Novel base-pairing interactions at the tRNA wobble position crucial for accurate reading of the genetic code

Nature Communications

Volumn 7, Issue , 2016, Pages

  Rozov, Alexey ^a   Demeshkina, Natalia ^a   Khusainov, Iskander ^a,b   Westhof, Eric ^a   Yusupov, Marat ^a   Yusupova, Gulnara ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b KAZAN FEDERAL UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLAMINOMETHYL 2 THIOURIDINE; GUANOSINE; ISOLEUCINE; PYRIMIDINE; TRANSFER RNA; UNCLASSIFIED DRUG; URIDINE DERIVATIVE; 5-METHYLAMINOMETHYL-2-THIOURIDINE; CODON; MESSENGER RNA; THIOURIDINE;

BACTERIUM; GENE EXPRESSION; GENETIC ANALYSIS; MUTATION; PROTEIN; RNA;

ARTICLE; BASE PAIRING; CODON; ESCHERICHIA COLI; GENETIC CODE; NONHUMAN; PROTEIN STRUCTURE; STOP CODON; X RAY ANALYSIS; ANALOGS AND DERIVATIVES; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN SYNTHESIS; RIBOSOME;

ESCHERICHIA COLI;

BASE PAIRING; BASE SEQUENCE; CODON; ESCHERICHIA COLI; GENETIC CODE; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, TRANSFER; THIOURIDINE;

EID: 84955515428     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10457     Document Type: Article

References (56)

