Neddylation requires glycyl-tRNA synthetase to protect activated E2

Nature Structural and Molecular Biology

Volumn 23, Issue 8, 2016, Pages 730-737

  Mo, Zhongying ^a   Zhang, Qian ^a   Liu, Ze ^a   Lauer, Janelle ^b   Shi, Yi ^a   Sun, Litao ^a   Griffin, Patrick R ^b   Yang, Xiang Lei ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE TRANSFER RNA LIGASE; GLYCOPROTEIN E1; GLYCOPROTEIN E2; NEDD8 PROTEIN; NEDD8 PROTEIN, HUMAN; PROTEIN BINDING; UBA3 PROTEIN, HUMAN; UBE2M PROTEIN, HUMAN; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; FEMALE; GENE SILENCING; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; NEDDYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; BREAST TUMOR; CELL CYCLE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; KAPLAN MEIER METHOD; KINETICS; METABOLISM; MORTALITY; PHYSIOLOGY; PROPORTIONAL HAZARDS MODEL; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN STABILITY;

BREAST NEOPLASMS; CATALYTIC DOMAIN; CELL CYCLE; GLYCINE-TRNA LIGASE; HEK293 CELLS; HELA CELLS; HUMANS; KAPLAN-MEIER ESTIMATE; KINETICS; PROPORTIONAL HAZARDS MODELS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEOLYSIS; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINS;

EID: 84976285887     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3250     Document Type: Article

References (58)

