Human cytoplasmic ProX edits mischarged tRNAPro with amino acid but not tRNA specificity

Biochemical Journal

Volumn 450, Issue 1, 2013, Pages 243-252

  Ruan, Liang Liang ^a   Zhou, Xiao Long ^a   Tan, Min ^a   Wang, En Duo ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

Aminoacyl tRNA synthetase; ProX; Specificity determinant; TRNA editing; TRNA specificity; TRNAPro

Indexed keywords

ALANINE; AMINO ACID; HSPROX PROTEIN; PROTEIN; RECOMBINANT PROTEIN; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; DEACYLATION; EMBRYO; HUMAN; HUMAN CELL; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMINO ACIDS; AMINO ACYL-TRNA SYNTHETASES; BINDING SITES; CYTOPLASM; HUMANS; HYDROLYSIS; RNA EDITING; RNA, TRANSFER; RNA, TRANSFER, PRO; SUBSTRATE SPECIFICITY;

EID: 84873035361     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121493     Document Type: Article

References (41)

1. Ibba, M. and Söll, D. (2000) Aminoacyl-tRNA synthesis. Annu. Rev. Biochem. 69, 617-650
2. Zhou, X. L., Wang, M., Tan, M., Huang, Q. A., Eriani, G. and Wang, E. D. (2010) Functional characterization of leucine-specific domain 1 from eukaryal and archaeal leucyl-tRNA synthetases. Biochem. J. 429, 505-513
3. Fersht, A. R. (1981) Enzymic editing mechanisms and the genetic-code. Proc. R. Soc. London Ser. B 212, 351-379
4. Nureki, O., Vassylyev, D. G., Tateno, M., Shimada, A., Nakama, T., Fukai, S., Konno, M., Hendrickson, T. L., Schimmel, P. and Yokoyama, S. (1998) Enzyme structure with two catalytic sites for double-sieve selection of substrate. Science 280, 578-582
5. Zhou, X. L., Zhu, B. and Wang, E. D. (2008) The CP2 domain of leucyl-tRNA synthetase is crucial for amino acid activation and post-transfer editing. J. Biol. Chem. 283, 36608-36616
6. 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
7. Liu, R. J., Tan, M., Du, D. H., Xu, B. S., Eriani, G. and Wang, E. D. (2011) Peripheral insertion modulates the editing activity of the isolated CP1 domain of leucyl-tRNA synthetase. Biochem. J. 440, 217-227
8. 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
9. 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
10. 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
11. Zhou, X. L., Tan, M., Wang, M., Chen, X. and Wang, E. D. (2010) Post-transfer editing by a eukaryotic leucyl-tRNA synthetase resistant to the broad-spectrum drug AN2690. Biochem. J. 430, 325-333
12. Fukai, S., Nureki, O., Sekine, S., Shimada, A., Tao, J. S., 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
13. Roy, H., Ling, J. Q., Irnov, M. and Ibba, M. (2004) Post-transfer editing in vitro and in vivoby the β subunit of phenylalanyl-tRNA synthetase. EMBO J. 23, 4639-4648
14. Dock-Bregeon, A., Sankaranarayanan, R., Romby, P., Caillet, J., Springer, M., Rees, B., Francklyn, C. S., Ehresmann, C. and Moras, D. (2000) Transfer RNA-mediated editing in threonyl-tRNA synthetase. The class II solution to the double discrimination problem. Cell 103, 877-884
15. Zhou, X. L., Ruan, Z. R., Huang, Q., Tan, M. and Wang, E. D. (2012) Translational fidelity maintenance preventing Ser mis-incorporation at Thr codon in protein from eukaryote. Nucleic Acids Res., doi: 10.1093/nar/gks982
16. 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
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
18. 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
19. Korencic, D., Ahel, I., Schelert, J., Sacher, M., Ruan, B. F., 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
20. An, S. and Musier-Forsyth, K. (2004) Trans-editing of Cys-tRNAPro by Haemophilus influenzae YbaK protein. J. Biol. Chem. 279, 42359-42362
