The mechanism of pre-transfer editing in yeast mitochondrial threonyl-tRNA synthetase

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 28518-28525

  Ling, Jiqiang ^a   Peterson, Kaitlyn M ^b   Simonovic, Ivana ^b   Söll, Dieter ^a   Simonovic, Miljan ^b  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ADENYLATE; AMINOACYLATION; BIOLOGICAL PROCESS; CELLULAR FUNCTION; CONFORMATIONAL CHANGE; NUCLEOPHILIC ATTACK; SYNTHETASES; THREONYL-TRNA SYNTHETASE; WATER MOLECULE;

MOLECULES; YEAST;

AMINO ACIDS;

ADENOSINE PHOSPHATE; MITOCHONDRIAL THREONYL TRNA SYNTHETASE; SERINE; THREONINE; THREONINE TRANSFER RNA LIGASE; UNCLASSIFIED DRUG;

AMINOACYLATION; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME BINDING; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME MODIFICATION; ENZYME STABILITY; HYDROLYSIS KINETICS; MOLECULAR DYNAMICS; NUCLEOPHILICITY; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CRYSTALLOGRAPHY, X-RAY; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA EDITING; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; THREONINE-TRNA LIGASE;

EID: 84865211306     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.372920     Document Type: Article

References (45)

1. Ibba, M., and Söll, D. (2000) Aminoacyl-tRNA synthesis. Annu. Rev. Biochem. 69, 617-650
2. Ruan, B., Palioura, S., Sabina, J., Marvin-Guy, L., Kochhar, S., Larossa, R. A., and Söll, D. (2008) Quality control despite mistranslation caused by an ambiguous genetic code. Proc. Natl. Acad. Sci. U.S.A. 105, 16502-16507
3. Netzer, N., Goodenbour, J. M., David, A., Dittmar, K. A., Jones, R. B., Schneider, J. R., Boone, D., Eves, E. M., Rosner, M. R., Gibbs, J. S., Embry, A., Dolan, B., Das, S., Hickman, H. D., Berglund, P., Bennink, J. R., Yewdell, J. W., and Pan, T. (2009) Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462, 522-526
4. Li, L., Boniecki, M. T., Jaffe, J. D., Imai, B. S., Yau, P. M., Luthey-Schulten, Z. A., and Martinis, S. A. (2011) Naturally occurring aminoacyl-tRNA synthetases editing-domain mutations that cause mistranslation in Mycoplasma parasites. Proc. Natl. Acad. Sci. U.S.A. 108, 9378-9383
5. Reynolds, N. M., Lazazzera, B. A., and Ibba, M. (2010) Cellular mechanisms that control mistranslation. Nat. Rev. Microbiol. 8, 849-856
6. 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
7. Roy, H., Ling, J., Irnov, M., and Ibba, M. (2004) Post-transfer editing in vitro and in vivo by the β-subunit of phenylalanyl-tRNA synthetase. EMBO J. 23, 4639-4648
8. Karkhanis, V. A., Mascarenhas, A. P., and Martinis, S. A. (2007) Amino acid toxicities of Escherichia coli that are prevented by leucyl-tRNA synthetase amino acid editing. J. Bacteriol. 189, 8765-8768
9. Reynolds, N. M., Ling, J., Roy, H., Banerjee, R., Repasky, S. E., Hamel, P., and Ibba, M. (2010) Cell-specific differences in the requirements for translation quality control. Proc. Natl. Acad. Sci. U.S.A. 107, 4063-4068
10. 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
11. Ling, J., Reynolds, N., and Ibba, M. (2009) Aminoacyl-tRNA synthesis and translational quality control. Annu. Rev. Microbiol. 63, 61-78
12. Mascarenhas, A. P., An, S., Rosen, A. E., Martinis, S. A., and Musier- Forsyth, K. (2008) in Protein Engineering (RajBhandary, U. L., and Köhrer, C., eds) pp. 153-200, Springer-Verlag, New York
13. Schmidt, E., and Schimmel, P. (1994) Mutational isolation of a sieve for editing in a transfer RNA synthetase. Science 264, 265-267
14. 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
15. Lincecum, T. L., Jr., Tukalo, M., Yaremchuk, A., Mursinna, R. S., Williams, A. M., Sproat, B. S., Van Den Eynde, W., Link, A., Van Calenbergh, S., Grøtli, M., Martinis, S. A., and Cusack, S. (2003) Structural and mechanistic basis of pre- and post-transfer editing by leucyl-tRNA synthetase. Mol. Cell 11, 951-963
16. An, S., and Musier-Forsyth, K. (2004) Trans-editing of Cys-tRNAPro by Haemophilus influenzae YbaK protein. J. Biol. Chem. 279, 42359-42362
17. Guo, M., Chong, Y. E., Shapiro, R., Beebe, K., Yang, X. L., and Schimmel, P. (2009) Paradox of mistranslation of serine for alanine caused by AlaRS recognition dilemma. Nature 462, 808-812
18. Dock-Bregeon, A. C., Rees, B., Torres-Larios, A., Bey, G., Caillet, J., and Moras, D. (2004) Achieving error-free translation: the mechanism of proofreading of threonyl-tRNA synthetase at atomic resolution. Mol. Cell 16, 375-386
