Essential nontranslational functions of tRNA synthetases

Nature Chemical Biology

Volumn 9, Issue 3, 2013, Pages 145-153

  Paul, Min ^a   Schimmel, Paul ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMINO ACID TRANSFER RNA LIGASE; APOPTOSIS SIGNAL REGULATING KINASE 1; APTAMER; BIOLOGICAL MARKER; DNA DEPENDENT PROTEIN KINASE; GLUTAMINE; LEUCINE; MESSENGER RNA; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SCAFFOLD PROTEIN; SYNTHETASE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN A;

AMINOACYLATION; ANIMAL; ANTIANGIOGENIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ATAXIA; AUTOIMMUNE DISEASE; BINDING SITE; CANCER CONTROL; CANCER THERAPY; CARDIOVASCULAR SYSTEM; CELL STRAIN HEK293; COLORECTAL CANCER; CONFORMATIONAL TRANSITION; DERMATOMYOSITIS; DIMERIZATION; DNA DAMAGE; EUKARYOTE; HOMEOSTASIS AND REGULATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; LYSOSOME MEMBRANE; MAMMAL CELL; METASTASIS; NERVE DEGENERATION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PANCREAS CANCER; POLYMYOSITIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; UBIQUITINATION;

AMINO ACYL-TRNA SYNTHETASES; ANIMALS; BIOCATALYSIS; HUMANS; MODELS, MOLECULAR; PROTEIN BIOSYNTHESIS; RNA, TRANSFER, AMINO ACYL;

EID: 84874028131     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1158     Document Type: Review

References (100)

1. Carter, C.W. Jr. Cognition, mechanism, and evolutionary relationships in aminoacyl-tRNA synthetases. Annu. Rev. Biochem. 62, 715-748 (1993).
2. Ibba, M. & Söll, D. Aminoacyl-tRNA synthesis. Annu. Rev. Biochem. 69, 617-650 (2000).
3. Ryckelynck, M., Giegé, R. & Frugier, M. tRNAs and tRNA mimics as cornerstones of aminoacyl-tRNA synthetase regulations. Biochimie 87, 835-845 (2005). (Pubitemid 41297810)
4. Putney, S.D. & Schimmel, P. An aminoacyl tRNA synthetase binds to a specific DNA sequence and regulates its gene transcription. Nature 291, 632-635 (1981). (Pubitemid 11033562)
5. Sarkar, J., Poruri, K., Boniecki, M.T., McTavish, K.K. & Martinis, S.A. Yeast mitochondrial leucyl-tRNA synthetase CP1 domain has functionally diverged to accommodate RNA splicing at expense of hydrolytic editing. J. Biol. Chem. 287, 14772-14781 (2012).
6. Paukstelis, P.J., Chen, J.H., Chase, E., Lambowitz, A.M. & Golden, B.L. Structure of a tyrosyl-tRNA synthetase splicing factor bound to a group I intron RNA. Nature 451, 94-97 (2008).
7. Arnez, J.G. & Moras, D. Structural and functional considerations of the aminoacylation reaction. Trends Biochem. Sci. 22, 211-216 (1997). (Pubitemid 27246637)
8. Torres-Larios, A., Sankaranarayanan, R., Rees, B., Dock-Bregeon, A.C. & Moras, D. Conformational movements and cooperativity upon amino acid, ATP and tRNA binding in threonyl-tRNA synthetase. J. Mol. Biol. 331, 201-211 (2003).
9. Jain, M. et al. Metabolite profiling identifies a key role for glycine in rapid cancer cell proliferation. Science 336, 1040-1044 (2012).
10. Possemato, R. et al. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 476, 346-350 (2011).
11. Wang, J. et al. Dependence of mouse embryonic stem cells on threonine catabolism. Science 325, 435-439 (2009).
12. Kim, J. & Guan, K.L. Amino acid signaling in TOR activation. Annu. Rev. Biochem. 80, 1001-1032 (2011).
13. Han, J.M. et al. Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell 149, 410-424 (2012).
14. Segev, N. & Hay, N. Hijacking leucyl-tRNA synthetase for amino acid-dependent regulation of TORC1. Mol. Cell 46, 4-6 (2012).
15. Hoffman, R.M. Tumor-seeking Salmonella amino acid auxotrophs. Curr. Opin. Biotechnol. 22, 917-923 (2011).
16. Ruggiero, R.A. et al. Concomitant tumor resistance: the role of tyrosine isomers in the mechanisms of metastases control. Cancer Res. 72, 1043-1050 (2012).
