Virus-encoded aminoacyl-tRNA synthetases: Structural and functional characterization of mimivirus TyrRS and MetRS

Journal of Virology

Volumn 81, Issue 22, 2007, Pages 12406-12417

  Abergel, Chantal ^a   Rudinger Thirion, Joëlle ^b   Giegé, Richard ^b   Claverie, Jean Michel ^a  

^a CNRS Aix Marseille University   (France)

^b INST DE BIOL MOLEC ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; VIRUS DNA;

AMINO ACID ANALYSIS; ARTICLE; DNA VIRUS; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; EUKARYOTE; GENE TRANSFER; GENETIC CODE; MIMIVIRIDAE; MIMIVIRUS METRS; MIMIVIRUS TYRRS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA TRANSLATION; STRUCTURE ACTIVITY RELATION; TRANSLATION INITIATION; TRANSLATION REGULATION;

ACANTHAMOEBA; ANIMALS; ANTICODON; CRYSTALLOGRAPHY, X-RAY; DNA VIRUSES; METHIONINE-TRNA LIGASE; PHYLOGENY; PROTEIN STRUCTURE, SECONDARY; RNA, TRANSFER, MET; RNA, TRANSFER, TYR; TYROSINE-TRNA LIGASE; VIRAL PROTEINS;

ARCHAEA; DNA VIRUSES; EUKARYOTA; MIMIVIRUS;

EID: 35949003882     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01107-07     Document Type: Article

References (62)