1. Kamitani, T., Kito, K., Nguyen, H.P. & Yeh, E.T. Characterization of NEDD8, a developmentally down-regulated ubiquitin-like protein. J. Biol. Chem. 272, 28557-28562 (1997).
2. Osaka, F. et al. Covalent modifier NEDD8 is essential for SCF ubiquitin-ligase in fission yeast. EMBO J. 19, 3475-3484 (2000).
3. Tateishi, K., Omata, M., Tanaka, K. & Chiba, T. The NEDD8 system is essential for cell cycle progression and morphogenetic pathway in mice. J. Cell Biol. 155, 571-579 (2001).
4. Kerscher, O., Felberbaum, R. & Hochstrasser, M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159-180 (2006).
5. Liakopoulos, D., Doenges, G., Matuschewski, K. & Jentsch, S. A novel protein modification pathway related to the ubiquitin system. EMBO J. 17, 2208-2214 (1998).
6. Osaka, F. et al. A new NEDD8-ligating system for cullin-4A. Genes Dev. 12, 2263-2268 (1998).
7. Furukawa, M., Zhang, Y., McCarville, J., Ohta, T. & Xiong, Y. The CUL1 C-terminal sequence and ROC1 are required for efficient nuclear accumulation, NEDD8 modification, and ubiquitin ligase activity of CUL1. Mol. Cell. Biol. 20, 8185-8197 (2000).
8. Huang, D.T. et al. E2-RING expansion of the NEDD8 cascade confers specificity to cullin modification. Mol. Cell 33, 483-495 (2009).
9. Enchev, R.I., Schulman, B.A. & Peter, M. Protein neddylation: beyond cullin-RING ligases. Nat. Rev. Mol. Cell Biol. 16, 30-44 (2015).
10. Soucy, T.A., Dick, L.R., Smith, P.G., Milhollen, M.A. & Brownell, J.E. The NEDD8 conjugation pathway and its relevance in cancer biology and therapy. Genes Cancer 1, 708-716 (2010).
11. Welchman, R.L., Gordon, C. & Mayer, R.J. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol. 6, 599-609 (2005).
12. Vijay-Kumar, S., Bugg, C.E. & Cook, W.J. Structure of ubiquitin refined at 1.8 A resolution. J. Mol. Biol. 194, 531-544 (1987).
13. Bublitz, C. The properties of a glycyl-soluble-RNA synthetase from chick embryo. Biochim. Biophys. Acta 113, 158-166 (1966).
14. Zhou, Q. et al. Orthogonal use of a human tRNA synthetase active site to achieve multifunctionality. Nat. Struct. Mol. Biol. 17, 57-61 (2010).
15. Huang, D.T. et al. A unique E1-E2 interaction required for optimal conjugation of the ubiquitin-like protein NEDD8. Nat. Struct. Mol. Biol. 11, 927-935 (2004).
16. Eletr, Z.M., Huang, D.T., Duda, D.M., Schulman, B.A. & Kuhlman, B. E2 conjugating enzymes must disengage from their E1 enzymes before E3-dependent ubiquitin and ubiquitin-like transfer. Nat. Struct. Mol. Biol. 12, 933-934 (2005).
17. 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).
18. Scott, D.C. et al. Structure of a RING E3 trapped in action reveals ligation mechanism for the ubiquitin-like protein NEDD8. Cell 157, 1671-1684 (2014).
19. Duhovny, D., Nussinov, R. & Wolfson, H.J. Efficient unbound docking of rigid molecules. Algorithms Bioinform 2452, 185-200 (2002).
20. Schneidman-Duhovny, D., Inbar, Y., Nussinov, R. & Wolfson, H.J. PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res. 33, W363-W367 (2005).
21. Guo, R.T., Chong, Y.E., Guo, M. & Yang, X.L. Crystal structures and biochemical analyses suggest a unique mechanism and role for human glycyl-tRNA synthetase in Ap4A homeostasis. J. Biol. Chem. 284, 28968-28976 (2009).
22. Pagano, M. et al. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269, 682-685 (1995).
23. Toyoshima, H. & Hunter, T. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell 78, 67-74 (1994).
24. Soucy, T.A. et al. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458, 732-736 (2009).
25. Hengst, L. & Reed, S.I. Translational control of p27Kip1 accumulation during the cell cycle. Science 271, 1861-1864 (1996).
26. Petroski, M.D. & Deshaies, R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6, 9-20 (2005).
27. Cardozo, T. & Pagano, M. The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5, 739-751 (2004).
28. Stanley, D.J. et al. Inhibition of a NEDD8 cascade restores restriction of HIV by APOBEC3G. PLoS Pathog. 8, e1003085 (2012).
29. Mazauric, M.H. et al. 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 (1998).
30. Dil Kuazi, A. et al. NEDD8 protein is involved in ubiquitinated inclusion bodies. J. Pathol. 199, 259-266 (2003).
31. Mori, F. et al. Accumulation of NEDD8 in neuronal and glial inclusions of neurodegenerative disorders. Neuropathol. Appl. Neurobiol. 31, 53-61 (2005).
32. 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).
33. Yao, P. & Fox, P.L. Aminoacyl-tRNA synthetases in medicine and disease. EMBO Mol. Med. 5, 332-343 (2013).
34. Dubourg, O. et al. The G526R glycyl-tRNA synthetase gene mutation in distal hereditary motor neuropathy type V. Neurology 66, 1721-1726 (2006).
35. Motley, W.W. et al. Charcot-Marie-Tooth-linked mutant GARS is toxic to peripheral neurons independent of wild-type GARS levels. PLoS Genet. 7, e1002399 (2011).
36. He, W. et al. CMT2D neuropathy is linked to the neomorphic binding activity of glycyl-tRNA synthetase. Nature 526, 710-714 (2015).
37. 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).
38. Chairatvit, K. & Ngamkitidechakul, C. Control of cell proliferation via elevated NEDD8 conjugation in oral squamous cell carcinoma. Mol. Cell. Biochem. 306, 163-169 (2007).
39. Salon, C. et al. Altered pattern of Cul-1 protein expression and neddylation in human lung tumours: relationships with CAND1 and cyclin E protein levels. J. Pathol. 213, 303-310 (2007).
40. Podust, V.N. et al. A Nedd8 conjugation pathway is essential for proteolytic targeting of p27Kip1 by ubiquitination. Proc. Natl. Acad. Sci. USA 97, 4579-4584 (2000).
41. Nakayama, K.I. & Nakayama, K. Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev. Cancer 6, 369-381 (2006).
42. Kobayashi, A. et al. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24, 7130-7139 (2004).
43. Kamura, T. et al. Activation of HIF1α ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc. Natl. Acad. Sci. USA 97, 10430-10435 (2000).
44. Winston, J.T. et al. The SCFβ-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IκBα and β-catenin and stimulates IκBα ubiquitination in vitro. Genes Dev. 13, 270-283 (1999).
45. Nishitani, H. et al. Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J. 25, 1126-1136 (2006).
46. Sarantopoulos, J. et al. Phase I study of the investigational NEDD8-activating enzyme inhibitor pevonedistat (TAK-924/MLN4924) in patients with advanced solid tumors. Clin. Cancer Res. 22, 847-857 (2016).
47. Swords, R.T. et al. Pevonedistat (MLN4924), a first-in-class NEDD8-activating enzyme inhibitor, in patients with acute myeloid leukaemia and myelodysplastic syndromes: a phase 1 study. Br. J. Haematol. 169, 534-543 (2015).
48. Györffy, B. et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res. Treat. 123, 725-731 (2010).
49. Williams, T.F., Mirando, A.C., Wilkinson, B., Francklyn, C.S. & Lounsbury, K.M. Secreted threonyl-tRNA synthetase stimulates endothelial cell migration and angiogenesis. Sci. Rep. 3, 1317 (2013).
50. Kim, D.G. et al. Interaction of two translational components, lysyl-tRNA synthetase and p40/37LRP, in plasma membrane promotes laminin-dependent cell migration. FASEB J. 26, 4142-4159 (2012).
51. Kim, D.G. et al. Chemical inhibition of prometastatic lysyl-tRNA synthetase-laminin receptor interaction. Nat. Chem. Biol. 10, 29-34 (2014).
52. Huang, D.T. & Schulman, B.A. Expression, purification, and characterization of the E1 for human NEDD8, the heterodimeric APPBP1-UBA3 complex. Methods Enzymol. 398, 9-20 (2005).
53. 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).
54. 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).
55. Xu, X. et al. Unique domain appended to vertebrate tRNA synthetase is essential for vascular development. Nat. Commun. 3, 681 (2012).
56. Jin, J., Li, X., Gygi, S.P. & Harper, J.W. Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 447, 1135-1138 (2007).
57. Chalmers, M.J. et al. Probing protein ligand interactions by automated hydrogen/deuterium exchange mass spectrometry. Anal. Chem. 78, 1005-1014 (2006).
58. Pascal, B.D. et al. HDX workbench: software for the analysis of H/D exchange MS data. J. Am. Soc. Mass Spectrom. 23, 1512-1521 (2012).