21. Heacock, D., Forsyth, C. J., Shiba, K. and Musier-Forsyth, K. (1996) Synthesis and aminoacyl-tRNA synthetase inhibitory activity of prolyl adenylate analogs. Bioorg. Chem. 24, 273-289
22. Beuning, P. J. and Musier-Forsyth, K. (2001) Species-specific differences in amino acid editing by class II prolyl-tRNA synthetase. J. Biol. Chem. 276, 30779-30785
23. Bunjun, S., Stathopoulos, C., Graham, D., Min, B., Kitabatake, M., Wang, A. L., Wang, C. C., Vivares, C. P., Weiss, L. M. and Söll, D. (2000) A dual-specificity aminoacyl-tRNA synthetase in the deep-rooted eukaryote Giardia lamblia. Proc. Natl. Acad. Sci. U.S.A. 97, 12997-13002
24. Ahel, I., Stathopoulos, C., Ambrogelly, A., Sauerwald, A., Toogood, H., Hartsch, T. and Söll, D. (2002) Cysteine activation is an inherent in vitro property of prolyl-tRNA synthetases. J. Biol. Chem. 277, 34743-34748
25. Pro with cysteine. J. Biol. Chem. 277, 34749-34754
26. Crepin, T., Yaremchuk, A., Tukalo, M. and Cusack, S. (2006) Structures of two bacterial prolyl-tRNA synthetases with and without a cis-editing domain. Structure 14, 1511-1525
27. Wong, F. C., Beuning, P. J., Nagan, M., Shiba, K. and Musier-Forsyth, K. (2002) Functional role of the prokaryotic proline-tRNA synthetase insertion domain in amino acid editing. Biochemistry 41, 7108-7115
28. Zhou, X. L., Du, D. H., Tan, M., Lei, H. Y., Ruan, L. L., Eriani, G. and Wang, E. D. (2011) Role of tRNA amino acid-accepting end in aminoacylation and its quality control. Nucleic Acids Res. 39, 8857-8868
29. Palencia, A., Crepin, T., Vu, M. T., Lincecum, 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
30. Ling, J. Q., Reynolds, N. and Ibba, M. (2009) Aminoacyl-tRNA synthesis and translational quality control. Annu. Rev. Microbiol. 63, 61-78
31. Nangle, L. A., De Crecy Lagard, V., Doring, V. and Schimmel, P. (2002) Genetic code ambiguity. Cell viability related to the severity of editing defects in mutant tRNA synthetases. J. Biol. Chem. 277, 45729-45733
32. Bacher, J. M., de Crecy-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
33. Yao, P., Zhou, X. L., He, R., Xue, M. Q., Zheng, Y. G., Wang, Y. F. and Wang, E. D. (2008) Unique residues crucial for optimal editing in yeast cytoplasmic leucyl-tRNA synthetase are revealed by using a novel knockout yeast strain. J. Biol. Chem. 283, 22591-22600
34. 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
35. Lehmann, S., Funck, D., Szabados, L. and Rentsch, D. (2010) Proline metabolism and transport in plant development. Amino Acids 39, 949-962
36. Nawaz, M. H., Merriman, E., Yang, X. L. and Schimmel, P. (2011) p23(H) implicated as cis/trans regulator of AlaXp-directed editing for mammalian cell homeostasis. Proc. Natl. Acad. Sci. U.S.A. 108, 2723-2728
37. Pro editing by Haemophilus influenzae YbaK via a novel synthetase.YbaK.tRNA ternary complex. J. Biol. Chem. 280, 34465-34472
38. Cys deacylase. J. Biol. Chem. 280, 25887-25891
39. LaRiviere, F. J., Wolfson, A. D. and Uhlenbeck, O. C. (2001) Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science 294, 165-168
40. Sivaram, P. and Deutscher, M. P. (1990) Existence of two forms of rat liver arginyl-tRNA synthetase suggests channeling of aminoacyl-tRNA for protein synthesis. Proc. Natl. Acad. Sci. U.S.A. 87, 3665-3669
41. Xu, M. G., Li, J., Du, X. and Wang, E. D. (2004) Groups on the side chain of T252 in Escherichia colileucyl-tRNA synthetase are important for discrimination of amino acids and cell viability. Biochem. Biophys. Res. Commun. 318, 11-16