New functions of aminoacyl-tRNA synthetases beyond translation

Nature Reviews Molecular Cell Biology

Volumn 11, Issue 9, 2010, Pages 668-674

  Guo, Min ^a,b   Yang, Xiang Lei ^a   Schimmel, Paul ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CHEMOKINE; AMINO ACID TRANSFER RNA LIGASE; APOPTOSIS SIGNAL REGULATING KINASE 1; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR2; GAMMA INTERFERON; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; PROTEOME; VASCULOTROPIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; AMINOACYLATION; ANGIOGENESIS; ANTICODON; BINDING SITE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; EUKARYOTE; EVOLUTION; GENE DUPLICATION; GENE MUTATION; HOMEOSTASIS; HUMAN; LAST COMMON ANCESTOR; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; RNA SPLICING; RNA TRANSLATION;

AMINO ACYL-TRNA SYNTHETASES; ANIMALS; EUKARYOTA; EVOLUTION, MOLECULAR; HUMANS; PROTEIN BIOSYNTHESIS;

EUKARYOTA;

EID: 77956095201     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm2956     Document Type: Review

References (65)

1. Carter, C. W. Jr. Cognition, mechanism, and evolutionary relationships in aminoacyl-tRNA synthetases. Annu. Rev. Biochem. 62, 715-748 (1993).
2. Woese, C. R., Olsen, G. J., Ibba, M. & Söll, D. Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol. Mol. Biol. Rev. 64, 202-236 (2000).
3. Rodin, S. N. & Ohno, S. Two types of aminoacyl-tRNA synthetases could be originally encoded by complementary strands of the same nucleic acid. Orig. Life Evol. Biosph. 25, 565-589 (1995).
4. Pham, Y. et al. A minimal TrpRS catalytic domain supports sense/antisense ancestry of class I and II aminoacyl-tRNA synthetases. Mol. Cell 25, 851-862 (2007).
5. Ribas de Pouplana, L. & Schimmel, P. Two classes of tRNA synthetases suggested by sterically compatible dockings on tRNA acceptor stem. Cell 104, 191-193 (2001).
6. Terada, T. et al. Functional convergence of two lysyltRNA synthetases with unrelated topologies. Nature Struct. Biol. 9, 257-262 (2002).
7. Ling, J., Reynolds, N. & Ibba, M. Aminoacyl-tRNA synthesis and translational quality control. Annu. Rev. Microbiol. 63, 61-78 (2009).
8. Guo, M. et al. The C-Ala domain brings together editing and aminoacylation functions on one tRNA. Science 325, 744-747 (2009).
9. Guo, M., Schimmel, P. & Yang, X. L. Functional expansion of human tRNA synthetases achieved by structural inventions. FEBS Lett. 584, 434-442 (2010).
10. Rho, S. B. et al. Genetic dissection of protein-protein interactions in multi-tRNA synthetase complex. Proc. Natl Acad. Sci. USA 96, 4488-4493 (1999).
11. Kao, J. et al. Characterization of a novel tumor-derived cytokine. Endothelial-monocyte activating polypeptide II. J. Biol. Chem. 269, 25106-25119 (1994).
12. Ko, Y. G., Park, H. & Kim, S. Novel regulatory interactions and activities of mammalian tRNA synthetases. Proteomics 2, 1304-1310 (2002).
13. Kim, M. J. et al. Downregulation of FUSE-binding protein and c-Myc by tRNA synthetase cofactor p38 is required for lung cell differentiation. Nature Genet. 34, 330-336 (2003).
14. Park, B. J. et al. The haploinsufficient tumor suppressor p18 upregulates p53 via interactions with ATM/ATR. Cell 120, 209-221 (2005).
15. Zhu, X. et al. MSC p43 required for axonal development in motor neurons. Proc. Natl Acad. Sci. USA 106, 15944-15949 (2009).
16. Wakasugi, K. & Schimmel, P. Two distinct cytokines released from a human aminoacyl-tRNA synthetase. Science 284, 147-151 (1999).
17. Wakasugi, K. & Schimmel, P. Highly differentiated motifs responsible for two cytokine activities of a split human tRNA synthetase. J. Biol. Chem. 274, 23155-23159 (1999).
18. Kapoor, M., Otero, F. J., Slike, B. M., Ewalt, K. L. &Yang, X. L. Mutational separation of aminoacylation and cytokine activities of human tyrosyl-tRNA synthetase. Chem. Biol. 16, 531-539 (2009).
