix B, Armache J-P, Barrio-Garcia C et al. 2014. Structures of the Sec61 complex engaged in nascent peptide translocation or membrane insertion. Nature 506:107–10
    [Google Scholar]
  75. 74. 
    Bischoff L, Berninghausen O, Beckmann R 2014. Molecular basis for the ribosome functioning as an L-tryptophan sensor. Cell Rep 9:469–75
    [Google Scholar]
  76. 75. 
    Bhushan S, Hoffmann T, Seidelt B, Frauenfeld J, Mielke T et al. 2011. SecM-stalled ribosomes adopt an altered geometry at the peptidyl transferase center. PLOS Biol 9:e1000581
    [Google Scholar]
  77. 76. 
    Shanmuganathan V, Schiller N, Magoulopoulou A, Cheng J, Braunger K et al. 2019. Structural and mutational analysis of the ribosome-arresting human XBP1u. eLife 8:e46267
    [Google Scholar]
  78. 77. 
    Matheisl S, Berninghausen O, Becker T, Beckmann R 2015. Structure of a human translation termination complex. Nucleic Acids Res 43:8615–26
    [Google Scholar]
  79. 78. 
    Javed A, Cabrita LD, Cassaignau AME, Wlodarski T, Christodoulou J, Orlova EV 2019. Visualising nascent chain dynamics at the ribosome exit tunnel by cryo-electron microscopy. bioRxiv 722611. https://doi.org/10.1101/722611
    [Crossref]
  80. 79. 
    Mulder FAA, Bouakaz L, Lundell A, Venkataramana M, Liljas A et al. 2004. Conformation and dynamics of ribosomal stalk protein L12 in solution and on the ribosome. Biochemistry 43:5930–36
    [Google Scholar]
  81. 80. 
    Christodoulou J, Larsson G, Fucini P, Connell SR, Pertinhez TA et al. 2004. Heteronuclear NMR investigations of dynamic regions of intact Escherichia coli ribosomes. PNAS 101:10949–54
    [Google Scholar]
  82. 81. 
    Wang X, Kirkpatrick JP, Launay HMM, de Simone A, Häussinger D et al. 2019. Probing the dynamic stalk region of the ribosome using solution NMR. Sci. Rep. 9:567–69
    [Google Scholar]
  83. 82. 
    Eichmann C, Preissler S, Riek R, Deuerling E 2010. Cotranslational structure acquisition of nascent polypeptides monitored by NMR spectroscopy. PNAS 107:9111–16
    [Google Scholar]
  84. 83. 
    Rutkowska A, Beerbaum M, Rajagopalan N, Fiaux J, Schmieder P et al. 2009. Large-scale purification of ribosome-nascent chain complexes for biochemical and structural studies. FEBS Lett 583:2407–13
    [Google Scholar]
  85. 84. 
    Chan SHS, Waudby CA, Cassaignau AME, Cabrita LD, Christodoulou J 2015. Increasing the sensitivity of NMR diffusion measurements by paramagnetic longitudinal relaxation enhancement, with application to ribosome–nascent chain complexes. J. Biomol. NMR 63:151–63
    [Google Scholar]
  86. 85. 
    Deleted in proof
  87. 86. 
    Bock LV, Kolář MH, Grubmüller H 2018. Molecular simulations of the ribosome and associated translation factors. Curr. Opin. Struct. Biol. 49:27–35
    [Google Scholar]
  88. 87. 
    O'Brien EP, Vendruscolo M, Dobson CM 2012. Prediction of variable translation rate effects on cotranslational protein folding. Nat. Commun. 3:868
    [Google Scholar]
  89. 88. 
    O'Brien EP, Ciryam P, Vendruscolo M, Dobson CM 2014. Understanding the influence of codon translation rates on cotranslational protein folding. Acc. Chem. Res. 47:1536–44
    [Google Scholar]
  90. 89. 
    Gumbart J, Trabuco LG, Schreiner E, Villa E, Schulten K 2009. Regulation of the protein-conducting channel by a bound ribosome. Structure 17:1453–64
    [Google Scholar]
  91. 90. 
    Camilloni C, Cavalli A, Vendruscolo M 2013. Replica-averaged metadynamics. J. Chem. Theory Comput. 9:5610–17
    [Google Scholar]
  92. 91. 
    Shen Y, Lange O, Delaglio F, Rossi P, Aramini JM et al. 2008. Consistent blind protein structure generation from NMR chemical shift data. PNAS 105:4685–90
    [Google Scholar]
  93. 92. 
