SAG/RBX2 is a novel substrate of NEDD4-1 E3 ubiquitin ligase and mediates NEDD4-1 induced chemosensitization

Oncotarget

Volumn 5, Issue 16, 2014, Pages 6746-6755

  Zhou, Weihua ^a   Xu, Jie ^a   Zhao, Yongchao ^a   Sun, Yi ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

E3 ubiquitin ligase; NEDD4 1 E3 ligase; Protein ubiquitylation and degradation; SAG E3 ligase

Indexed keywords

CUL 5 PROTEIN; ETOPOSIDE; LIGASE; SENSITIVE TO APOPTOSIS GENE PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CUL5 PROTEIN, HUMAN; CULLIN; ESCRT PROTEIN; NEDD4 UBIQUITIN PROTEIN LIGASES; RNF7 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; CHEMOSENSITIZATION; CONTROLLED STUDY; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; HUMAN; HUMAN CELL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RING FINGER MOTIF; UBIQUITINATION; BIOSYNTHESIS; DRUG EFFECTS; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CULLIN PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ETOPOSIDE; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; PROTEIN STRUCTURE, TERTIARY; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84907081645     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2246     Document Type: Article

References (42)

1. Dye BT, Schulman BA. Structural mechanisms underlying posttranslational modification by ubiquitin-like proteins. Annual review of biophysics and biomolecular structure. 2007; 36:131-150.
2. Rotin D, Kumar S. Physiological functions of the HECT family of ubiquitin ligases. Nature reviews. 2009; 10(6):398-409.
3. Hershko A, Ciechanover A. The ubiquitin system. Annual review of biochemistry. 1998; 67:425-479.
4. Lipkowitz S, Weissman AM. RINGs of good and evil: RING finger ubiquitin ligases at the crossroads of tumour suppression and oncogenesis. Nature reviews. 2011; 11(9):629-643.
5. Duan H, Wang Y, Aviram M, Swaroop M, Loo JA, Bian J, Tian Y, Mueller T, Bisgaier CL, Sun Y. SAG, a novel zinc RING finger protein that protects cells from apoptosis induced by redox agents. Molecular and cellular biology. 1999; 19(4):3145-3155.
6. Zhou W, Wei W, Sun Y. Genetically engineered mouse models for functional studies of SKP1-CUL1-F-box-protein (SCF) E3 ubiquitin ligases. Cell research. 2013; 23(5):599-619.
7. Sun Y, Tan M, Duan H, Swaroop M. SAG/ROC/Rbx/Hrt, a zinc RING finger gene family: molecular cloning, biochemical properties, and biological functions. Antioxidants & redox signaling. 2001; 3(4):635-650.
8. Chen A, Wu K, Fuchs SY, Tan P, Gomez C, Pan ZQ. The conserved RING-H2 finger of ROC1 is required for ubiquitin ligation. The Journal of biological chemistry. 2000; 275(20):15432-15439.
9. Gu Q, Bowden GT, Normolle D, Sun Y. SAG/ROC2 E3 ligase regulates skin carcinogenesis by stage-dependent targeting of c-Jun/AP1 and IkappaB-alpha/NF-kappaB. The Journal of cell biology. 2007; 178(6):1009-1023.
10. He H, Gu Q, Zheng M, Normolle D, Sun Y. SAG/ROC2/RBX2 E3 ligase promotes UVB-induced skin hyperplasia, but not skin tumors, by simultaneously targeting c-Jun/AP-1 and p27. Carcinogenesis. 2008; 29(4):858-865.
11. Jia L, Yang J, Hao X, Zheng M, He H, Xiong X, Xu L, Sun Y. Validation of SAG/RBX2/ROC2 E3 ubiquitin ligase as an anticancer and radiosensitizing target. Clin Cancer Res. 2010; 16(3):814-824.