1. Abergel, C., B. Coutard, D. Byrne, S. Chenivesse, J. B. Claude, C. Deregnaucourt, T. Fricaux, C. Gianesini-Boutreux, S. Jeudy, R. Lebrun, C. Maza, C. Notredame, O. Poirot, K. Suhre, M. Varagnol, and J.-M. Claverie. 2003. Structural genomics of highly conserved microbial genes of unknown function in search of new antibacterial targets. J. Struct. Funct. Genomics 4:141-157.
2. Abergel, C., S. Chenivesse, D. Byrne, K. Suhre, V. Arondel, and J.-M. Claverie. 2005. Mimivirus TyrRS: preliminary structural and functional characterization of the first amino-acyl tRNA synthetase found in a virus. Acta Crystallogr. F 61:212-215.
3. Adl, S. M., A. G. Simpson, M. A. Farmer, R. A. Andersen, O. R. Anderson, J. R. Barta, S. S. Bowser, G. Brugerolle, R. A. Fensome, S. Fredericq, T. Y. James, S. Karpov, P. Kugrens, J. Krug, C. E. Lane, L. A. Lewis, J. Lodge, D. H. Lynn, D. G. Mann, R. M. McCourt, L. Mendoza, O. Moestrup, S. E. Mozley-Standridge, T. A. Nerad, C. A. Shearer, A. V. Smirnov, F. W. Spiegel, and M. F. Taylor. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52:399-451.
4. Aphasizhev, R., A. Théobald-Dietrich, D. Kostyuk, S. N. Kochetkov, L. Kisselev, R. Giegé, and F. Fasiolo. 1997. Structure and aminoacylation capacities of tRNA transcripts containing deoxyribonucleotides. RNA 3:893-904.
5. Arnez, J. G., and D. Moras. 1997. Structural and functional considerations of the aminoacylation reaction. Trends Biochem. Sci. 22:211-216.
6. Bedouelle, H., and G. Winter. 1986. A model of synthetase/transfer RNA interaction as deduced by protein engineering. Nature 320:371-373.
7. Bedouelle, H. 1990. Recognition of tRNAtyr by tyrosyl-tRNA synthetase. Biochimie 72:589-598.
8. Bedouelle, H. 2005. Tyrosyl-tRNA synthetases, p. 111-124. In M. Ibba, C. Francklyn, and S. Cusack (ed.), Aminoacyl-tRNA synthetases. Landes Biosciences, Georgetown, TX.
9. Tyr/TyrRS aminoacylation systems. Biochimie 87:873-883.
10. Bricogne, G., C. Vonrhein, C. Flensburg, M. Schiltz, and W. Paciorek. 2003. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D 59:2023-2030.
11. Brunger, A. T., P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J. S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallograph. D 54:905-921.
12. Campanacci, V., D. Y. Dubois, H. D. Becker, D. Kern, S. Spinelli, C. Valencia, F. Pagot, A. Salomoni, S. Grisel, R. Vincentelli, C. Bignon, J. Lapointe, R. Giegé, and C. Cambillau. 2004. The Escherichia coli YadB gene product reveals a novel aminoacyl-tRNA synthetase like activity. J. Mol. Biol. 337:273-283.
13. Carter, C. W., Jr. 1993. Cognition, mechanism, and evolutionary relationships in aminoacyl-tRNA synthetases. Annu. Rev. Biochem. 62:715-748.
14. Cherniack, A. D., G. Garriga, J. D. Kittle, Jr., R. A. Akins, and A. M. Lambowitz. 1990. Function of Neurospora mitochondrial tyrosyl-tRNA synthetase in RNA splicing requires an idiosyncratic domain not found in other synthetase. Cell 62:745-755.
15. Claverie, J.-M., H. Ogata, S. Audic, C. Abergel, K. Suhre, and P.-E. Fournier. 2006. Mimivirus and the emerging concept of giant virus. Virus Res. 117:133-144.
16. Collaborative Computational Project Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50:760-763.
17. Cusack, S., C. Berthet-Colominas, M. Härtlein, N. Nassar, and R. Leberman. 1990. A second class of synthetase structure revealed by X-ray analysis of Escherichia coli seryl-tRNA synthetase at 2.5 Å. Nature 347:249-255.
18. Delarue, M., and D. Moras. 1993. The aminoacyl-tRNA synthetases family: modules at work. Bioessays 15:675-687.
19. Despons, L., B. Senger, F. Fasiolo, and P. Walter. 1992. The anticodon triplet is not sufficient to confer methionine acceptance to a transfer RNA. J. Mol. Biol. 225:897-907.
20. Dessen, P., G. Zaccaï, and S. Blanquet. 1982. Neutron scattering studies of Escherichia coli tyrosyl-tRNA synthetase and of its interaction with tRNA-tyr. J. Mol. Biol. 159:651-664.
21. Dirheimer, G., and J.-P. Ebel. 1967. Fractionation of Brewer's yeast t-RNA by countercurrent distribution. Bull. Soc. Chim. Biol. (Paris) 49:1679-1687.
22. Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
23. Eriani, G., M. Delarue, O. Poch, J. Gangloff, and D. Moras. 1990. Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature 347:203-206.
24. Evans, P. R. 1993. Data reduction, p. 114-122. In L. Sawyer, N. Isaacs, and S. Bailey (ed)., Proceedings of CCP4 Study Weekend, on data collection and processing. Daresbury Laboratory, Warrington, United Kingdom.
25. Fechter, P., J. Rudinger, R. Giegé, and A. Theobald- Dietrich. 1998. Ribozyme processed tRNA transcripts with unfriendly internal promoter for T7 RNA polymerase: production and activity. FEBS Lett. 436:99-103.
26. Fechter, P., J. Rudinger-Thirion, A. Theobald-Dietrich, and R. Giegé. 2000. Specific tyrosylation of the bulky tRNA-like structure of Brome mosaic virus RNA relies solely on identity nucleotides present in its amino acid accepting domain. Biochemistry 39:1725-1733.
27. Fersht. A. R., and R. Jakes. 1975. Tyrosyl-tRNA synthetase from Escherichia coli. Stoichiometry of ligand binding and half-of-the-sites reactivity in aminoacylation. Biochemistry 14:3344-3350.
28. Francklyn, C., J. J. Perona, J. Puetz, and Y. M. Hou. 2002. Aminoacyl-tRNA synthetases: versatile players in the changing theater of translation. RNA 8:1363-1372.
