A WHEP domain regulates the dynamic structure and activity of Caenorhabditis elegans glycyl-tRNA synthetase

Journal of Biological Chemistry

Volumn 291, Issue 32, 2016, Pages 16567-16575

  Chang, Chih Yao ^a   Chien, Chin I ^a   Chang, Chia Pei ^a   Lin, Bo Chun ^a   Wang, Chien Chia ^a  

^a NATIONAL CENTRAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY;

AMINOACYL-TRNA SYNTHETASES; CAENORHABDITIS ELEGANS; CATALYTIC EFFICIENCIES; DELETION MUTANTS; DYNAMIC STRUCTURE; MITOCHONDRIAL DEFECTS; N-TERMINAL SEQUENCES; STRUCTURAL FLEXIBILITIES;

ENZYME ACTIVITY;

GLYCINE TRANSFER RNA LIGASE; ISOENZYME; CAENORHABDITIS ELEGANS PROTEIN; GRS1 PROTEIN, S CEREVISIAE; MITOCHONDRIAL PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO TERMINAL SEQUENCE; AMINOACYLATION; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME STRUCTURE; GENE; GENE FUNCTION; GRS1 GENE; INTRACELLULAR SIGNALING; MAD DOMAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN TARGETING; RNA BINDING; THERMOSTABILITY; UPREGULATION; WHEP DOMAIN; ANIMAL; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; SACCHAROMYCES CEREVISIAE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GLYCINE-TRNA LIGASE; MITOCHONDRIAL PROTEINS; PROTEIN DOMAINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84982851925     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.730812     Document Type: Article

References (35)

