New structural insights into the decoding mechanism: Translation infidelity via a G·U pair with Watson-Crick geometry

FEBS Letters

Volumn 587, Issue 13, 2013, Pages 1848-1857

  Demeshkina, Natalia ^a,b,c   Jenner, Lasse ^a,b,c,d   Westhof, Eric ^a   Yusupov, Marat ^a,b,c   Yusupova, Gulnara ^a,b,c  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b CNRS   (France)

^c INSERM   (France)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

Keyword Ribosome decoding tRNA selection

Indexed keywords

AMINOACYL TRANSFER RNA; GUANINE; MESSENGER RNA; RIBOSOME RNA; TRANSFER RNA; URACIL;

ANTICODON; BASE PAIRING; CODON; CRYSTALLOGRAPHY; DNA STRUCTURE; ENERGY EXPENDITURE; GENETIC CODE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; RIBOSOME; RNA CONFORMATION; RNA TRANSLATION;

BASE PAIRING; CODON; CRYSTALLOGRAPHY, X-RAY; GENETIC CODE; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RIBOSOMES;

EID: 84878947991     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.05.009     Document Type: Review

References (79)

1. S. Melnikov One core, two shells: bacterial and eukaryotic ribosomes Nat. Struct. Mol. Biol. 19 2012 560 567
2. K.B. Gromadski, T. Daviter, and M.V. Rodnina A uniform response to mismatches in codon-anticodon complexes ensures ribosomal fidelity Mol. Cell 21 2006 369 377
3. H.S. Zaher, and R. Green Quality control by the ribosome following peptide bond formation Nature 457 2009 161 166
4. E.B. Kramer, and P.J. Farabaugh The frequency of translational misreading errors in E. coli is largely determined by tRNA competition RNA 13 2007 87 96
5. J.J. Hopfield Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity Proc. Natl. Acad. Sci. USA 71 1974 4135 4139
6. J. Ninio Kinetic amplification of enzyme discrimination Biochimie 57 1975 587 595
7. R.C. Thompson, and P.J. Stone Proofreading of the codon-anticodon interaction on ribosomes Proc. Natl. Acad. Sci. USA 74 1977 198 202
8. H.F. Noller Biochemical characterization of the ribosomal decoding site Biochimie 88 2006 935 941
9. D. Moazed, and H.F. Noller Binding of tRNA to the ribosomal A and P sites protects two distinct sets of nucleotides in 16 S rRNA J. Mol. Biol. 211 1990 135 145
10. D. Moazed, and H.F. Noller Interaction of antibiotics with functional sites in 16S ribosomal RNA Nature 327 1987 389 394
11. T. Powers, and H.F. Noller Dominant lethal mutations in a conserved loop in 16S rRNA Proc. Natl. Acad. Sci. USA 87 1990 1042 1046
12. T. Powers, and H.F. Noller Selective perturbation of G530 of 16 S rRNA by translational miscoding agents and a streptomycin-dependence mutation in protein S12 J. Mol. Biol. 235 1994 156 172
13. D. Fourmy, M.I. Recht, S.C. Blanchard, and J.D. Puglisi Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic Science 274 1996 1367 1371
14. D. Fourmy, S. Yoshizawa, and J.D. Puglisi Paromomycin binding induces a local conformational change in the A-site of 16 S rRNA J. Mol. Biol. 277 1998 333 345
15. Q. Vicens, and E. Westhof Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site Structure 9 2001 647 658
16. T. Pape, W. Wintermeyer, and M. Rodnina Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome EMBO J. 18 1999 3800 3807
17. J.M. Ogle Recognition of cognate transfer RNA by the 30S ribosomal subunit Science 292 2001 897 902
18. J.M. Ogle, F.V. Murphy, M.J. Tarry, and V. Ramakrishnan Selection of tRNA by the ribosome requires a transition from an open to a closed form Cell 111 2002 721 732
19. H. Stark Visualization of elongation factor Tu on the Escherichia coli ribosome Nature 389 1997 403 406
20. M. Valle Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process EMBO J. 21 2002 3557 3567
21. H. Stark Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex Nat. Struct. Biol. 9 2002 849 854
22. M. Valle Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy Nat. Struct. Biol. 10 2003 899 906
23. E. Villa Ribosome-induced changes in elongation factor Tu conformation control GTP hydrolysis Proc. Natl. Acad. Sci. USA 106 2009 1063 1068