29. Frugier, M., M. Ryckelynck, and R. Giegé. 2005. tRNA-balanced expression of a eukaryal aminoacyl-tRNA synthetase by an mRNA-mediated pathway. EMBO Rep. 6:860-865.
30. Giegé, R., M. Sissler, and C. Florentz. 1998. Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res. 26:5017-5035.
31. Gouet, P., E. Courcelle, D. I. Stuart, and F. Metoz. 1999. ESPript: multiple sequence alignments in PostScript. Bioinformatics 15:305-308.
32. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phytogenies by maximum likelihood. Syst. Biol. 52:696-704.
33. Hartley, J. L., G. F. Temple, and M. A. Brasch. 2000. DNA cloning using in vitro site-specific recombination. Genome Res. 10:1788-1795.
34. Hendrickson, W. A., J. R. Horton, and D. M. LeMaster. 1990. Selenome-thionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 9:1665-1672.
35. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD-visual molecular dynamics. J. Mol. Graphics 14:33-38.
36. Kleeman, T. A., D. Wei, K. L. Simpson, and E. A. First. 1997. Human tyrosyl-tRNA synthetase shares amino acid sequence homology with a putative cytokine. J. Biol. Chem. 272:14420-14425.
37. Kobayashi, T., O. Nureki, R. Ishitani, A. Yaremchuk, M. Tukalo, S. Cusack, K. Sakamoto, and S. Yokoyama. 2003. Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion. Nat. Struct. Biol. 10:425-432.
38. Kuratani, M., H. Sakai, M. Takahashi, T. Yanagisawa, T. Kobayashi, K. Murayama, L. Chen, Z. J. Liu, B. C. Wang, C. Kuroishi, S. Kuramitsu, T. Terada, Y. Bessho, M. Shirouzu, S. Sekine, and S. Yokoyama. 2006. Crystal structures of tyrosyl-tRNA synthetases from Archaea. J. Mol. Biol. 355:395-408.
39. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
40. Leslie, A. 1993. Auto indexing of rotation diffraction images and parameter refinement, p. 44-51. In L. Sawyer, N. Issacs, and S. Bailey (ed.), Proceedings of CCP4 Study Weekend, on data collection and processing. Darcsbury Laboratory, Warrington, United Kingdom.
41. Myers, C. A., B. Kuhla, S. Cusack, and A. M. Lambowitz. 2002. tRNA-like recognition of group I introns by a tyrosyl-tRNA synthetase. Proc. Natl. Acad. Sci. USA 99:2630-2635.
42. Nair, S., L. Ribas de Pouplana, F. Houman, A. Avruch, X. Shen, and P. Schimmel. 1997. Species-specific tRNA recognition in relation to tRNA synthetase contact residues. J. Mol. Biol. 269:1-9.
43. Navaza, J. 2001. Implementation of molecular replacement in AMoRe. Acta Crystallogr. D 57:1367-1372.
44. Nicholls, A., K. A. Sharp, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct. Funct. Genet. 11:281-296.
45. Notredame, C., D. Higgins, and J. Heringa. 2000. T-Coffee: a novel method for multiple sequence alignments. J. Mol. Biol. 302:205-217.
46. Ogata, H., C. Abergel, D. Raoult, and J.-M. Claverie. 2005. Response to comment on the 1.2-megabase genome sequence of mimivirus. Science 308:1114.
47. Perret, V., C. Florentz, J. D. Puglisi, and R. Giegé. 1992. Effect of conformational features on the aminoacylation of tRNAs and consequences on the permutation of tRNA specificities. J. Mol. Biol. 226:323-333.
48. Poirot, O., K. Suhre, C. Abergel, E. O'Toole, and C. Notredame. 2004. 3DCoffee@igs: a web server for combining sequences and structures into a multiple sequence alignment. Nucleic Acids Res. 32:W37-W40.
49. Raoult, D., S. Audic, C. Robert, C. Abergel, P. Renesto, H. Ogata, B. La Scola, M. Suzan, and J.-M. Claverie. 2004. The 1.2-Mb genome sequence of Mimivirus. Science 306:1344-1350.
50. Roussel, A., and C. Cambillau. 1991. TURBO-FRODO in silicon graphics geometry partners directory. Silicon Graphics, Mountain View, CA.
51. Sali, A., and T. L. Blundell. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
52. Schulman, L. H., and H. Pelka. 1988. Anticodon switching changes the identity of methionine and valine transfer RNAs. Science 242:765-768.
53. Senger, B., and F. Fasiolo. 1996. Yeast tRNAMet recognition by methionyl-tRNA synthetase requires determinants from the primary, secondary and tertiary structure: a review. Biochimie 78:597-604.
54. Sohm, B., M. Frugier, H. Brulé, K. Olszak, A. Przykorska, and C. Florentz. 2003. Towards understanding human mitochondrial leucine aminoacylation identity. J. Mol. Biol. 328:995-1010.
55. Sprinzl, M., and K. S. Vassilenko. 2005. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 33:D139-D140.
56. Suzan-Monti, M., B. La Scola, and D. Raoult. 2006. Genomic and evolutionary aspects of Mimivirus. Virus Res. 117:145-155.
57. Van Etten, J. L., M. V. Graves, D. G. Müller, W. Boland, and N. Delaroque. 2002. Phycodnaviridae - large DNA algal viruses. Arch. Virol. 147:1479-1516.
58. Wakasugi, K., C. L. Quinn, N. Tao, and P. Schimmel. 1998. Genetic code in evolution: switching species-specific aminoacylation with a peptide transplant. EMBO J. 17:297-305.
59. Wakasugi, K., and P. Schimmel. 1999. Two distinct cytokines released from a human aminoacyl-tRNA synthetase. Science 284:147-150.
60. Yamada, T., H. Onimatsu, and J. L. Van Etten. 2006. Chlorella viruses. Adv. Virus Res. 66:293-336.
61. Yang, X. L., F. J. Otero, R. J. Skene, D. E. McRee, P. Schimmel, and L. Ribas de Pouplana. 2003. Crystal structures that suggest late development of genetic code components for differentiating aromatic side chains. Proc. Natl. Acad. Sci. USA 100:15376-15380.
62. Yaremchuk, A., I. Kriklivyi, M. Tukalo, and S. Cusack. 2002. Class 1 tyrosyltRNA synthetase has a class II mode of cognate tRNA recognition. EMBO J. 21:3829-3840.