Dynamic basis of fidelity and speed in translation: Coordinated multistep mechanisms of elongation and termination

Protein Science

Volumn 26, Issue 7, 2017, Pages 1352-1362

  Prabhakar, Arjun ^a,b   Choi, Junhong ^a,b   Wang, Jinfan ^a   Petrov, Alexey ^a   Puglisi, Joseph D ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

elongation; fidelity; mRNA; ribosome; termination; translation; tRNA

Indexed keywords

ELONGATION FACTOR TU; MESSENGER RNA; MOLECULAR MOTOR; PEPTIDYLTRANSFERASE; TRANSFER RNA; STOP CODON;

AMINO ACID SEQUENCE; BINDING AFFINITY; CODON; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENERGY EXPENDITURE; GENETIC CODE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; RIBOSOME SUBUNIT; RNA TRANSLATION; STOP CODON; SYNTHETIC BIOLOGY; TRANSCRIPTION ELONGATION; TRANSCRIPTION TERMINATION; TRANSLATION ELONGATION; ANIMAL; HUMAN; METABOLISM; PHYSIOLOGY; TRANSLATION TERMINATION;

ANIMALS; CODON, TERMINATOR; HUMANS; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; RNA, TRANSFER;

EID: 85019556011     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.3190     Document Type: Review

References (87)

