The structural basis of transfer RNA mimicry and conformational plasticity by a viral RNA

Nature

Volumn 511, Issue 7509, 2014, Pages 366-369

  Colussi, Timothy M ^a,c   Costantino, David A ^a   Hammond, John A ^a,d   Ruehle, Grant M ^a   Nix, Jay C ^b   Kieft, Jeffrey S ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c NORTHEASTERN UNIVERSITY   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFER RNA; VIRUS RNA;

CRYSTAL STRUCTURE; MIMICRY; MOLECULAR ANALYSIS; PHENOTYPIC PLASTICITY; RESOLUTION; RNA; VIRUS;

AMINOACYLATION; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; MOLECULAR INTERACTION; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; RIBOSOME; RNA CONFORMATION; RNA SEQUENCE; X RAY CRYSTALLOGRAPHY;

RNA VIRUSES; TURNIP YELLOW MOSAIC VIRUS;

3' UNTRANSLATED REGIONS; AMINO ACYL-TRNA SYNTHETASES; AMINOACYLATION; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; RIBOSOMES; RNA FOLDING; RNA, GUIDE; RNA, TRANSFER; RNA, VIRAL; TYMOVIRUS;

EID: 84904513426     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13378     Document Type: Article

References (45)

1. Dethoff, E. A., Chugh, J., Mustoe, A. M. & Al-Hashimi, H. M. Functional complexity and regulation through RNA dynamics. Nature 482, 322-330 (2012).
2. Yot, P., Pinck, M., Haenni, A. L., Duranton, H. M. & Chapeville, F. Valine-specific tRNA-like structure in turnip yellowmosaic virusRNA. Proc. Natl Acad. Sci. USA 67, 1345-1352 (1970).
3. Pinck, M., Yot, P., Chapeville, F.&Duranton, H. M. Enzymatic binding of valine to the 39 end of TYMV-RNA. Nature 226, 954-956 (1970).
4. Litvak, S., Carr, D. S. & Chapeville, F. TYMV RNA as a substrate of the tRNA nucleotidyltransferase. FEBS Lett. 11, 316-319 (1970).
5. Hammond, J. A., Rambo, R. P. & Kieft, J. S. Multi-domain packing in the aminoacylatable 39 end of a plant viral RNA. J. Mol. Biol. 399, 450-463 (2010).
6. Dreher, T. W. Role of tRNA-like structures in controlling plant virus replication. Virus Res. 139, 217-229 (2009).
7. Giegé, R., Frugier, M. & Rudinger, J. tRNA mimics. Curr. Opin. Struct. Biol. 8, 286-293 (1998).
8. Cliffe, A. R.,Nash, A. A.&Dutia, B. M. Selective uptake ofsmallRNAmolecules in the virion of murine gammaherpesvirus 68. J. Virol. 83, 2321-2326 (2009).
9. Dreher, T. W. Viral tRNAs and tRNA-like structures. Wiley. Interdiscip. Rev. RNA 1, 402-414 (2010).
10. Wilusz, J. E., Freier, S. M. & Spector, D. L. 39 End processing of a long nuclearretained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell 135, 919-932 (2008).
11. Hammond, J. A., Rambo, R. P., Filbin, M. E. & Kieft, J. S. Comparison and functional implications of the 3D architectures of viral tRNA-like structures. RNA 15, 294-307 (2009).
12. Rietveld, K., Linschooten, K., Pleij, C. W. & Bosch, L. The three-dimensional folding of the tRNA-like structure of tobacco mosaic virus RNA. A new building principle applied twice. EMBO J. 3, 2613-2619 (1984).
13. Rietveld, K., Pleij, C. W. & Bosch, L. Three-dimensional models of the tRNA-like 39 termini of some plant viral RNAs. EMBO J. 2, 1079-1085 (1983).
14. Rietveld, K., Van Poelgeest, R., Pleij, C. W., Van Boom, J. H.& Bosch, L. The tRNA-like structure at the 39 terminus of turnip yellow mosaic virus RNA. Differences and similarities with canonical tRNA. Nucleic Acids Res. 10, 1929-1946 (1982).
15. Florentz, C. et al. The tRNA-like structure of turnip yellow mosaic virus RNA: structural organization of the last 159 nucleotides fromthe 39OHterminus.EMBO J. 1, 269-276 (1982).
16. Giegé, R., Florentz, C. & Dreher, T. W. The TYMV tRNA-like structure. Biochimie 75, 569-582 (1993).
17. Matsuda, D. & Dreher, T. W. The tRNA-like structure of turnip yellow mosaic virus RNA is a 39-translational enhancer. Virology 321, 36-46 (2004).
18. Singh, R. N. & Dreher, T. W. Turnip yellow mosaic virus RNA-dependent RNA polymerase: initiation of minus strand synthesis in vitro. Virology 233, 430-439 (1997).