1. Carter, C. W., Jr. (1993) Cognition, mechanism, and evolutionary relationships in aminoacyl-tRNA synthetases. Annu. Rev. Biochem. 62, 715-748
2. Burbaum, J. J., and Schimmel, P. (1991) Structural relationships and the classification of aminoacyl-tRNA synthetases. J. Biol. Chem. 266, 16965-16968
3. Giegé, R. (2006) The early history of tRNA recognition by aminoacyl-tRNA synthetases. J Biosci 31, 477-488
4. Giegé, R., Sissler, M., and Florentz, C. (1998) Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res. 26, 5017-5035
5. Huang, H. Y., Tang, H. L., Chao, H. Y., Yeh, L. S., and Wang, C. C. (2006) An unusual pattern of protein expression and localization of yeast alanyl-tRNA synthetase isoforms. Mol. Microbiol. 60, 189-198
6. Tang, H. L., Yeh, L. S., Chen, N. K., Ripmaster, T., Schimmel, P., and Wang, C. C. (2004) Translation of a yeast mitochondrial tRNA synthetase initiated at redundant non-AUG codons. J. Biol. Chem. 279, 49656-49663
7. Chang, K. J., and Wang, C. C. (2004) Translation initiation from a naturally occurring non-AUG codon in Saccharomyces cerevisiae. J. Biol. Chem. 279, 13778-13785
8. Natsoulis, G., Hilger, F., and Fink, G. R. (1986) The HTS1 gene encodes both the cytoplasmic and mitochondrial histidine tRNA synthetases of S. cerevisiae. Cell 46, 235-243
9. Chatton, B., Walter, P., Ebel, J. P., Lacroute, F., and Fasiolo, F. (1988) The yeast VAS1 gene encodes both mitochondrial and cytoplasmic valyl-tRNA synthetases. J. Biol. Chem. 263, 52-57
10. Mazauric, M. H., Reinbolt, J., Lorber, B., Ebel, C., Keith, G., Giegé, R., and Kern, D. (1996) An example of non-conservation of oligomeric structure in prokaryotic aminoacyl-tRNA synthetases. Biochemical and structural properties of glycyl-tRNA synthetase from Thermus thermophilus. Eur. J. Biochem. 241, 814-826
11. Ostrem, D. L., and Berg, P. (1970) Glycyl-tRNA synthetase: an oligomeric protein containing dissimilar subunits. Proc. Natl. Acad. Sci. U.S.A. 67, 1967-1974
12. Nada, S., Chang, P. K., and Dignam, J. D. (1993) Primary structure of the gene for glycyl-tRNA synthetase from Bombyx mori. J. Biol. Chem. 268, 7660-7667
13. Shiba, K., Schimmel, P., Motegi, H., and Noda, T. (1994) Human glycyl-tRNA synthetase. Wide divergence of primary structure from bacterial counterpart and species-specific aminoacylation. J. Biol. Chem. 269, 30049-30055
14. Chien, C. I., Chen, Y. L., Chen, S. J., Chou, C. M., Chen, C. Y., and Wang, C. C. (2015) Vanderwaltozyma polyspora possesses two glycyl-tRNA synthetase genes: One constitutive and one inducible. Fungal Genet. Biol. 76, 47-56
15. Mazauric, M. H., Keith, G., Logan, D., Kreutzer, R., Giegé, R., and Kern, D. (1998) Glycyl-tRNA synthetase from Thermus thermophilus: wide structural divergence with other prokaryotic glycyl-tRNA synthetases and functional inter-relation with prokaryotic and eukaryotic glycylation systems. Eur. J. Biochem. 251, 744-757
16. Krajewski, K. M., Lewis, R. A., Fuerst, D. R., Turansky, C., Hinderer, S. R., Garbern, J., Kamholz, J., and Shy, M. E. (2000) Neurological dysfunction and axonal degeneration in Charcot-Marie-Tooth disease type 1A. Brain 123, 1516-1527
17. Antonellis, A., Ellsworth, R. E., Sambuughin, N., Puls, I., Abel, A., Lee-Lin, S. Q., Jordanova, A., Kremensky, I., Christodoulou, K., Middleton, L. T., Sivakumar, K., Ionasescu, V., Funalot, B., Vance, J. M., Goldfarb, L. G., et al. (2003) Glycyl tRNA synthetase mutations in Charcot-Marie-Tooth disease type 2D and distal spinal muscular atrophy type V. Am. J. Hum. Genet. 72, 1293-1299
18. Motley, W. W., Talbot, K., and Fischbeck, K. H. (2010) GARS axonopathy: not every neuron's cup of tRNA. Trends Neurosci. 33, 59-66
19. Nangle, L. A., Zhang, W., Xie, W., Yang, X. L., and Schimmel, P. (2007) Charcot-Marie-Tooth disease-associated mutant tRNA synthetases linked to altered dimer interface and neurite distribution defect. Proc. Natl. Acad. Sci. U.S.A. 104, 11239-11244
20. Achilli, F., Bros-Facer, V., Williams, H. P., Banks, G. T., AlQatari, M., Chia, R., Tucci, V., Groves, M., Nickols, C. D., Seburn, K. L., Kendall, R., Cader, M. Z., Talbot, K., van Minnen, J., Burgess, R. W., et al. (2009) An ENU-induced mutation in mouse glycyl-tRNA synthetase (GARS) causes peripheral sensory and motor phenotypes creating a model of Charcot-Marie-Tooth type 2D peripheral neuropathy. Dis. Model Mech. 2, 359-373
21. Grice, S. J., Sleigh, J. N., Motley, W. W., Liu, J. L., Burgess, R. W., Talbot, K., and Cader, M. Z. (2015) Dominant, toxic gain-of-function mutations in gars lead to non-cell autonomous neuropathology. Hum. Mol. Genet. 24, 4397-4406
22. Chang, C. P., Chang, C. Y., Lee, Y. H., Lin, Y. S., and Wang, C. C. (2015) Divergent alanyl-tRNA synthetase genes of Vanderwaltozyma polyspora descended from a common ancestor through whole-genome duplication followed by asymmetric evolution. Mol. Cell. Biol. 35, 2242-2253
23. Liao, C. C., Lin, C. H., Chen, S. J., and Wang, C. C. (2012) Trans-kingdom rescue of Gln-tRNAGln synthesis in yeast cytoplasm and mitochondria. Nucleic Acids Res. 40, 9171-9181
24. Sakurai, M., Ohtsuki, T., and Watanabe, K. (2005) Modification at position 9 with 1-methyladenosine is crucial for structure and function of nematode mitochondrial tRNAs lacking the entire T-arm. Nucleic Acids Res. 33, 1653-1661
25. Jakubowski, H. (2012) Quality control in tRNA charging. Wiley Interdiscip Rev. RNA 3, 295-310
26. Martinis, S. A., Plateau, P., Cavarelli, J., and Florentz, C. (1999) Aminoacyl-tRNA synthetases: a family of expanding functions. EMBO J. 18, 4591-4596
27. Park, M. C., Kang, T., Jin, D., Han, J. M., Kim, S. B., Park, Y. J., Cho, K., Park, Y. W., Guo, M., He, W., Yang, X. L., Schimmel, P., and Kim, S. (2012) Secreted human glycyl-tRNA synthetase implicated in defense against ERK-activated tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 109, E640-E647
28. He, W., Bai, G., Zhou, H., Wei, N., White, N. M., Lauer, J., Liu, H., Shi, Y., Dumitru, C. D., Lettieri, K., Shubayev, V., Jordanova, A., Guergueltcheva, V., Griffin, P. R., Burgess, R. W., et al. (2015) CMT2D neuropathy is linked to the neomorphic binding activity of glycyl-tRNA synthetase. Nature 526, 710-714
29. Ray, P. S., and Fox, P. L. (2014) Origin and evolution of glutamyl-prolyl tRNA synthetase WHEP domains reveal evolutionary relationships within Holozoa. PLoS One 9, e98493
30. Jia, J., Arif, A., Ray, P. S., and Fox, P. L. (2008) WHEP domains direct noncanonical function of glutamyl-prolyl tRNA synthetase in translational control of gene expression. Mol. Cell 29, 679-690
31. He, W., Zhang, H. M., Chong, Y. E., Guo, M., Marshall, A. G., and Yang, X. L. (2011) Dispersed disease-causing neomorphic mutations on a single protein promote the same localized conformational opening. Proc. Natl. Acad. Sci. U.S.A. 108, 12307-12312
32. Turner, R. J., Lovato, M., and Schimmel, P. (2000) One of two genes encoding glycyl-tRNA synthetase in Saccharomyces cerevisiae provides mitochondrial and cytoplasmic functions. J. Biol. Chem. 275, 27681-27688
33. Chang, C. P., Tseng, Y. K., Ko, C. Y., and Wang, C. C. (2012) Alanyl-tRNA synthetase genes of Vanderwaltozyma polyspora arose from duplication of a dual-functional predecessor of mitochondrial origin. Nucleic Acids Res. 40, 314-322
34. Chang, C. P., Lin, G., Chen, S. J., Chiu, W. C., Chen, W. H., and Wang, C. C. (2008) Promoting the formation of an active synthetase/tRNA complex by a nonspecific tRNA-binding domain. J. Biol. Chem. 283, 30699-30706
35. Ladror, U. S., Egan, D. A., Snyder, S. W., Capobianco, J. O., Goldman, R. C., Dorwin, S. A., Johnson, R. W., Edalji, R., Sarthy, A. V., McGonigal, T., Walter, K. A., and Holzman, T. F. (1998) Domain structure analysis of elongation factor-3 from Saccharomyces cerevisiae by limited proteolysis and differential scanning calorimetry. Protein Sci. 7, 2595-2601