1. Shieh Y-W, Minguez P, Bork P, Auburger JJ, Guilbride DL, Kramer G, Bukau B (2015) Operon structure and cotranslational subunit association direct protein assembly in bacteria. Science 350:678–680.
2. Buhr F, Jha S, Thommen M, Mittelstaet J, Kutz F, Schwalbe H, Rodnina MV, Komar AA (2016) Synonymous codons direct cotranslational folding toward different protein conformations. Mol Cell 61:341–351.
3. Voorhees RM, Ramakrishnan V (2013) Structural basis of the translational elongation cycle. Annu Rev Biochem 82:203–236.
4. Frank J, Gonzalez RL (2010) Structure and dynamics of a processive Brownian motor: the translating ribosome. Annu Rev Biochem 79:381–412.
5. Zaher HS, Green R (2009) Quality control by the ribosome following peptide bond formation. Nature 457:161–166.
6. Edelmann P, Gallant J (1977) On the translational error theory of aging. Proc Natl Acad Sci USA 74:3396–3398.
7. Precup J, Ulrich AK, Roopnarine O, Parker J (1989) Context specific misreading of phenylalanine codons. Mol Gen Genet 218:397–401.
8. Young R, Bremer H (1976) Polypeptide-chain-elongation rate in Escherichia coli B/r as a function of growth rate. Biochem J 160:185–194.
9. Hopfield JJ (1974) Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc Natl Acad Sci USA 71:4135–4139.
10. Ninio J (1975) Kinetic amplification of enzyme discrimination. Biochimie 57:587–595.
11. Ogle JM, Brodersen DE, Clemons WM, Tarry MJ, Carter AP, Ramakrishnan V (2001) Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292:897–902.
12. Ogle JM, Murphy FV, Tarry MJ, Ramakrishnan V (2002) Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111:721–732.
13. Yoshizawa S, Fourmy D, Puglisi JD (1999) Recognition of the codon-anticodon helix by ribosomal RNA. Science 285:1722–1725.
14. Gromadski KB, Rodnina MV (2004) Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol Cell 13:191–200.
15. Juette MF, Terry DS, Wasserman MR, Altman RB, Zhou Z, Zhao H, Blanchard SC (2016) Single-molecule imaging of non-equilibrium molecular ensembles on the millisecond timescale. Nat Methods 13:1–7.
16. Lee T, Blanchard S, Kim H, Puglisi J, Chu S (2007) The role of fluctuations in tRNA selection by the ribosome. Proc Natl Acad Sci USA 104:13661–13665.
17. Johansson M, Zhang J, Ehrenberg M (2012) Genetic code translation displays a linear trade-off between efficiency and accuracy of tRNA selection. Proc Natl Acad Sci USA 109:131–136.
18. Zhang J, Ieong K-W, Johansson M, Ehrenberg M (2015) Accuracy of initial codon selection by aminoacyl-tRNAs on the mRNA-programmed bacterial ribosome. Proc Natl Acad Sci USA 112:9602–9607.
19. Zhang J, Ieong K-W, Mellenius H, Ehrenberg M (2016) Proofreading neutralizes potential error hotspots in genetic code translation by transfer RNAs. RNA 055632.115-.
20. Manickam N, Nag N, Abbasi A, Patel K, Farabaugh PJ (2014) Studies of translational misreading in vivo show that the ribosome very efficiently discriminates against most potential errors. RNA 20:9–15.
21. Blanchard SC Jr RLG, Kim HD, Chu S, Puglisi JD (2004) tRNA selection and kinetic proofreading in translation. Nat Struct Mol Biol 11:1008–1014.
22. Ieong K-W, Uzun Ü, Selmer M, Ehrenberg M (2016) Two proofreading steps amplify the accuracy of genetic code translation. Proc Natl Acad Sci USA 201610917.
23. Noller HF, Hoffarth V, Zimniak L (1992) Unusual resistance of peptidyl transferase to protein extraction procedures. Science 256:1416–1419.
24. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA (2000) The structural basis of ribosome activity in peptide bond synthesis. Science 289:920–930.
25. Selmer M, Dunham CM, Murphy FV, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313:1935–1942.
26. Trobro S, Aqvist J (2008) Role of ribosomal protein L27 in peptidyl transfer. Biochemistry 47:4898–4906.
27. Sievers A, Beringer M, Rodnina MV, Wolfenden R (2004) The ribosome as an entropy trap. Proc Natl Acad Sci USA 101:7897–7901.
28. Trobro S, Aqvist J (2005) Mechanism of peptide bond synthesis on the ribosome. Proc Natl Acad Sci USA 102:12395–12400.
29. Dominissini D, Nachtergaele S, Moshitch-Moshkovitz S, Peer E, Kol N, Ben-Haim MS, Dai Q, Di Segni A, Salmon-Divon M, Clark WC, Zheng G, Pan T, Solomon O, Eyal E, Hershkovitz V, Han D, Doré LC, Amariglio N, Rechavi G, He C (2016) The dynamic N1-methyladenosine methylome in eukaryotic messenger RNA. Nature 530:441–446.
30. Meyer KD, Saletore Y, Zumbo P, Elemento O, Mason CE, Jaffrey SR (2012) Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell 149:1635–1646.
31. Schwartz S, Bernstein DA, Mumbach MR, Jovanovic M, Herbst RH, León-Ricardo BX, Engreitz JM, Guttman M, Satija R, Lander ES, Fink G, Regev A (2014) Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell 159:148–162.
32. Carlile TM, Rojas-Duran MF, Zinshteyn B, Shin H, Bartoli KM, Gilbert WV (2014) Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature 515:143–146.
33. Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L, Osenberg S, Cesarkas K, Jacob-Hirsch J, Amariglio N, Kupiec M, Sorek R, Rechavi G (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485:201–206.
34. Choi J, Ieong K-W, Demirci H, Chen J, Petrov A, Prabhakar A, O'Leary SE, Dominissini D, Rechavi G, Soltis SM, Ehrenberg M, Puglisi JD (2016) N6-methyladenosine in mRNA disrupts tRNA selection and translation-elongation dynamics. Nat Struct Mol Biol.
35. Slobodin B, Han R, Calderone V, Vrielink JAFO, Loayza-puch F, Elkon R, Agami R, Methylation N (2017) Transcription impacts the efficiency of mRNA translation via co-transcriptional N6-adenosine article transcription impacts the efficiency of mRNA translation via co-transcriptional. Cell 169:326–337.
36. Navon SP, Kornberg G, Chen J, Schwartzman T, Tsai A, Puglisi EV, Puglisi JD, Adir N (2016) Amino acid sequence repertoire of the bacterial proteome and the occurrence of untranslatable sequences. Proc Natl Acad Sci USA 113:7166–7170.
37. Tsai A, Kornberg G, Johansson M, Chen J, Puglisi J (2014) The dynamics of SecM-induced translational stalling. Cell Rep 7:1521–1533.
38. Marks J, Kannan K, Roncase EJ, Klepacki D, Kefi A, Orelle C, Vázquez-Laslop N, Mankin AS (2016) Context-specific inhibition of translation by ribosomal antibiotics targeting the peptidyl transferase center. Proc Natl Acad Sci USA 113:12150–12155.
39. Kannan K, Kanabar P, Schryer D, Florin T, Oh E, Bahroos N, Tenson T, Weissman JS, Mankin AS (2014) The general mode of translation inhibition by macrolide antibiotics. Proc Natl Acad Sci USA 111:15958–15963.
40. Johansson M, Chen J, Tsai A, Kornberg G, Puglisi JD (2014) Sequence-dependent elongation dynamics on macrolide-bound ribosomes. Cell Rep 7:1534–1546.
41. Richter JD, Coller J (2015) Pausing on polyribosomes: make way for elongation in translational control. Cell 163:292–300.
42. Sharma H, Adio S, Senyushkina T, Belardinelli R, Peske F, Rodnina MV [YEAR] Kinetics of spontaneous and EF-G-accelerated rotation of ribosomal subunits. Cell Rep [VOL:PAGE #S].
43. Frank J, Agrawal RK (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406:318–322.
44. Valle M, Zavialov A, Sengupta J, Rawat U, Ehrenberg M, Frank J (2003) Locking and unlocking of ribosomal motions. Cell 114:123–134.
45. Spiegel PC, Ermolenko DN, Noller HF (2007) Elongation factor G stabilizes the hybrid-state conformation of the 70S ribosome. RNA 13:1473–1482.
46. Tourigny DS, Fernández IS, Kelley AC, Ramakrishnan V (2013) Elongation factor G bound to the ribosome in an intermediate state of translocation. Science 340:10.1126/science.1235490.
47. Brilot AF, Korostelev AA, Ermolenko DN, Grigorieff N (2013) Structure of the ribosome with elongation factor G trapped in the pretranslocation state. Proc Natl Acad Sci USA 110:20994–20999.
48. Guo Z, Noller HF (2012) Rotation of the head of the 30S ribosomal subunit during mRNA translocation. Proc Natl Acad Sci USA 109:20391–20394.
49. Zhou J, Lancaster L, Donohue JP, Noller HF (2014) How the ribosome hands the A-site tRNA to the P site during EF-G–catalyzed translocation. Science 345:1188–1191.
50. Marshall RA, Dorywalska M, Puglisi JD (2008) Irreversible chemical steps control intersubunit dynamics during translation. Proc Natl Acad Sci USA 105:15364–15369.
51. Chen J, Petrov A, Tsai A, O'Leary SE, Puglisi JD (2013) Coordinated conformational and compositional dynamics drive ribosome translocation. Nat Struct Mol Biol 20:718–727.
52. Ermolenko DN, Majumdar ZK, Hickerson RP, Spiegel PC, Clegg RM, Noller HF (2007) Observation of intersubunit movement of the ribosome in solution using FRET. J Mol Biol 370:530–540.
53. Liu T, Kaplan A, Alexander L, Yan S, Wen J-D, Lancaster L, Wickersham CE, Fredrick K, Noller H, Tinoco Jr I, Bustamante CJ (2014) Direct measurement of the mechanical work during translocation by the ribosome. Elife 3:e03406.
54. Wen J-D, Lancaster L, Hodges C, Zeri A-C, Yoshimura SH, Noller HF, Bustamante C, Tinoco I (2008) Following translation by single ribosomes one codon at a time. Nature 452:598–603.
55. Aitken CE, Puglisi JD (2010) Following the intersubunit conformation of the ribosome during translation in real time. Nat Struct Mol Biol 17:793–800.
56. Cornish PV, Ermolenko DN, Noller HF, Ha T (2008) Spontaneous intersubunit rotation in single ribosomes. Mol Cell 30:578–588.
57. Sørensen MA, Pedersen S (1991) Absolute in vivo translation rates of individual codons in Escherichia coli. J Mol Biol 222:265–280.
58. Zhu M, Dai X, Wang Y-P (2016) Real time determination of bacterial in vivo ribosome translation elongation speed based on LacZα complementation system. Nucleic Acids Res 44:e155.