    Clore GM, Iwahara J. 2009. Theory, practice, and applications of paramagnetic relaxation enhancement for the characterization of transient low-population states of biological macromolecules and their complexes. Chem. Rev. 109:4108–39
    [Google Scholar]
  94. 93. 
    Robustelli P, Kohlhoff K, Cavalli A, Vendruscolo M 2010. Using NMR chemical shifts as structural restraints in molecular dynamics simulations of proteins. Structure 18:923–33
    [Google Scholar]
  95. 94. 
    Sanbonmatsu KY, Tung CS. 2007. High performance computing in biology: multimillion atom simulations of nanoscale systems. J. Struct. Biol. 157:470–80
    [Google Scholar]
  96. 95. 
    Trovato F, O'Brien EP. 2016. Insights into cotranslational nascent protein behavior from computer simulations. Annu. Rev. Biophys. 45:345–69
    [Google Scholar]
  97. 95a. 
    Senior AW, Evans R, Jumper J, Kirkpatrick J, Sifre Let al. 2020. Improved protein structure prediction using potentials from deep learning. Nature 577:70610
    [Google Scholar]
  98. 96. 
    Liu K, Rehfus JE, Mattson E, Kaiser CM 2017. The ribosome destabilizes native and non-native structures in a nascent multidomain protein. Protein Sci 26:1439–51
    [Google Scholar]
  99. 97. 
    Toal S, Schweitzer-Stenner R. 2014. Local order in the unfolded state: conformational biases and nearest neighbor interactions. Biomolecules 4:725–73
    [Google Scholar]
  100. 98. 
    Robustelli P, Piana S, Shaw DE 2018. Developing a molecular dynamics force field for both folded and disordered protein states. PNAS 115:E4758–66
    [Google Scholar]
  101. 99. 
    Bowler BE. 2012. Residual structure in unfolded proteins. Curr. Opin. Struct. Biol. 22:4–13
    [Google Scholar]
  102. 100. 
    Waudby CA, Wlodarski T, Karyadi M-E, Cassaignau AME, Chan SHS et al. 2018. Systematic mapping of free energy landscapes of a growing filamin domain during biosynthesis. PNAS 115:9744–49
    [Google Scholar]
  103. 101. 
    Neira JL, Fersht AR. 1999. Exploring the folding funnel of a polypeptide chain by biophysical studies on protein fragments. J. Mol. Biol. 285:1309–33
    [Google Scholar]
  104. 102. 
    de Prat Gay G, Ruiz-Sanz J, Neira JL, Corrales FJ, Otzen DE et al. 1995. Conformational pathway of the polypeptide chain of chymotrypsin inhibitor-2 growing from its N terminus in vitro. Parallels with the protein folding pathway. J. Mol. Biol. 254:968–79
    [Google Scholar]
  105. 103. 
    Cruz-Vera LR, Rajagopal S, Squires C, Yanofsky C 2005. Features of ribosome-peptidyl-tRNA interactions essential for tryptophan induction of tna operon expression. Mol. Cell 19:333–43
    [Google Scholar]
  106. 104. 
    Vázquez-Laslop N, Thum C, Mankin AS 2008. Molecular mechanism of drug-dependent ribosome stalling. Mol. Cell 30:190–202
    [Google Scholar]
  107. 105. 
    Youngman EM, Brunelle JL, Kochaniak AB, Green R 2004. The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell 117:589–99
    [Google Scholar]
  108. 106. 
    Knight AM, Culviner PH, Kurt-Yilmaz N, Zou T, Ozkan SB, Cavagnero S 2013. Electrostatic effect of the ribosomal surface on nascent polypeptide dynamics. ACS Chem. Biol. 8:1195–204
    [Google Scholar]
  109. 107. 
    Record MT Jr, Courtenay ES, Cayley DS, Guttman HJ. 1998. Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci. 23:143–48
    [Google Scholar]
  110. 108. 
    Fedyukina DV, Jennaro TS, Cavagnero S 2014. Charge segregation and low hydrophobicity are key features of ribosomal proteins from different organisms. J. Biol. Chem. 289:6740–50
    [Google Scholar]
  111. 109. 
    Selmer M, Dunham CM, Murphy FV IV, Weixlbaumer A, Petry S et al. 2006. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313:1935–42
    [Google Scholar]
  112. 110. 
    Nierhaus KH. 2014. Mg2+, K+, and the ribosome. J. Bacteriol. 196:3817–19
    [Google Scholar]
  113. 111. 
    Chadani Y, Niwa T, Izumi T, Sugata N, Nagao A et al. 2017. Intrinsic ribosome destabilization underlies translation and provides an organism with a strategy of environmental sensing. Mol. Cell 68:528–39
    [Google Scholar]
  114. 112. 