17. Levine, A.J. & Puzio-Kuter, A.M. The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 330, 1340-1344 (2010).
18. DeBerardinis, R.J. & Cheng, T. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 29, 313-324 (2010).
19. Wise, D.R. et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc. Natl. Acad. Sci. USA 105, 18782-18787 (2008).
20. Hattori, K., Naguro, I., Runchel, C. & Ichijo, H. The roles of ASK family proteins in stress responses and diseases. Cell Commun. Signal. 7, 9 (2009).
21. 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).
22. Wahab, S.Z. & Yang, D.C. Synthesis of diadenosine 5′,5′′′-P1,P4-tetraphosphate by lysyl-tRNA synthetase and a multienzyme complex of aminoacyl-tRNA synthetases from rat liver. J. Biol. Chem. 260, 5286-5289 (1985). (Pubitemid 15003267)
23. Zamecnik, P. Diadenosine 5′,5′′′-P1,P4- tetraphosphate (Ap4A): its role in cellular metabolism. Anal. Biochem. 134, 1-10 (1983).
24. Bochner, B.R., Lee, P.C., Wilson, S.W., Cutler, C.W. & Ames, B.N. AppppA and related adenylylated nucleotides are synthesized as a consequence of oxidation stress. Cell 37, 225-232 (1984). (Pubitemid 14079854)
25. Lee, Y.N., Nechushtan, H., Figov, N. & Razin, E. The function of lysyl-tRNA synthetase and Ap4A as signaling regulators of MITF activity in FcεRI-activated mast cells. Immunity 20, 145-151 (2004). (Pubitemid 38258391)
26. 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).
27. Ofir-Birin, Y. et al. Structural switch of lysyl-tRNA synthetases between translation and transcription. Mol. Cell 49, 30-42 (2013).
28. Blanquet, S., Plateau, P. & Brevet, A. The role of zinc in 5′,5′-diadenosine tetraphosphate production by aminoacyl-transfer RNA synthetases. Mol. Cell. Biochem. 52, 3-11 (1983). (Pubitemid 13065216)
29. Justin, N., De Marco, V., Aasland, R. & Gamblin, S.J. Reading, writing and editing methylated lysines on histone tails: new insights from recent structural studies. Curr. Opin. Struct. Biol. 20, 730-738 (2010).
30. Tzima, E. et al. VE-cadherin links tRNA synthetase cytokine to anti-angiogenic function. J. Biol. Chem. 280, 2405-2408 (2005). (Pubitemid 40189338)
31. Guo, M., Yang, X.L. & Schimmel, P. New functions of aminoacyl-tRNA synthetases beyond translation. Nat. Rev. Mol. Cell Biol. 11, 668-674 (2010).
32. Shiba, K. Intron positions delineate the evolutionary path of a pervasively appended peptide in five human aminoacyl-tRNA synthetases. J. Mol. Evol. 55, 727-733 (2002). (Pubitemid 35387405)
33. 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)
34. Sajish, M. et al. Trp-tRNA synthetase bridges DNA-PKcs to PARP-1 to link IFN-γ and p53 signaling. Nat. Chem. Biol. 8, 547-554 (2012).
35. Ray, P.S. et al. Evolution of function of a fused metazoan tRNA synthetase. Mol. Biol. Evol. 28, 437-447 (2011).
36. Cerini, C. et al. A component of the multisynthetase complex is a multifunctional aminoacyl-tRNA synthetase. EMBO J. 10, 4267-4277 (1991). (Pubitemid 21905459)
37. Arif, A., Jia, J., Moodt, R.A., DiCorleto, P.E. & Fox, P.L. Phosphorylation of glutamyl-prolyl tRNA synthetase by cyclin-dependent kinase 5 dictates transcript-selective translational control. Proc. Natl. Acad. Sci. USA 108, 1415-1420 (2011).
38. 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).
39. 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). (Pubitemid 351400920)
40. Herzog, W., Muller, K., Huisken, J. & Stainier, D.Y. Genetic evidence for a noncanonical function of seryl-tRNA synthetase in vascular development. Circ. Res. 104, 1260-1266 (2009).
41. Fukui, H., Hanaoka, R. & Kawahara, A. Noncanonical activity of seryl-tRNA synthetase is involved in vascular development. Circ. Res. 104, 1253-1259 (2009).