59. Rodnina MV, Savelsbergh A, Katunin VI, Wintermeyer W (1997) Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature 385:37–41.
60. Holtkamp W, Cunha CE, Peske F, Konevega AL, Wintermeyer W, Rodnina MV (2014) GTP hydrolysis by EF-G synchronizes tRNA movement on small and large ribosomal subunits. EMBO J 33: 1073 LP-1085.
61. Cunha CE, Belardinelli R, Peske F, Holtkamp W, Wintermeyer W, Rodnina MV (2013) Dual use of GTP hydrolysis by elongation factor G on the ribosome. Translation 1:e24315.
62. Gordon J (1970) Regulation of the in vivo synthesis of the polypeptide chain elongation factors in Escherichia coli. Biochemistry 9:912–917.
63. Bakshi S, Siryaporn A, Goulian M, Weisshaar JC (2012) Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Mol Microbiol 85:21–38.
64. Petrov AS, Bernier CR, Hsiao C, Norris AM, Kovacs NA, Waterbury CC, Stepanov VG, Harvey SC, Fox GE, Wartell RM, Hud NV, Williams LD (2014) Evolution of the ribosome at atomic resolution. Proc Natl Acad Sci USA 111:10251–10256.
65. Petrov AS, Gulen B, Norris AM, Kovacs NA, Bernier CR, Lanier KA, Fox GE, Harvey SC, Wartell RM, Hud NV, Williams LD (2015) History of the ribosome and the origin of translation. Proc Natl Acad Sci USA [VOL:PAGE #S].
66. Rodriguez-Correa D, Dahlberg AE (2008) Kinetic and thermodynamic studies of peptidyltransferase in ribosomes from the extreme thermophile Thermus thermophilus. RNA 14:2314–2318.
67. Chen C, Cui X, Beausang JF, Zhang H, Farrell I, Cooperman BS, Goldman YE (2016) Elongation factor G initiates translocation through a power stroke. Proc Natl Acad Sci 113:7515–7520.
68. Margus T, Remm M, Tenson T (2007) Phylogenetic distribution of translational GTPases in bacteria. BMC Genomics 8:15.
69. Grentzmann G, Brechemier-Baey D, Heurgue V, Mora L, Buckingham RH (1994) Localization and characterization of the gene encoding release factor RF3 in Escherichia coli. Proc Natl Acad Sci USA 91:5848–5852.
70. O'Connor M (2015) Interactions of release factor RF3 with the translation machinery. Mol Genet Genomics 290:1335–1344.
71. Freistroffer DV, Pavlov MY, MacDougall J, Buckingham RH, Ehrenberg M (1997) Release factor RF3 in E.coli accelerates the dissociation of release factors RF1 and RF2 from the ribosome in a GTP-dependent manner. EMBO J 16:4126–4133.
72. Jørgensen F, Adamski FM, Tate WP, Kurland CG (1993) Release factor-dependent false stops are infrequent in Escherichia coli. J Mol Biol 230:41–50.
73. Parker J (1989) Errors and alternatives in reading the universal genetic code. Microbiol Rev 53:273–298.
74. Ito K, Uno M, Nakamura Y (2000) A tripeptide “anticodon” deciphers stop codons in messenger RNA. Nature 403:680–684.
75. Frolova LY, Tsivkovskii RY, Sivolobova GF, Oparina NY, Serpinsky OI, Blinov VM, Tatkov SI, Kisselev LL (1999) Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis. RNA 5:1014–1020.
76. Freistroffer DV, Kwiatkowski M, Buckingham RH, Ehrenberg M (2000) The accuracy of codon recognition by polypeptide release factors. Proc Natl Acad Sci USA 97:2046–2051.
77. Shin DH, Brandsen J, Jancarik J, Yokota H, Kim R, Kim S-H (2004) Structural analyses of peptide release factor 1 from Thermotoga maritima reveal domain flexibility required for its interaction with the ribosome. J Mol Biol 341:227–239.
78. Vestergaard B, Van LB, Andersen GR, Nyborg J, Buckingham RH, Kjeldgaard M (2001) Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol Cell 8:1375–1382.
79. Klaholz BP, Pape T, Zavialov AV, Myasnikov AG, Orlova EV, Vestergaard B, Ehrenberg M, van Heel M (2003) Structure of the Escherichia coli ribosomal termination complex with release factor 2. Nature 421:90–94.
80. Korostelev A, Asahara H, Lancaster L, Laurberg M, Hirschi A, Zhu J, Trakhanov S, Scott WG, Noller HF (2008) Crystal structure of a translation termination complex formed with release factor RF2. Proc Natl Acad Sci 105:19684–19689.
81. Laurberg M, Asahara H, Korostelev A, Zhu J, Trakhanov S, Noller HF (2008) Structural basis for translation termination on the 70S ribosome. Nature 454:852–857.
82. Hetrick B, Lee K, Joseph S (2009) Kinetics of stop codon recognition by release factor 1. Biochemistry 48:11178–11184.
83. Trappl K, Joseph S (2016) Ribosome induces a closed to open conformational change in release factor 1. J Mol Biol 428:1333–1344.
84. Sund J, Andér M, Åqvist J (2010) Principles of stop-codon reading on the ribosome. Nature 465:947–950.
85. Pierson WE, Hoffer ED, Keedy HE, Simms CL, Dunham CM, Zaher HS (2016) Uniformity of peptide release is maintained by methylation of release factors. Cell Rep 17:11–18.
86. Zavialov AV, Mora L, Buckingham RH, Ehrenberg M (2002) Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3. Mol Cell 10:789–798.
87. Trobro S, Åqvist J (2007) A model for how ribosomal release factors induce peptidyl-tRNA cleavage in termination of protein synthesis. Mol Cell 27:758–766.