    Turnock G, Birch B. 1973. Binding of putrescine and spermidine to ribosomes from Escherichia coli. FEBS J 33:467–74
    [Google Scholar]
  115. 113. 
    Schavemaker PE, Śmigiel WM, Poolman B 2017. Ribosome surface properties may impose limits on the nature of the cytoplasmic proteome. eLife 6:21
    [Google Scholar]
  116. 114. 
    DeMott CM, Majumder S, Burz DS, Reverdatto S, Shekhtman A 2017. Ribosome mediated quinary interactions modulate in-cell protein activities. Biochemistry 56:4117–26
    [Google Scholar]
  117. 115. 
    Peterson JH, Woolhead CA, Bernstein HD 2010. The conformation of a nascent polypeptide inside the ribosome tunnel affects protein targeting and protein folding. Mol. Microbiol. 78:203–17
    [Google Scholar]
  118. 116. 
    Kudva R, Tian P, Pardo-Avila F, Carroni M, Best RB et al. 2018. The shape of the bacterial ribosome exit tunnel affects cotranslational protein folding. eLife 7:19
    [Google Scholar]
  119. 117. 
    Waudby CA, Dobson CM, Christodoulou J 2019. Nature and regulation of protein folding on the ribosome. Trends Biochem. Sci. 44:P914–26
    [Google Scholar]
  120. 118. 
    Wright CF, Teichmann SA, Clarke J, Dobson CM 2005. The importance of sequence diversity in the aggregation and evolution of proteins. Nature 438:878–81
    [Google Scholar]
  121. 119. 
    Han J-H, Batey S, Nickson AA, Teichmann SA, Clarke J 2007. The folding and evolution of multidomain proteins. Nat. Rev. Mol. Cell Biol. 8:319–30
    [Google Scholar]
  122. 120. 
    Borgia MB, Borgia A, Best RB, Steward A, Nettels D et al. 2011. Single-molecule fluorescence reveals sequence-specific misfolding in multidomain proteins. Nature 474:662–65
    [Google Scholar]
  123. 121. 
    Liu K, Maciuba K, Kaiser CM 2019. The ribosome cooperates with a chaperone to guide multi-domain protein folding. Mol. Cell 74:310–319.e7
    [Google Scholar]
  124. 122. 
    Chow CC, Chow C, Raghunathan V, Huppert TJ, Kimball EB, Cavagnero S 2003. Chain length dependence of apomyoglobin folding: structural evolution from misfolded sheets to native helices. Biochemistry 42:7090–99
    [Google Scholar]
  125. 123. 
    Rüdiger S, Germeroth L, Schneider-Mergener J, Bukau B 1997. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J 16:1501–7
    [Google Scholar]
  126. 124. 
    Su Y, Zou Z, Feng S, Zhou P, Cao L 2007. The acidity of protein fusion partners predominantly determines the efficacy to improve the solubility of the target proteins expressed in Escherichia coli. J. Biotechnol 129:373–82
    [Google Scholar]
  127. 125. 
    Plückthun A. 2011. Ribosome display: a perspective. Ribosome Display and Related Technologies JA Douthwaite, RH Jackson 3–28 Methods Mol. Biol. Ser. 805 New York: Springer
    [Google Scholar]
  128. 126. 
    Camps M, Herman A, Loh E, Loeb LA 2007. Genetic constraints on protein evolution. Crit. Rev. Biochem. Mol. Biol. 42:313–26
    [Google Scholar]
  129. 127. 
    Segev N, Gerst JE. 2018. Specialized ribosomes and specific ribosomal protein paralogs control translation of mitochondrial proteins. J. Cell Biol. 217:117–26
    [Google Scholar]
  130. 128. 
    Melnikov S, Manakongtreecheep K, Söll D 2018. Revising the structural diversity of ribosomal proteins across the three domains of life. Mol. Biol. Evol. 35:1588–98
    [Google Scholar]
  131. 129. 
    Petrov AS, Wood EC, Bernier CR, Norris AM, Brown A, Amunts A 2019. Structural patching fosters divergence of mitochondrial ribosomes. Mol. Biol. Evol. 36:207–19
    [Google Scholar]
  132. 130. 
    Chin JW. 2017. Expanding and reprogramming the genetic code. Nature 550:53–60
    [Google Scholar]
  133. 131. 
    Neumann H, Wang K, Davis L, Garcia-Alai M, Chin JW 2010. Encoding multiple unnatural amino acids via evolution of a quadruplet-decoding ribosome. Nature 464:441–44
    [Google Scholar]
  134. 132. 