19. Wakasugi, K. et al. Induction of angiogenesis by a fragment of human tyrosyl-tRNA synthetase. J. Biol. Chem. 277, 20124-20126 (2002). (Pubitemid 34967300)
20. Strieter, R. M. et al. CXC chemokines: angiogenesis, immunoangiostasis, and metastases in lung cancer. Ann. NY Acad. Sci.1028, 351-360 (2004).
21. Tandle, A. T. et al. Endothelial monocyte activating polypeptide-II modulates endothelial cell responses by degrading hypoxia-inducible factor-1α through interaction with PSMA7, a component of the proteasome. Exp. Cell Res. 315, 1850-1859 (2009).
22. Yang, X. L., Skene, R. J., McRee, D. E. & Schimmel, P. Crystal structure of a human aminoacyl-tRNA synthetase cytokine. Proc. Natl Acad. Sci. USA 99, 15369-15374 (2002). (Pubitemid 35403941)
23. Yang, X. L. et al. Gain-of-function mutational activation of human tRNA synthetase procytokine. Chem. Biol. 14, 1323-1333 (2007).
24. Fleckner, J., Rasmussen, H. H. & Justesen, J. Human interferon γ potently induces the synthesis of a 55-kDa protein (γ2) highly homologous to rabbit peptide chain release factor and bovine tryptophanyl-tRNA synthetase. Proc. Natl Acad. Sci. USA 88, 11520-11524 (1991).
25. Wakasugi, K. et al. A human aminoacyl-tRNA synthetase as a regulator of angiogenesis. Proc. Natl Acad. Sci. USA 99, 173-177 (2002). (Pubitemid 34060336)
26. Kise, Y. et al. A short peptide insertion crucial for angiostatic activity of human tryptophanyl-tRNA synthetase. Nature Struct. Mol. Biol. 11, 149-156 (2004).
27. Dorrell, M. I., Aguilar, E., Scheppke, L., Barnett, F. H. & Friedlander, M. Combination angiostatic therapy completely inhibits ocular and tumor angiogenesis. Proc. Natl Acad. Sci. USA 104, 967-972 (2007).
28. Tzima, E. et al. VE-cadherin links tRNA synthetase cytokine to anti-angiogenic function. J. Biol. Chem. 280, 2405-2408 (2005).
29. Zhou, Q. et al. Orthogonal use of a human tRNA synthetase active site to achieve multifunctionality. Nature Struct. Mol. Biol. 17, 57-61 (2010).
30. Yang, X. L. et al. Crystal structures that suggest late development of genetic code components for differentiating aromatic side chains. Proc. Natl Acad. Sci. USA 100, 15376-15380 (2003).
31. Cerini, C., Semeriva, M. & Gratecos, D. Evolution of the aminoacyl-tRNA synthetase family and the organization of the Drosophila glutamyl-prolyl-tRNA synthetase gene. Intron/exon structure of the gene, control of expression of the two mRNAs, selective advantage of the multienzyme complex. Eur. J. Biochem. 244, 176-185 (1997).
32. Cerini, C. et al. A component of the multisynthetase complex is a multifunctional aminoacyl-tRNA synthetase. EMBO J. 10, 4267-4277 (1991).
33. Mukhopadhyay, R., Jia, J., Arif, A., Ray, P. S. & Fox, P. L. The GAIT system: a gatekeeper of inflammatory gene expression. Trends. Biochem. Sci. 34, 324-331 (2009).
34. Jia, J., Arif, A., Ray, P. S. & Fox, P. L. WHEP domains direct noncanonical function of glutamyl-prolyl tRNA synthetase in translational control of gene expression. Mol. Cell 29, 679-690 (2008).
35. Ray, P. S. et al. A stress-responsive RNA switch regulates VEGFA expression. Nature 457, 915-919 (2009).
36. Kleiman, L. & Cen, S. The tRNALys packaging complex in HIV-1. Int. J. Biochem. Cell Biol. 36, 1776-1786 (2004).
37. Park, S. G. et al. Human lysyl-tRNA synthetase is secreted to trigger proinflammatory response. Proc. Natl Acad. Sci. USA 102, 6356-6361 (2005).
38. Yannay-Cohen, N. et al. LysRS serves as a key signaling molecule in the immune response by regulating gene expression. Mol. Cell 34, 603-611 (2009).
39. Amsterdam, A. et al. Identification of 315 genes essential for early zebrafish development. Proc. Natl Acad. Sci. USA 101, 12792-12797 (2004).
40. Fukui, H., Hanaoka, R. & Kawahara, A. Noncanonical activity of seryl-tRNA synthetase is involved in vascular development. Circ. Res. 104, 1253-1259 (2009).