19. Skuzeski, J. M., Bozarth, C. S. & Dreher, T. W. The turnip yellow mosaic virus tRNAlike structure cannot be replaced by generic tRNA-like elements or by heterologous 39 untranslated regions known to enhance mRNA expression and stability. J. Virol. 70, 2107-2115 (1996).
20. Matsuda, D., Yoshinari, S. & Dreher, T. W. eEF1A binding to aminoacylated viral RNA represses minus strand synthesis by TYMV RNA-dependent RNA polymerase. Virology 321, 47-56 (2004).
21. Shi, H. & Moore, P. B. The crystal structure of yeast phenylalanine tRNA at 1.93A? resolution: a classic structure revisited. RNA 6, 1091-1105 (2000).
22. Dumas, P. et al. 3-D graphics modelling of the tRNA-like 39-end of turnip yellow mosaic virus RNA: structural and functional implications. J. Biomol. Struct. Dyn. 4, 707-728 (1987).
23. Singh, R. N. & Dreher, T. W. Specific site selection in RNA resulting from a combination of nonspecific secondary structure and-CCR-boxes: initiation of minus strand synthesis by turnip yellow mosaic virus RNA-dependent RNA polymerase. RNA 4, 1083-1095 (1998).
24. Deiman, B. A., Koenen, A. K., Verlaan, P. W. & Pleij, C. W. Minimal template requirements for initiation of minus-strand synthesis in vitro by the RNAdependent RNA polymerase of turnip yellow mosaic virus. J. Virol. 72, 3965-3972 (1998).
25. Fukai, S. et al. Structural basis for double-sieve discrimination of L-valine from L-isoleucineand L-threonine by the complex of tRNAVal and valyl-tRNAsynthetase. Cell 103, 793-803 (2000).
26. Dreher, T. W., Tsai, C. H., Florentz, C. & Giege, R. Specific valylation of turnip yellow mosaic virus RNA by wheat germ valyl-tRNA synthetase determined by three anticodon loop nucleotides. Biochemistry 31, 9183-9189 (1992).
27. Dreher, T. W. & Goodwin, J. B. Transfer RNA mimicry among tymoviral genomic RNAs ranges from highly efficient to vestigial. Nucleic Acids Res. 26, 4356-4364 (1998).
28. Barends, S., Bink, H. H., van den Worm, S. H., Pleij, C. W. & Kraal, B. Entrapping ribosomes for viral translation: tRNA mimicry as a molecular Trojan horse. Cell 112, 123-129 (2003).
29. Berthelot, F., Bogdanovsky, D., Schapira, G. & Gros, F. Interchangeability of factors and tRNA's in bacterial and eukaryotic translation initiation systems. Mol. Cell. Biochem. 1, 63-72 (1973).
30. Leontis, N. B. & Westhof, E. Geometric nomenclature and classification of RNA base pairs. RNA 7, 499-512 (2001).
31. Keel, A. Y., Rambo, R. P., Batey, R. T. & Kieft, J. S. A general strategy to solve the phase problem in RNA crystallography. Structure 15, 761-772 (2007).
32. Wientges, J., Putz, J., Giege, R., Florentz, C. & Schwienhorst, A. Selection of viral RNA-derived tRNA-like structures with improved valylation activities. Biochemistry 39, 6207-6218 (2000).
33. Kabsch, W. Xds. Acta Crystallogr. D 66, 125-132 (2010).
34. Kabsch, W. Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D 66, 133-144 (2010).
35. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
36. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
37. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
38. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21 (2010).
39. Davis, I. W., Murray, L. W., Richardson, J. S. & Richardson, D. C. MolProbity: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32, W615-W619 (2004).
40. Zhu, J. et al. Crystal structures of complexes containing domains from two viral internal ribosome entry site (IRES) RNAs bound to the 70S ribosome. Proc. Natl Acad. Sci. USA 108, 1839-1844 (2011).
41. Costantino, D. & Kieft, J. S. A preformed compact ribosome-binding domain in the cricket paralysis-like virus IRES RNAs. RNA 11, 332-343 (2005).
42. Kieft, J. S., Zhou, K., Jubin, R. & Doudna, J. A. Mechanismof ribosome recruitment by hepatitis C IRES RNA. RNA 7, 194-206 (2001).
43. Kolk, M. H. et al. NMR structure of a classical pseudoknot: interplay of single-and double-stranded RNA. Science 280, 434-438 (1998).
44. Nissen, P. et al. Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270, 1464-1472 (1995).
45. Karplus, P. A. & Diederichs, K. Linking crystallographic model and data quality. Science 336, 1030-1033 (2012).