1. Machnicka, M. A. et al. MODOMICS: A database of RNA modification pathways-2013 update. Nucleic Acids Res. 41, D262-D267 (2013).
2. El Yacoubi, B., Bailly, M. & de Crecy-Lagard, V. Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu. Rev. Genet. 46, 69-95 (2012).
3. Nishimura, S. & Watanabe, K. The discovery of modified nucleosides from the early days to the present: A personal perspective. J. Biosci. 31, 465-475 (2006).
4. Agris, P. F., Vendeix, F. A. & Graham, W. D. TRNA's wobble decoding of the genome: 40 years of modification. J. Mol. Biol. 366, 1-13 (2007).
5. Cantara, W. A. et al. The RNA modification database, RNAMDB: 2011 update. Nucleic Acids Res. 39, D195-D201 (2011).
6. Durant, P. C., Bajji, A. C., Sundaram, M., Kumar, R. K. & Davis, D. R. Structural effects of hypermodified nucleosides in the Escherichia coli and human tRNALys anticodon loop: The effect of nucleosides s2U, mcm5U, mcm5s2U, mnm5s2U, t6A, and ms2t6A. Biochemistry 44, 8078-8089 (2005).
7. Stuart, J. W., Koshlap, K. M., Guenther, R. & Agris, P. F. Naturally-occurring modification restricts the anticodon domain conformational space of tRNA(Phe). J. Mol. Biol. 334, 901-918 (2003).
8. Crick, F. H. Codon-anticodon pairing: The wobble hypothesis. J. Mol. Biol. 19, 548-555 (1966).
9. Yarian, C. et al. Accurate translation of the genetic code depends on tRNA modified nucleosides. J. Biol. Chem. 277, 16391-16395 (2002).
10. Bjork, G. R. et al. Transfer RNA modification. Annu. Rev. Biochem. 56, 263-287 (1987).
11. Agris, P. F. Wobble position modified nucleosides evolved to select transfer RNA codon recognition: A modified-wobble hypothesis. Biochimie 73, 1345-1349 (1991).
12. Beuning, P. J. & Musier-Forsyth, K. Transfer RNA recognition by aminoacyl-tRNA synthetases. Biopolymers 52, 1-28 (1999).
13. Grosjean, H. & Bjork, G. R. Enzymatic conversion of cytidine to lysidine in anticodon of bacterial isoleucyl-tRNA-an alternative way of RNA editing. Trends Biochem. Sci. 29, 165-168 (2004).
14. Bjork, G. R. et al. Transfer RNA modification: influence on translational frameshifting and metabolism. FEBS Lett. 452, 47-51 (1999).
15. Urbonavicius, J., Qian, Q., Durand, J. M., Hagervall, T. G. & Bjork, G. R. Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J. 20, 4863-4873 (2001).
16. Thiaville, P. C. & de Crecy-Lagard, V. The emerging role of complex modifications of tRNA in signaling pathways. Microb. Cell 2, 1-4 (2015).
17. Kellogg, D. A., Doctor, B. P., Loebel, J. E. & Nirenberg, M. W. RNA codons and protein synthesis. IX. Synonym codon recognition by multiple species of valine-, alanine-, and methionine-sRNA. Proc. Natl Acad. Sci. USA 55, 912-919 (1966).
18. Crick, F. H. The origin of the genetic code. J. Mol. Biol. 38, 367-379 (1968).
19. Raba, M. et al. Nucleotide sequence of three isoaccepting lysine tRNAs from rabbit liver and SV40-transformed mouse fibroblasts. Eur. J. Biochem. 97, 305-318 (1979).
20. Sprinzl, M. & Vassilenko, K. S. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 33, D139-D140 (2005).
21. Armengod, M. E. et al. Enzymology of tRNA modification in the bacterial MnmEG pathway. Biochimie 94, 1510-1520 (2012).
22. Kumar, R. K. & Davis, D. R. Synthesis and studies on the effect of 2-thiouridine and 4-thiouridine on sugar conformation and RNA duplex stability. Nucleic Acids Res. 25, 1272-1280 (1997).
23. Ogle, J. M. et al. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292, 897-902 (2001).
24. Murphy, F. V. T. & Ramakrishnan, V. Structure of a purine-purine wobble base pair in the decoding center of the ribosome. Nat. Struct. Mol. Biol. 11, 1251-1252 (2004).
25. Murphy, F. V. T., Ramakrishnan, V., Malkiewicz, A. & Agris, P. F. The role of modifications in codon discrimination by tRNA(Lys)UUU. Nat. Struct. Mol. Biol. 11, 1186-1191 (2004).
26. Vendeix, F. A. et al. Human tRNA(Lys3)(UUU) is pre-structured by natural modifications for cognate and wobble codon binding through keto-enol tautomerism. J. Mol. Biol. 416, 467-485 (2012).
27. Weixlbaumer, A. et al. Mechanism for expanding the decoding capacity of transfer RNAs by modification of uridines. Nat. Struct. Mol. Biol. 14, 498-502 (2007).
28. Jenner, L. B., Demeshkina, N., Yusupova, G. & Yusupov, M. Structural aspects of messenger RNA reading frame maintenance by the ribosome. Nat. Struct. Mol. Biol. 17, 555-560 (2010).
29. Demeshkina, N., Jenner, L., Westhof, E., Yusupov, M. & Yusupova, G. A new understanding of the decoding principle on the ribosome. Nature 484, 256-259 (2012).
30. Rozov, A., Demeshkina, N., Westhof, E., Yusupov, M. & Yusupova, G. Structural insights into the translational infidelity mechanism. Nat. Commun. 6, 7251 (2015).
31. Selmer, M. et al. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313, 1935-1942 (2006).
32. Fernandez, I. S. et al. Unusual base pairing during the decoding of a stop codon by the ribosome. Nature 500, 107-110 (2013).
33. Schmeing, T. M., Voorhees, R. M., Kelley, A. C. & Ramakrishnan, V. How mutations in tRNA distant from the anticodon affect the fidelity of decoding. Nat. Struct. Mol. Biol. 18, 432-436 (2011).
34. Holley, R. W. et al. Structure of a ribonucleic acid. Science 147, 1462-1465 (1965).
35. Ogle, J. M., Murphy, F. V., Tarry, M. J. & Ramakrishnan, V. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111, 721-732 (2002).
36. Yokoyama, S. et al. Molecular mechanism of codon recognition by tRNA species with modified uridine in the first position of the anticodon. Proc. Natl Acad. Sci. USA 82, 4905-4909 (1985).
37. Mazumdar, S. K. & Saenger, W. Molecular structure of poly-2-thiouridylic acid, a double helix with non-equivalent polynucleotide chains. J. Mol. Biol. 85, 213-219 (1974).
38. Demeshkina, N., Jenner, L., Yusupova, G. & Yusupov, M. Interactions of the ribosome with mRNA and tRNA. Curr. Opin. Struct. Biol. 20, 325-332 (2010).
39. Nakamura, Y. Codon Usage Database http://www. kazusa. or. jp/codon/ (2007).
40. Frédéric Dardel, F. K. Bioinformatics: Genomics and Post-Genomics (John Wiley & Sons, Ltd., 2006).
41. Takai, K. & Yokoyama, S. Roles of 5-substituents of tRNA wobble uridines in the recognition of purine-ending codons. Nucleic Acids Res. 31, 6383-6391 (2003).
42. Egli, M. & Sarkhel, S. Lone pair-aromatic interactions: To stabilize or not to stabilize. Acc. Chem. Res. 40, 197-205 (2007).
43. Wohlgemuth, I., Pohl, C., Mittelstaet, J., Konevega, A. L. & Rodnina, M. V. Evolutionary optimization of speed and accuracy of decoding on the ribosome. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 2979-2986 (2011).
44. Kramer, E. B. & Farabaugh, P. J. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 13, 87-96 (2007).
45. Johansson, M., Zhang, J. & Ehrenberg, M. Genetic code translation displays a linear trade-off between efficiency and accuracy of tRNA selection. Proc. Natl Acad. Sci. USA 109, 131-136 (2012).
46. Manickam, N., Nag, N., Abbasi, A., Patel, K. & Farabaugh, P. J. Studies of translational misreading in vivo show that the ribosome very efficiently discriminates against most potential errors. RNA 20, 9-15 (2014).
47. Moazed, D. & Noller, H. F. Binding of tRNA to the ribosomal A and P sites protects two distinct sets of nucleotides in 16S rRNA. J. Mol. Biol. 211, 135-145 (1990).
48. Demeshkina, N., Jenner, L., Westhof, E., Yusupov, M. & Yusupova, G. New structural insights into the decoding mechanism: Translation infidelity via a G. U pair with Watson-Crick geometry. FEBS Lett. 587, 1848-1857 (2013).
49. Westhof, E., Yusupov, M. & Yusupova, G. Recognition of Watson-Crick base pairs: constraints and limits due to geometric selection and tautomerism. F1000Prime Rep. 6, 19 (2014).
50. Grosjean, H., de Crecy-Lagard, V. & Marck, C. Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes. FEBS Lett. 584, 252-264 (2010).
51. Jenner, L., Demeshkina, N., Yusupova, G. & Yusupov, M. Structural rearrangements of the ribosome at the tRNA proofreading step. Nat. Struct. Mol. Biol. 17, 1072-1078 (2010).
52. Mueller, M., Wang, M. & Schulze-Briese, C. Optimal fine phi-slicing for single-photon-counting pixel detectors. Acta Crystallogr. D Biol. Crystallogr. 68, 42-56 (2012).
53. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
54. Adams, P. D. et al. PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
55. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
56. Karplus, P. A. & Diederichs, K. Linking crystallographic model and data quality. Science 336, 1030-1033 (2012).