12. Tan M, Zhu Y, Kovacev J, Zhao Y, Pan ZQ, Spitz DR, Sun Y. Disruption of Sag/Rbx2/Roc2 induces radiosensitization by increasing ROS levels and blocking NF-kappaB activation in mouse embryonic stem cells. Free radical biology & medicine. 2010; 49(6):976-983.
13. Li H, Tan M, Jia L, Wei D, Zhao Y, Chen G, Xu J, Zhao L, Thomas D, Beer DG, Sun Y. Inactivation of SAG/RBX2 E3 ubiquitin ligase suppresses KrasG12D-driven lung tumorigenesis. The Journal of clinical investigation. 2014; 124(2):835-846.
14. Gu Q, Tan M, Sun Y. SAG/ROC2/Rbx2 is a novel activator protein-1 target that promotes c-Jun degradation and inhibits 12-O-tetradecanoylphorbol-13-acetate-induced neoplastic transformation. Cancer research. 2007; 67(8):3616-3625.
15. Tan M, Gu Q, He H, Pamarthy D, Semenza GL, Sun Y. SAG/ROC2/RBX2 is a HIF-1 target gene that promotes HIF-1 alpha ubiquitination and degradation. Oncogene. 2008; 27(10):1404-1411.
16. Yang B, Kumar S. Nedd4 and Nedd4-2: closely related ubiquitin-protein ligases with distinct physiological functions. Cell death and differentiation. 2010; 17(1):68-77.
17. Wang X, Trotman LC, Koppie T, Alimonti A, Chen Z, Gao Z, Wang J, Erdjument-Bromage H, Tempst P, Cordon-Cardo C, Pandolfi PP, Jiang X. NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell, 2007; 128(1):129-139.
18. Trotman LC, Wang X, Alimonti A, Chen Z, Teruya-Feldstein J, Yang H, Pavletich NP, Carver BS, Cordon-Cardo C, Erdjument-Bromage H, Tempst P, Chi SG, Kim HJ, et al. Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell. 2007; 128(1):141-156.
19. Cao XR, Lill NL, Boase N, Shi PP, Croucher DR, Shan H, Qu J, Sweezer EM, Place T, Kirby PA, Daly RJ, Kumar S, Yang B. Nedd4 controls animal growth by regulating IGF-1 signaling. Science signaling. 2008; 1(38):ra5.
20. Fouladkou F, Landry T, Kawabe H, Neeb A, Lu C, Brose N, Stambolic V, Rotin D. The ubiquitin ligase Nedd4-1 is dispensable for the regulation of PTEN stability and localization. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(25):8585-8590.
21. Vecchione A, Marchese A, Henry P, Rotin D, Morrione A. The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Molecular and cellular biology. 2003; 23(9):3363-3372.
22. Monami G, Emiliozzi V, Morrione A. Grb10/Nedd4-mediated multiubiquitination of the insulin-like growth factor receptor regulates receptor internalization. Journal of cellular physiology. 2008; 216(2):426-437.
23. Persaud A, Alberts P, Hayes M, Guettler S, Clarke I, Sicheri F, Dirks P, Ciruna B, Rotin D. Nedd4-1 binds and ubiquitylates activated FGFR1 to control its endocytosis and function. The EMBO journal. 2011; 30(16):3259-3273.
24. Fan CD, Lum MA, Xu C, Black JD, Wang X. Ubiquitin-dependent regulation of phospho-AKT dynamics by the ubiquitin E3 ligase, NEDD4-1, in the insulin-like growth factor-1 response. The Journal of biological chemistry. 2013; 288(3):1674-1684.
25. Magnifico A, Ettenberg S, Yang C, Mariano J, Tiwari S, Fang S, Lipkowitz S, Weissman AM. WW domain HECT E3s target Cbl RING finger E3s for proteasomal degradation. The Journal of biological chemistry. 2003; 278(44):43169-43177.
26. Chen C, Matesic LE. The Nedd4-like family of E3 ubiquitin ligases and cancer. Cancer metastasis reviews. 2007; 26(3-4):587-604.