42. Xu, X. et al. Unique domain appended to vertebrate tRNA synthetase is essential for vascular development. Nat. Commun. 3, 681 (2012).
43. Francin, M., Kaminska, M., Kerjan, P. & Mirande, M. The N-terminal domain of mammalian lysyl-tRNA synthetase is a functional tRNA-binding domain. J. Biol. Chem. 277, 1762-1769 (2002). (Pubitemid 34968747)
44. Frugier, M., Moulinier, L. & Giegé, R. A domain in the N-terminal extension of class IIb eukaryotic aminoacyl-tRNA synthetases is important for tRNA binding. EMBO J. 19, 2371-2380 (2000). (Pubitemid 30259018)
45. Negrutskii, B.S., Shalak, V.F., Kerjan, P., El'skaya, A.V. & Mirande, M. Functional interaction of mammalian valyl-tRNA synthetase with elongation factor EF-1α in the complex with EF-1H. J. Biol. Chem. 274, 4545-4550 (1999).
46. He, R., Zu, L.D., Yao, P., Chen, X. & Wang, E.D. Two non-redundant fragments in the N-terminal peptide of human cytosolic methionyl-tRNA synthetase were indispensable for the multi-synthetase complex incorporation and enzyme activity. Biochim. Biophys. Acta 1794, 347-354 (2009).
47. Kerjan, P., Cerini, C., Semeriva, M. & Mirande, M. The multienzyme complex containing nine aminoacyl-tRNA synthetases is ubiquitous from Drosophila to mammals. Biochim. Biophys. Acta 1199, 293-297 (1994). (Pubitemid 24130905)
48. Lee, S.W., Cho, B.H., Park, S.G. & Kim, S. Aminoacyl-tRNA synthetase complexes: beyond translation. J. Cell Sci. 117, 3725-3734 (2004). (Pubitemid 39207312)
49. Robinson, J.C., Kerjan, P. & Mirande, M. Macromolecular assemblage of aminoacyl-tRNA synthetases: quantitative analysis of protein-protein interactions and mechanism of complex assembly. J. Mol. Biol. 304, 983-994 (2000). (Pubitemid 32047095)
50. Quevillon, S., Robinson, J.C., Berthonneau, E., Siatecka, M. & Mirande, M. Macromolecular assemblage of aminoacyl-tRNA synthetases: identification of protein-protein interactions and characterization of a core protein. J. Mol. Biol. 285, 183-195 (1999). (Pubitemid 29034036)
51. Han, J.M. et al. Hierarchical network between the components of the multi-tRNA synthetase complex: implications for complex formation. J. Biol. Chem. 281, 38663-38667 (2006).
52. 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). (Pubitemid 351282536)
53. Kang, T. et al. AIMP3/p18 controls translational initiation by mediating the delivery of charged initiator tRNA to initiation complex. J. Mol. Biol. 423, 475-481 (2012).
54. Park, S.G., Choi, E.C. & Kim, S. Aminoacyl-tRNA synthetase- interacting multifunctional proteins (AIMPs): a triad for cellular homeostasis. IUBMB Life 62, 296-302 (2010).
55. Zhu, X. et al. MSC p43 required for axonal development in motor neurons. Proc. Natl. Acad. Sci. USA 106, 15944-15949 (2009).
56. Park, S.G. et al. The novel cytokine p43 stimulates dermal fibroblast proliferation and wound repair. Am. J. Pathol. 166, 387-398 (2005).
57. Kim, J.Y. et al. p38 is essential for the assembly and stability of macromolecular tRNA synthetase complex: implications for its physiological significance. Proc. Natl. Acad. Sci. USA 99, 7912-7916 (2002). (Pubitemid 34650979)
58. Kim, M.J. et al. Downregulation of FUSE-binding protein and c-myc by tRNA synthetase cofactor p38 is required for lung cell differentiation. Nat. Genet. 34, 330-336 (2003). (Pubitemid 36792868)
59. Choi, J.W., Um, J.Y., Kundu, J.K., Surh, Y.J. & Kim, S. Multidirectional tumor-suppressive activity of AIMP2/p38 and the enhanced susceptibility of AIMP2 heterozygous mice to carcinogenesis. Carcinogenesis 30, 1638-1644 (2009).
