Interdomain communication modulates the tRNA-dependent pre-transfer editing of leucyl-tRNA synthetase

Biochemical Journal

Volumn 449, Issue 1, 2013, Pages 123-131

  Tan, Min ^a   Zhu, Bin ^a,b   Liu, Ru Juan ^a   Chen, Xin ^a,c   Zhou, Xiao Long ^a   Wang, En Duo ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b HARVARD MEDICAL SCHOOL   (United States)

^c XIAMEN UNIVERSITY   (China)

Author keywords

Domain communication; Leucyl tRNA synthetase (LeuRS); Pre transfer editing; Quality control; tRNA

Indexed keywords

AMINO ACID; ESCHERICHIA COLI LEUCYL TRANSFER RNA SYNTHETASE; LEUCINE TRANSFER RNA LIGASE; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN CONFORMATION; QUALITY CONTROL; RNA EDITING; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LEUCINE-TRNA LIGASE; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA EDITING; RNA, TRANSFER, LEU;

ESCHERICHIA COLI;

EID: 84870867839     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121258     Document Type: Article

References (42)

1. Schimmel, P. (1987) Aminoacyl tRNA synthetases: general scheme of structure-function relationships in the polypeptides and recognition of transfer RNAs. Annu. Rev. Biochem. 56, 125-158
2. Woese, C. R., Olsen, G. J., Ibba, M. and Soll, D. (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol. Mol. Biol. Rev. 64, 202-236 (Pubitemid 30143846)
3. Ibba, M. and Söll, D. (2000) Aminoacyl-tRNA synthesis. Annu. Rev. Biochem. 69, 617-650
4. Eriani, G., Delarue, M., Poch, O., Gangloff, J. and Moras, D. (1990) Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature 347, 203-206
5. Cusack, S., Härtlein, M. and Leberman, R. (1991) Sequence, structural and evolutionary relationships between class 2 aminoacyl-tRNA synthetases. Nucleic Acids Res. 19, 3489-3498 (Pubitemid 21912707)
6. Schimmel, P. and Ribas de Pouplana, L. (1995) Transfer RNA: from minihelix to genetic code. Cell 81, 983-986
7. Schimmel, P. and Ribas de Pouplana, L. (2001) Formation of two classes of tRNA synthetases in relation to editing functions and genetic code. Cold Spring Harb. Symp. Quant. Biol. 66, 161-166 (Pubitemid 36097923)
8. Ling, J., Reynolds, N. and Ibba, M. (2009) Aminoacyl-tRNA synthesis and translational quality control. Annu. Rev. Microbiol. 63, 61-78
9. Jakubowski, H. and Goldman, E. (1992) Editing of errors in selection of amino acids for protein synthesis. Microbiol. Rev. 56, 412-429
10. Chen, J. F., Guo, N. N., Li, T., Wang, E. D. and Wang, Y. L. (2000) CP1 domain in Escherichia coli leucyl-tRNA synthetase is crucial for its editing function. Biochemistry 39, 6726-6731 (Pubitemid 30354005)
11. Zhao, M. W., Zhu, B., Hao, R., Xu, M. G., Eriani, G. and Wang, E. D. (2005) Leucyl-tRNA synthetase from the ancestral bacterium Aquifex aeolicus contains relics of synthetase evolution. EMBO J. 24, 1430-1439 (Pubitemid 40593063)
12. Lin, L., Hale, S. P. and Schimmel, P. (1996) Aminoacylation error correction. Nature 384, 33-34
13. ile and mupirocin. Science 285, 1074-1077
14. Fukai, S., Nureki, O., Sekine, S., Shimada, A., Tao, J., Vassylyev, D. G. and Yokoyama, S. (2000) Structural basis for double-sieve discrimination of L-valine from L-isoleucine and L-threonine by the complex of tRNA(Val) and valyl-tRNA synthetase. Cell 103, 793-803
15. Wong, F. C., Beuning, P. J., Silvers, C. and Musier-Forsyth, K. (2003) An isolated class II aminoacyl-tRNA synthetase insertion domain is functional in amino acid editing. J. Biol. Chem. 278, 52857-52864 (Pubitemid 38035885)
16. Pro editing by Haemophilus influenzae YbaK via a novel synthetase.YbaK.tRNA ternary complex. J. Biol. Chem. 280, 34465-34472
17. Ahel, I., Korencic, D., Ibba, M. and Söll, D. (2003) Trans-editing of mischarged tRNAs. Proc. Natl. Acad. Sci. U.S.A. 100, 15422-15427 (Pubitemid 38021005)
18. Korencic, D., Ahel, I., Schelert, J., Sacher, M., Ruan, B., Stathopoulos, C., Blum, P., Ibba, M. and Söll, D. (2004) A freestanding proofreading domain is required for protein synthesis quality control in Archaea. Proc. Natl. Acad. Sci. U.S.A. 101, 10260-10265 (Pubitemid 38924913)
19. Sokabe, M., Okada, A., Yao, M., Nakashima, T. and Tanaka, I. (2005) Molecular basis of alanine discrimination in editing site. Proc. Natl. Acad. Sci. U.S.A. 102, 11669-11674 (Pubitemid 41170784)