27. Persaud A, Alberts P, Amsen EM, Xiong X, Wasmuth J, Saadon Z, Fladd C, Parkinson J, Rotin D. Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrays. Molecular systems biology. 2009; 5:333.
28. Kumar S, Harvey KF, Kinoshita M, Copeland NG, Noda M, Jenkins NA. cDNA cloning, expression analysis, and mapping of the mouse Nedd4 gene. Genomics. 1997; 40(3):435-443.
29. Lu PJ, Zhou XZ, Shen M, Lu KP. Function of WW domains as phosphoserine-or phosphothreonine-binding modules. Science. 1999; 283(5406):1325-1328.
30. Kamura T, Maenaka K, Kotoshiba S, Matsumoto M, Kohda D, Conaway RC, Conaway JW, Nakayama KI. VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes & development. 2004; 18(24):3055-3065.
31. Huang DT, Ayrault O, Hunt HW, Taherbhoy AM, Duda DM, Scott DC, Borg LA, Neale G, Murray PJ, Roussel MF, Schulman BA. E2-RING expansion of the NEDD8 cascade confers specificity to cullin modification. Molecular cell. 2009; 33(4):483-495.
32. Reynolds PJ, Simms JR, Duronio RJ. Identifying determinants of cullin binding specificity among the three functionally different Drosophila melanogaster Roc proteins via domain swapping. PloS one. 2008; 3(8):e2918.
33. Sun Y, Li H. Functional characterization of SAG/RBX2/ROC2/RNF7, an antioxidant protein and an E3 ubiquitin ligase. Protein & cell. 2013; 4(2):103-116.
34. Wang X, Shi Y, Wang J, Huang G, Jiang X. Crucial role of the C-terminus of PTEN in antagonizing NEDD4-1-mediated PTEN ubiquitination and degradation. The Biochemical journal. 2008; 414(2):221-229.
35. Lee JR, Oestreich AJ, Payne JA, Gunawan MS, Norgan AP, Katzmann DJ. The HECT domain of the ubiquitin ligase Rsp5 contributes to substrate recognition. The Journal of biological chemistry. 2009; 284(46):32126-32137.
36. Swaroop M, Wang Y, Miller P, Duan H, Jatkoe T, Madore SJ, Sun Y. Yeast homolog of human SAG/ROC2/Rbx2/Hrt2 is essential for cell growth, but not for germination: chip profiling implicates its role in cell cycle regulation. Oncogene. 2000; 19(24):2855-2866.
37. Ohta T, Michel JJ, Xiong Y. Association with cullin partners protects ROC proteins from proteasome-dependent degradation. Oncogene. 1999;18(48):6758-6766.
38. Tan M, Gallegos JR, Gu Q, Huang Y, Li J, Jin Y, Lu H, Sun Y. SAG/ROC-SCF beta-TrCP E3 ubiquitin ligase promotes pro-caspase-3 degradation as a mechanism of apoptosis protection. Neoplasia. 2006; 8(12):1042-1054.
39. Zhao Y, Morgan MA, Sun Y. Targeting Neddylation Pathways to Inactivate Cullin-RING Ligases for Anticancer Therapy. Antioxidants & redox signaling. 2014.
40. Simonin A, Fuster D. Nedd4-1 and beta-arrestin-1 are key regulators of Na+/H+ exchanger 1 ubiquitylation, endocytosis, and function. The Journal of biological chemistry. 2010; 285(49):38293-38303.
41. Lin Q, Wang J, Childress C, Sudol M, Carey DJ, Yang W. HECT E3 ubiquitin ligase Nedd4-1 ubiquitinates ACK and regulates epidermal growth factor (EGF)-induced degradation of EGF receptor and ACK. Molecular and cellular biology. 2010; 30(6):1541-1554.
42. Tan M, Davis SW, Saunders TL, Zhu Y, Sun Y. RBX1/ROC1 disruption results in early embryonic lethality due to proliferation failure, partially rescued by simultaneous loss of p27. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106(15):6203-6208.