60. Ko, H.S. et al. Accumulation of the authentic parkin substrate aminoacyl-tRNA synthetase cofactor, p38/JTV-1, leads to catecholaminergic cell death. J. Neurosci. 25, 7968-7978 (2005). (Pubitemid 41254399)
61. Kwon, N.H. et al. Dual role of methionyl-tRNA synthetase in the regulation of translation and tumor suppressor activity of aminoacyl-tRNA synthetase-interacting multifunctional protein-3. Proc. Natl. Acad. Sci. USA 108, 19635-19640 (2011).
62. Park, B.J. et al. The haploinsufficient tumor suppressor p18 upregulates p53 via interactions with ATM/ATR. Cell 120, 209-221 (2005).
63. Kim, K.J. et al. Determination of three-dimensional structure and residues of the novel tumor suppressor AIMP3/p18 required for the interaction with ATM. J. Biol. Chem. 283, 14032-14040 (2008).
64. Howard, O.M. et al. Histidyl-tRNA synthetase and asparaginyl-tRNA synthetase, autoantigens in myositis, activate chemokine receptors on T lymphocytes and immature dendritic cells. J. Exp. Med. 196, 781-791 (2002).
65. Yamasaki, Y. et al. Unusually high frequency of autoantibodies to PL-7 associated with milder muscle disease in Japanese patients with polymyositis/dermatomyositis. Arthritis Rheum. 54, 2004-2009 (2006). (Pubitemid 43877951)
66. Xu, Z. et al. Internally deleted human tRNA synthetase suggests evolutionary pressure for repurposing. Structure 20, 1470-1477 (2012).
67. Wu, P.C. et al. In vivo sensitivity of human melanoma to tumor necrosis factor (TNF)-α is determined by tumor production of the novel cytokine endothelial-monocyte activating polypeptide II (EMAPII). Cancer Res. 59, 205-212 (1999). (Pubitemid 29062979)
68. Shalak, V. et al. The EMAPII cytokine is released from the mammalian multisynthetase complex after cleavage of its p43/proEMAPII component. J. Biol. Chem. 276, 23769-23776 (2001).
69. Zhou, Q. et al. Orthogonal use of a human tRNA synthetase active site to achieve multifunctionality. Nat. Struct. Mol. Biol. 17, 57-61 (2010).
70. Banin, E. et al. T2-TrpRS inhibits preretinal neovascularization and enhances physiological vascular regrowth in OIR as assessed by a new method of quantification. Invest. Ophthalmol. Vis. Sci. 47, 2125-2134 (2006). (Pubitemid 46768297)
71. Tzima, E. et al. Biologically active fragment of a human tRNA synthetase inhibits fluid shear stress-activated responses of endothelial cells. Proc. Natl. Acad. Sci. USA 100, 14903-14907 (2003). (Pubitemid 37517989)
72. Yao, P. et al. Coding region polyadenylation generates a truncated tRNA synthetase that counters translation repression. Cell 149, 88-100 (2012).
73. Han, J.M. et al. AIMP2/p38, the scaffold for the multi-tRNA synthetase complex, responds to genotoxic stresses via p53. Proc. Natl. Acad. Sci. USA 105, 11206-11211 (2008).
74. Choi, J.W. et al. AIMP2 promotes TNFα-dependent apoptosis via ubiquitin-mediated degradation of TRAF2. J. Cell Sci. 122, 2710-2715 (2009).
75. Choi, J.W. et al. Splicing variant of AIMP2 as an effective target against chemoresistant ovarian cancer. J. Mol. Cell Biol. 4, 164-173 (2012).
76. Choi, J.W. et al. Cancer-associated splicing variant of tumor suppressor AIMP2/p38: pathological implication in tumorigenesis. PLoS Genet. 7, e1001351 (2011).
77. Lee, J.W. et al. Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443, 50-55 (2006). (Pubitemid 44344044)
78. Beebe, K., Ribas De Pouplana, L. & Schimmel, P. Elucidation of tRNA-dependent editing by a class II tRNA synthetase and significance for cell viability. EMBO J. 22, 668-675 (2003). (Pubitemid 36193611)
79. Antonellis, A. & Green, E.D. The role of aminoacyl-tRNA synthetases in genetic diseases. Annu. Rev. Genomics Hum. Genet. 9, 87-107 (2008).
80. Zhao, Z. et al. Alanyl-tRNA synthetase mutation in a family with dominant distal hereditary motor neuropathy. Neurology 78, 1644-1649 (2012).