24. T.M. Schmeing The Crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA Science 326 2009 688 694
25. R.M. Voorhees, T.M. Schmeing, A.C. Kelley, and V. Ramakrishnan The mechanism for activation of GTP hydrolysis on the ribosome Science 330 2010 835 838
26. M. Johansson, M. Lovmar, and M. Ehrenberg Rate and accuracy of bacterial protein synthesis revisited Curr. Opin. Microbiol. 11 2008 141 147
27. I. Wohlgemuth, C. Pohl, J. Mittelstaet, A.L. Konevega, and M.V. Rodnina Evolutionary optimization of speed and accuracy of decoding on the ribosome Philos. Trans. R. Soc. Lond. B Biol. Sci. 366 2011 2979 2986
28. T.M. Schmeing, and V. Ramakrishnan What recent ribosome structures have revealed about the mechanism of translation Nature 461 2009 1234 1242
29. H.S. Zaher, and R. Green Fidelity at the molecular level: lessons from protein synthesis Cell 136 2009 746 762
30. K.B. Gromadski, and M.V. Rodnina Kinetic determinants of high-fidelity tRNA discrimination on the ribosome Mol. Cell 13 2004 191 200
31. R.A. Marshall, C.E. Aitken, M. Dorywalska, and J.D. Puglisi Translation at the single-molecule level Annu. Rev. Biochem. 77 2008 177 203
32. N. Ban, P. Nissen, J. Hansen, P.B. Moore, and T.A. Steitz The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution Science 289 2000 905 920
33. B.T. Wimberly Structure of the 30S ribosomal subunit Nature 407 2000 327 339
34. F. Schluenzen Structure of functionally activated small ribosomal subunit at 3.3 Å resolution Cell 102 2000 615 623
35. J.H. Cate, M.M. Yusupov, G.Z. Yusupova, T.N. Earnest, and H.F. Noller X-ray crystal structures of 70S ribosome functional complexes Science 285 1999 2095 2104
36. M.M. Yusupov Crystal structure of the ribosome at 5.5 Å resolution Science 292 2001 883 896
37. E.A. Birge, and C.G. Kurland Reversion of a streptomycin-dependent strain of Escherichia coli Mol. Gen. Genet.: MGG 109 1970 356 369
38. B.L. Brownstein, and L.J. Lewandowski A mutation suppressing streptomycin dependence: I. An effect on ribosome function J. Mol. Biol. 25 1967 99 109
39. G. Stoffler, E. Deusser, H.G. Wittmann, and D. Apirion Ribosomal proteins. XIX. Altered S5 ribosomal protein in an Escherichia coli revertant from strptomycin dependence to independence Mol. Gen. Genet.: MGG 111 1971 334 341
40. A.P. Carter Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics Nature 407 2000 340 348
41. L.B. Jenner, N. Demeshkina, G. Yusupova, and M. Yusupov Structural aspects of messenger RNA reading frame maintenance by the ribosome Nat. Struct. Mol. Biol. 17 2010 555 560
42. L.B. Jenner, N. Demeshkina, M. Yusupov, and G. Yusupova X-ray analysis of the prokaryotic and eukaryotic ribosomes J. Dinman, Biophysical Approaches to Translational Control of Gene Expression 2013 Springer-Verlag/Vien Austria 1 26
43. L. Jenner, N. Demeshkina, G. Yusupova, and M. Yusupov Structural rearrangements of the ribosome at the tRNA proofreading step Nat. Struct. Mol. Biol. 17 2010 1072 1078
44. L. Jenner, N. Demeshkina, G. Yusupova, and M. Yusupov Interaction of bacterial ribosome with mRNA and tRNA as studied by X-ray crystallographic analysis Rodnina Wintermeyer Green Structure, Function, and Dynamics 2011 Springer-Verlag/Vien Austria 75 82
45. E.P. Plant Differentiating between near- and non-cognate codons in Saccharomyces cerevisiae PLoS ONE 2 2007 e517
46. N. Demeshkina, L. Jenner, E. Westhof, M. Yusupov, and G. Yusupova A new understanding of the decoding principle on the ribosome Nature 484 2012 256 259
47. J. Parker Errors and alternatives in reading the universal genetic code Microbiol. Rev. 53 1989 273 298
48. D.A. Drummond, and C.O. Wilke The evolutionary consequences of erroneous protein synthesis Nat. Rev. Genet. 10 2009 715 724
49. H.S. Zaher, and R. Green Hyperaccurate and error-prone ribosomes exploit distinct mechanisms during tRNA selection Mol. Cell 39 2010 110 120
50. BPS Database of RNA Base-Pair Structures < http://bps.rutgers.edu/bps > (2008).