20. Bacher, J. M., de Crécy-Lagard, V. and Schimmel, P. R. (2005) Inhibited cell growth and protein functional changes from an editing-defective tRNA synthetase. Proc. Natl. Acad. Sci. U.S.A. 102, 1697-1701 (Pubitemid 40209230)
21. Chong, Y. E., Yang, X. L. and Schimmel, P. (2008) Natural homolog of tRNA synthetase editing domain rescues conditional lethality caused by mistranslation. J. Biol. Chem. 283, 30073-30078
22. Lee, J. W., Beebe, K., Nangle, L. A., Jang, J., Longo-Guess, C. M., Cook, S. A., Davisson, M. T., Sundberg, J. P., Schimmel, P. and Ackerman, S. L. (2006) Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443, 50-55 (Pubitemid 44344044)
23. Nangle, L. A., Motta, C. M. and Schimmel, P. (2006) Global effects of mistranslation from an editing defect in mammalian cells. Chem. Biol. 13, 1091-1100 (Pubitemid 44557071)
24. Alexander, R. W. and Schimmel, P. (2001) Domain-domain communication in aminoacyl-tRNA synthetases. Prog. Nucleic Acid Res. Mol. Biol. 69, 317-349 (Pubitemid 33804680)
25. Zhang, C. M. and Hou, Y. M. (2005) Domain-domain communication for tRNA aminoacylation: the importance of covalent connectivity. Biochemistry 44, 7240-7249
26. Alexander, R. W. and Schimmel, P. (1999) Evidence for breaking domain-domain functional communication in a synthetase-tRNA complex. Biochemistry 38, 16359-16365 (Pubitemid 129520559)
27. Steer, B. A. and Schimmel, P. (1999) Domain-domain communication in a miniature archaebacterial tRNA synthetase. Proc. Natl. Acad. Sci. U.S.A. 96, 13644-13649
28. Lazard, M., Kerjan, P., Agou, F. and Mirande, M. (2000) The tRNA-dependent activation of arginine by arginyl-tRNA synthetase requires inter-domain communication. J. Mol. Biol. 302, 991-1004
29. Uter, N. T. and Perona, J. J. (2004) Long-range intramolecular signaling in a tRNA synthetase complex revealed by pre-steady-state kinetics. Proc. Natl. Acad. Sci. U.S.A. 101, 14396-14401 (Pubitemid 39346760)
30. Xu, M. G., Zhao, M. W. and Wang, E. D. (2004) Leucyl-tRNA synthetase from the hyperthermophilic bacterium Aquifex aeolicus recognizes minihelices. J. Biol. Chem. 279, 32151-32158
31. Zhu, B., Zhao, M. W., Eriani, G. and Wang, E. D. (2007) A present-day aminoacyl-tRNA synthetase with ancestral editing properties. RNA 13, 15-21 (Pubitemid 46026176)
32. Palencia, A., Crépin, T., Vu, M. T., Lincecum, Jr, T. L., Martinis, S. A. and Cusack, S. (2012) Structural dynamics of the aminoacylation and proofreading functional cycle of bacterial leucyl-tRNA synthetase. Nat. Struct. Mol. Biol. 19, 677-684
33. Tan, M., Zhu, B., Zhou, X. L., He, R., Chen, X., Eriani, G. and Wang, E. D. (2010) tRNA-dependent pre-transfer editing by prokaryotic leucyl-tRNA synthetase. J. Biol. Chem. 285, 3235-3244
34. Cusack, S., Yaremchuk, A. and Tukalo, M. (2000) The 2 Å crystal structure of leucyl-tRNA synthetase and its complex with a leucyl-adenylate analogue. EMBO J. 19, 2351-61 (Pubitemid 30259016)
35. Leu in the post-transfer-editing conformation. Nat. Struct. Mol. Biol. 12, 923-930
36. Weimer, K. M., Shane, B. L., Brunetto, M., Bhattacharyya, S. and Hati, S. (2009) Evolutionary basis for the coupled-domain motions in Thermus thermophilus leucyl-tRNA synthetase. J. Biol. Chem. 284, 10088-10099
37. Leu. Sci. China C Life Sci. 41, 225-231
38. Rock, F. L., Mao, W., Yaremchuk, A., Tukalo, M., Crepin, T., Zhou, H., Zhang, Y. K., Hernandez, V., Akama, T., Baker, S. J. et al. (2007) An antifungal agent inhibits an aminoacyl-tRNA synthetase by trapping tRNA in the editing site. Science 316, 1759-1761 (Pubitemid 46988553)
39. Fersht, A. R., Ashford, J. S., Bruton, C. J., Jakes, R., Koch, G. L. and Hartley, B. S. (1975) Active site titration and aminoacyl adenylate binding stoichiometry of aminoacyl-tRNA synthetases. Biochemistry 14, 1-4
40. Gruic-Sovulj, I., Uter, N., Bullock, T. and Perona, J. J. (2005) tRNA-dependent aminoacyl-adenylate hydrolysis by a nonediting class I aminoacyl-tRNA synthetase. J. Biol. Chem. 280, 23978-23986 (Pubitemid 40884886)
41. Zhu, B., Yao, P., Tan, M., Eriani, G. and Wang, E. D. (2009) tRNA-independent pretransfer editing by class I leucyl-tRNA synthetase. J. Biol. Chem. 284, 3418-3424
42. Tan, M., Yan, W., Liu, R. J., Wang, M., Chen, X., Zhou, X. L. and Wang, E. D. (2012) A naturally occurring nonapeptide functionally compensates for the CP1 domain of leucyl-tRNA synthetase to modulate aminoacylation activity. Biochem. J. 443, 477-484