81. Froelich, C.A. & First, E.A. Dominant intermediate Charcot-Marie-Tooth disorder is not due to a catalytic defect in tyrosyl-tRNA synthetase. Biochemistry. 50, 7132-7145 (2011).
82. Xie, W., Nangle, L.A., Zhang, W., Schimmel, P. & Yang, X.L. Long-range structural effects of a Charcot-Marie-Tooth disease-causing mutation in human glycyl-tRNA synthetase. Proc. Natl. Acad. Sci. USA 104, 9976-9981 (2007). (Pubitemid 47175248)
83. 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). (Pubitemid 44374911)
84. Stum, M. et al. An assessment of mechanisms underlying peripheral axonal degeneration caused by aminoacyl-tRNA synthetase mutations. Mol. Cell. Neurosci. 46, 432-443 (2011).
85. He, W. et al. Dispersed disease-causing neomorphic mutations on a single protein promote the same localized conformational opening. Proc. Natl. Acad. Sci. USA 108, 12307-12312 (2011).
86. van de Vijver, M.J. et al. A gene-expression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347, 1999-2009 (2002). (Pubitemid 35461656)
87. Paik, S. et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351, 2817-2826 (2004). (Pubitemid 40051905)
88. Paley, E.L., Paley, D.E., Merkulova-Rainon, T. & Subbarayan, P.R. Hypoxia signature of splice forms of tryptophanyl-tRNA synthetase marks pancreatic cancer cells with distinct metastatic abilities. Pancreas 40, 1043-1056 (2011).
89. Ghanipour, A. et al. The prognostic significance of tryptophanyl-tRNA synthetase in colorectal cancer. Cancer Epidemiol. Biomarkers Prev. 18, 2949-2956 (2009).
90. Mun, J. et al. A proteomic approach based on multiple parallel separation for the unambiguous identification of an antibody cognate antigen. Electrophoresis 31, 3428-3436 (2010).
91. Kron, M.A., Petridis, M., Haertlein, M., Libranda-Ramirez, B. & Scaffidi, L.E. Do tissue levels of autoantigenic aminoacyl-tRNA synthetase predict clinical disease? Med. Hypotheses 65, 1124-1127 (2005). (Pubitemid 41425899)
92. Levine, S.M., Rosen, A. & Casciola-Rosen, L.A. Anti-aminoacyl tRNA synthetase immune responses: insights into the pathogenesis of the idiopathic inflammatory myopathies. Curr. Opin. Rheumatol. 15, 708-713 (2003). (Pubitemid 38156296)
93. Park, S.G. et al. Autoantibodies against aminoacyl-tRNA synthetase: novel diagnostic marker for type 1 diabetes mellitus. Biomarkers 15, 358-366 (2010).
94. Mörbt, N. et al. Chlorinated benzenes cause concomitantly oxidative stress and induction of apoptotic markers in lung epithelial cells (A549) at nonacute toxic concentrations. J. Proteome Res. 10, 363-378 (2011).
95. Kim, S.S., Hur, S.Y., Kim, Y.R., Yoo, N.J. & Lee, S.H. Expression of AIMP1, 2 and 3, the scaffolds for the multi-tRNA synthetase complex, is downregulated in gastric and colorectal cancer. Tumori. 97, 380-385 (2011).
96. Yao, C. et al. P43/pro-EMAPII: a potential biomarker for discriminating traumatic versus ischemic brain injury. J. Neurotrauma 26, 1295-1305 (2009).
97. Park, M.C. et al. Secreted human glycyl-tRNA synthetase implicated in defense against ERK-activated tumorigenesis. Proc. Natl. Acad. Sci. USA 109, E640-E647 (2012).
98. Schwarz, R.E. et al. Antitumor effects of EMAP II against pancreatic cancer through inhibition of fibronectin-dependent proliferation. Cancer Biol. Ther. 9, 632-639 (2010).
99. Han, J.M., Park, S.G., Lee, Y. & Kim, S. Structural separation of different extracellular activities in aminoacyl-tRNA synthetase-interacting multi-functional protein, p43/AIMP1. Biochem. Biophys. Res. Commun. 342, 113-118 (2006). (Pubitemid 43247367)
100. Han, J.M. et al. Identification of gp96 as a novel target for treatment of autoimmune disease in mice. PLoS ONE 5, e9792 (2010).