51. W. Wang, H.W. Hellinga, and L.S. Beese Structural evidence for the rare tautomer hypothesis of spontaneous mutagenesis Proc. Natl. Acad. Sci. USA 108 2011 17644 17648
52. K. Bebenek, L.C. Pedersen, and T.A. Kunkel Replication infidelity via a mismatch with Watson-Crick geometry Proc. Natl. Acad. Sci. USA 108 2011 1862 1867
53. G. Blaha, R.E. Stanley, and T.A. Steitz Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome Science 325 2009 966 970
54. M. Selmer Structure of the 70S ribosome complexed with mRNA and tRNA Science 313 2006 1935 1942
55. M. Laurberg Structural basis for translation termination on the 70S ribosome Nature 454 2008 852 857
56. M.A. Borovinskaya Structural basis for aminoglycoside inhibition of bacterial ribosome recycling Nat. Struct. Mol. Biol. 14 2007 727 732
57. J. Davies, L. Gorini, and B.D. Davis Misreading of RNA codewords induced by aminoglycoside antibiotics Mol. Pharmacol. 1 1965 93 106
58. R. Karimi, and M. Ehrenberg Dissociation rate of cognate peptidyl-tRNA from the A-site of hyper-accurate and error-prone ribosomes Eur. J. Biochem./FEBS 226 1994 355 360
59. T. Pape, W. Wintermeyer, and M.V. Rodnina Conformational switch in the decoding region of 16S rRNA during aminoacyl-tRNA selection on the ribosome Nat. Struct. Biol. 7 2000 104 107
60. R.M. Voorhees, A. Weixlbaumer, D. Loakes, A.C. Kelley, and V. Ramakrishnan Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome Nat. Struct. Mol. Biol. 16 2009 528 533
61. A. Tsai The impact of aminoglycosides on the dynamics of translation elongation Cell Rep. 3 2013 497 508
62. G.Z. Yusupova, M.M. Yusupov, J.H. Cate, and H.F. Noller The path of messenger RNA through the ribosome Cell 106 2001 233 241
63. T.M. Schmeing The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA Science 326 2009 688 694
64. K.B. Gromadski, T. Daviter, and M.V. Rodnina A uniform response to mismatches in codon-anticodon complexes ensures ribosomal fidelity Mol. Cell 21 2006 369 377
65. S. Yoshizawa, D. Fourmy, and J.D. Puglisi Recognition of the codon-anticodon helix by ribosomal RNA Science 285 1999 1722 1725
66. M. Diaconu Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation Cell 121 2005 991 1004
67. U. Kothe, H.J. Wieden, D. Mohr, and M.V. Rodnina Interaction of helix D of elongation factor Tu with helices 4 and 5 of protein L7/12 on the ribosome J. Mol. Biol. 336 2004 1011 1021
68. P. Geggier Conformational sampling of aminoacyl-tRNA during selection on the bacterial ribosome J. Mol. Biol. 399 2010 576 595
69. T. Pape, W. Wintermeyer, and M. Rodnina Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome EMBO J. 18 1999 3800 3807
70. M. Valle Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy Nat. Struct. Biol. 10 2003 899 906
71. H. Stark Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex Nat. Struct. Biol. 9 2002 849 854
72. X. Agirrezabala Structural insights into cognate versus near-cognate discrimination during decoding EMBO J. 30 2011 1497 1507
73. S.C. Blanchard, R.L. Gonzalez, H.D. Kim, S. Chu, and J.D. Puglisi TRNA selection and kinetic proofreading in translation Nat. Struct. Mol. Biol. 11 2004 1008 1014
74. T.M. Schmeing, R.M. Voorhees, A.C. Kelley, and V. Ramakrishnan How mutations in tRNA distant from the anticodon affect the fidelity of decoding Nat. Struct. Mol. Biol. 18 2011 432 436
75. L. Cochella, and R. Green An active role for tRNA in decoding beyond codon:anticodon pairing Science 308 2005 1178 1180
76. J.D. Watson, and F.H. Crick Genetical implications of the structure of deoxyribonucleic acid Nature 171 1953 964 967
77. J.D. Watson, and F.H. Crick Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid Nature 171 1953 737 738
78. V.H. Harris The effect of tautomeric constant on the specificity of nucleotide incorporation during DNA replication: support for the rare tautomer hypothesis of substitution mutagenesis J. Mol. Biol. 326 2003 1389 1401
79. M.D. Topal, and J.R. Fresco Complementary base pairing and the origin of substitution mutations Nature 263 1976 285 289