41. Herzog, W., Muller, K., Huisken, J. & Stainier, D. Y. Genetic evidence for a noncanonical function of seryltRNA synthetase in vascular development. Circ. Res. 104, 1260-1266 (2009).
42. Nilsen, T. W. & Graveley, B. R. Expansion of the eukaryotic proteome by alternative splicing. Nature 463, 457-463 (2010).
43. Koonin, E. V. Orthologs, paralogs, and evolutionary genomics. Annu. Rev. Genet. 39, 309-338 (2005).
44. Hu, S. et al. Profiling the human protein-DNA interactome reveals ERK2 as a transcriptional repressor of interferon signaling. Cell 139, 610-622 (2009).
45. Radisky, D. C., Stallings-Mann, M., Hirai, Y. &Bissell, M. J. Single proteins might have dual but related functions in intracellular and extracellular microenvironments. Nature Rev. Mol. Cell Biol. 10, 228-234 (2009).
46. Piatigorsky, J. Lens crystallins. Innovation associated with changes in gene regulation. J. Biol. Chem. 267, 4277-4280 (1992).
47. Jeffery, C. J. Moonlighting proteins. Trends Biochem. Sci. 24, 8-11 (1999).
48. Jeffery, C. J. Moonlighting proteins: old proteins learning new tricks. Trends Genet. 19, 415-417 (2003).
49. Jeffery, C. J. Moonlighting proteins\an update. Mol. Biosyst. 5, 345-350 (2009).
50. Bashton, M. & Chothia, C. The generation of new protein functions by the combination of domains. Structure 15, 85-99 (2007).
51. Warner, J. R. & McIntosh, K. B. How common are extraribosomal functions of ribosomal proteins? Mol. Cell 34, 3-11 (2009).
52. Blumenthal, T. & Carmichael, G. G. RNA replication: function and structure of Qβ-replicase. Annu. Rev. Biochem. 48, 525-548 (1979).
53. Wool, I. G. Extraribosomal functions of ribosomal proteins. Trends Biochem. Sci. 21, 164-165 (1996).
54. Sampath, P. et al. Noncanonical function of glutamyl-prolyl-tRNA synthetase: gene-specific silencing of translation. Cell 119, 195-208 (2004).
55. Mukhopadhyay, R. et al. DAPK-ZIPK-L13a axis constitutes a negative-feedback module regulating inflammatory gene expression. Mol. Cell 32, 371-382 (2008).
56. Tekle, Y. I., Grant, J. R., Kovner, A. M., Townsend, J. P. & Katz, L. A. Identification of new molecular markers for assembling the eukaryotic tree of life. Mol. Phylogenet. Evol. 55, 1177-1182 (2010).
57. Kaminska, M., Shalak, V. & Mirande, M. The appended C-domain of human methionyl-tRNA synthetase has a tRNA-sequestering function. Biochemistry 40, 14309-14316 (2001).
58. Kyriacou, S. V. & Deutscher, M. P. An important role for the multienzyme aminoacyl-tRNA synthetase complex in mammalian translation and cell growth. Mol. Cell 29, 419-427 (2008).
59. Ko, Y. G. et al. Glutamine-dependent antiapoptotic interaction of human glutaminyl-tRNA synthetase with apoptosis signal-regulating kinase 1. J. Biol. Chem. 276, 6030-6036 (2001).
60. Antonellis, A. et al. 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 (2003).
61. Park, S. G., Schimmel, P. & Kim, S. Aminoacyl tRNA synthetases and their connections to disease. Proc. Natl Acad. Sci. USA 105, 11043-11049 (2008).
62. Antonellis, A. & Green, E. D. The role of aminoacyltRNA synthetases in genetic diseases. Annu. Rev. Genomics Hum. Genet. 9, 87-107 (2008).
63. Seburn, K. L., Nangle, L. A., Cox, G. A., Schimmel, P. &Burgess, R. W. An active dominant mutation of glycyl-tRNA synthetase causes neuropathy in a Charcot-Marie-Tooth 2D mouse model. Neuron 51, 715-726 (2006).
64. Nangle, L. A., Zhang, W., Xie, W., Yang, X. L. &Schimmel, P. Charcot-Marie-Tooth diseaseassociated mutant tRNA synthetases linked to altered dimer interface and neurite distribution defect. Proc. Natl Acad. Sci. USA 104, 11239-11244 (2007).
65. Storkebaum, E. et al. Dominant mutations in the tyrosyl-tRNA synthetase gene recapitulate in Drosophila features of human Charcot-Marie-Tooth neuropathy. Proc. Natl Acad. Sci. USA 106, 11782-11787 (2009).