19. Baldwin, A. N., and Berg, P. (1966) Transfer ribonucleic acid-induced hydrolysis of valyladenylate bound to isoleucyl ribonucleic acid synthetase. J. Biol. Chem. 241, 839-845
20. Jakubowski, H. (1978) Valyl-tRNA synthetase from yellow lupin seeds: instability of enzyme-bound noncognate adenylates versus cognate adenylate. FEBS Lett. 95, 235-238
21. Nomanbhoy, T. K., Hendrickson, T. L., and Schimmel, P. (1999) Transfer RNA-dependent translocation of misactivated amino acids to prevent errors in protein synthesis. Mol. Cell 4, 519-528
22. Fukunaga, R., and Yokoyama, S. (2006) Structural basis for substrate recognition by the editing domain of isoleucyl-tRNA synthetase. J. Mol. Biol. 359, 901-912
23. Gruic-Sovulj, I., Rokov-Plavec, J., and Weygand-Durasevic, I. (2007) Hydrolysis of non-cognate aminoacyl-adenylates by a class II aminoacyltRNA synthetase lacking an editing domain. FEBS Lett. 581, 5110-5114
24. Splan, K. E., Ignatov, M. E., and Musier-Forsyth, K. (2008) Transfer RNA modulates the editing mechanism used by class II prolyl-tRNA synthetase. J. Biol. Chem. 283, 7128-7134
25. Boniecki, M. T., Vu, M. T., Betha, A. K., and Martinis, S. A. (2008) CP1- dependent partitioning of pre-transfer and post-transfer editing in leucyltRNA synthetase. Proc. Natl. Acad. Sci. U.S.A. 105, 19223-19228
26. Minajigi, A., and Francklyn, C. S. (2010) Aminoacyl transfer rate dictates choice of editing pathway in threonyl-tRNA synthetase. J. Biol. Chem. 285, 23810-23817
27. Roy, H., Ling, J., Alfonzo, J., and Ibba, M. (2005) Loss of editing activity during the evolution of mitochondrial phenylalanyl-tRNA synthetase.J. Biol. Chem. 280, 38186-38192
28. Copeland, R. A. (2000) in Enzymes: A Practical Introduction to Structure, Mechanism, and Data Analysis (Copeland, R. A., ed) 2 Ed., pp. 305-317, John Wiley and Sons, New York
29. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
30. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
31. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc- Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
32. Emsley, P., and Cowtan, K. (2004) COOT: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
33. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of COOT. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
34. 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
35. Su, D., Lieberman, A., Lang, B. F., Simonović, M., Söll, D., and Ling, J. (2011) An unusual tRNAThr derived from tRNAHis reassigns in yeast mitochondria the CUN codons to threonine. Nucleic Acids Res. 39, 4866-4874
36. Ling, J., Peterson, K. M., Simonović, I., Cho, C., Söll, D., and Simonović,M. (2012) Yeast mitochondrial threonyl-tRNA synthetase recognizes tRNA isoacceptors by distinct mechanisms and promotes CUN codon reassignment. Proc. Natl. Acad. Sci. U.S.A. 109, 3281-3286
37. Zaher, H. S., and Green, R. (2009) Fidelity at the molecular level: lessons from protein synthesis. Cell 136, 746-762
38. Drummond, D. A., and Wilke, C. O. (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134, 341-352
39. Drummond, D. A., and Wilke, C. O. (2009) The evolutionary consequences of erroneous protein synthesis. Nat. Rev. Genet. 10, 715-724
40. Guo, M., and Schimmel, P. (2012) Structural analyses clarify the complex control of mistranslation by tRNA synthetases. Curr. Opin. Struct. Biol. 22, 119-126
41. Sarkar, J., and Martinis, S. A. (2011) Amino acid-dependent shift in tRNA synthetase editing mechanisms. J. Am. Chem. Soc. 133, 18510-18513
42. Lue, S. W., and Kelley, S. O. (2005) An aminoacyl-tRNA synthetase with a defunct editing site. Biochemistry 44, 3010-3016
43. Hendrickson, T. L., Nomanbhoy, T. K., de Crécy-Lagard, V., Fukai, S., Nureki, O., Yokoyama, S., and Schimmel, P. (2002) Mutational separation of two pathways for editing by a class I tRNA synthetase. Mol. Cell 9, 353-362
44. Hati, S., Ziervogel, B., Sternjohn, J., Wong, F. C., Nagan, M. C., Rosen, A. E., Siliciano, P. G., Chihade, J. W., and Musier-Forsyth, K. (2006) Pretransfer editing by class II prolyl-tRNA synthetase: role of aminoacylation active site in "selective release" of noncognate amino acids. J. Biol. Chem. 281, 27862-27872
45. 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