    Sander IM, Chaney JL, Clark PL 2014. Expanding Anfinsen's principle: contributions of synonymous codon selection to rational protein design. J. Am. Chem. Soc. 136:858–61
    [Google Scholar]
  135. 133. 
    Zhang G, Ignatova Z. 2011. Folding at the birth of the nascent chain: coordinating translation with co-translational folding. Curr. Opin. Struct. Biol. 21:25–31
    [Google Scholar]
  136. 134. 
    Kurland CG. 1993. Major codon preference: theme and variations. Biochem. Soc. Trans. 21:841–46
    [Google Scholar]
  137. 135. 
    Zhang G, Hubalewska M, Ignatova Z 2009. Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nat. Struct. Mol. Biol. 16:274–80
    [Google Scholar]
  138. 136. 
    Cortazzo P, Cerveñansky C, Marín M, Reiss C, Ehrlich R, Deana A 2002. Silent mutations affect in vivo protein folding in Escherichia coli. Biochem. Biophys. Res. Commun 293:537–41
    [Google Scholar]
  139. 137. 
    Walsh IM, Bowman MA, Soto Santarriaga IF, Rodriguez A, Clark PL 2020. Synonymous codon substitutions perturb cotranslational protein folding in vivo and impair cell fitness. PNAS 117:3528–34
    [Google Scholar]
  140. 138. 
    Zhou M, Guo J, Cha J, Chae M, Chen S et al. 2013. Non-optimal codon usage affects expression, structure and function of clock protein FRQ. Nature 495:111–15
    [Google Scholar]
  141. 139. 
    Buhr F, Jha S, Thommen M, Mittelstaet J, Kutz F et al. 2016. Synonymous codons direct cotranslational folding toward different protein conformations. Mol. Cell 61:341–51
    [Google Scholar]
  142. 140. 
    Jacobs WM, Shakhnovich EI. 2017. Evidence of evolutionary selection for cotranslational folding. PNAS 114:11434–39
    [Google Scholar]
  143. 141. 
    Pechmann S, Frydman J. 2013. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat. Struct. Mol. Biol. 20:237–43
    [Google Scholar]
  144. 142. 
    Sørensen MA, Pedersen S. 1991. Absolute in vivo translation rates of individual codons in Escherichia coli. J. Mol. Biol 222:265–80
    [Google Scholar]
  145. 143. 
    Gardin J, Yeasmin R, Yurovsky A, Cai Y, Skiena S et al. 2014. Measurement of average decoding rates of the 61 sense codons in vivo. eLife 3:e03735
    [Google Scholar]
  146. 144. 
    Nissley DA, Sharma AK, Ahmed N, Friedrich UA, Kramer G et al. 2016. Accurate prediction of cellular co-translational folding indicates proteins can switch from post- to co-translational folding. Nat. Commun. 7:10341
    [Google Scholar]
  147. 145. 
    Kimchi-Sarfaty C, Oh JM, Kim I-W, Sauna ZE, Calcagno AM et al. 2007. A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science 315:525–28
    [Google Scholar]
  148. 146. 
    Tsai C-J, Sauna ZE, Kimchi-Sarfaty C, Ambudkar SV, Gottesman MM, Nussinov R 2008. Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima. J. Mol. Biol. 383:281–91
    [Google Scholar]
  149. 147. 
    Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. PNAS 98:10037–41
    [Google Scholar]
  150. 148. 
    Aitken CE, Puglisi JD. 2010. Following the intersubunit conformation of the ribosome during translation in real time. Nat. Struct. Mol. Biol. 17:793–800
    [Google Scholar]
  151. 149. 
    Chen J, Tsai A, Petrov A, Puglisi JD 2012. Nonfluorescent quenchers to correlate single-molecule conformational and compositional dynamics. J. Am. Chem. Soc. 134:5734–37
    [Google Scholar]
  152. 150. 
    Prabhakar A, Puglisi EV, Puglisi JD 2019. Single-molecule fluorescence applied to translation. Cold Spring Harb. Perspect. Biol. 11:a032714
    [Google Scholar]
  153. 151. 
    Nicola AV, Chen W, Helenius A 1999. Co-translational folding of an alphavirus capsid protein in the cytosol of living cells. Nat. Cell Biol. 1:341–45
    [Google Scholar]
  154. 152. 
    Selenko P, Wagner G. 2007. Looking into live cells with in-cell NMR spectroscopy. J. Struct. Biol. 158:244–53
    [Google Scholar]
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