Monoubiquitination is critical for ovarian tumor domain-containing ubiquitin aldehyde binding protein 1 (Otub1) to suppress UbcH5 enzyme and Stabilize p53 protein

Journal of Biological Chemistry

Volumn 289, Issue 8, 2014, Pages 5097-5108

  Li, Yuhuang ^a   Sun, Xiao Xin ^a   Elferich, Johannes ^b   Shinde, Ujwal ^b   David, Larry L ^a   Dai, Mu Shui ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

BINDING PROTEINS; MOLECULAR MECHANISM; OVARIAN TUMOR; P53 PROTEIN; UBIQUITIN;

PROTEINS;

LYSINE; MUTANT PROTEIN; OVARIAN TUMOR DOMAIN CONTAINING UBIQUITIN ALDEHYDE BINDING PROTEIN 1; PROTEIN MDM2; PROTEIN P53; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN CONJUGATING ENZYME H5; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONJUGATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVE SITE; ENZYME REPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MONOUBIQUITINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UBIQUITINATION;

DEUBIQUITINATING ENZYMES; DEUBIQUITINATION; MONOUBIQUITINATION; OTUB1; P53; UBCH5; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYME (UBC); UBIQUITINATION;

AMINO ACID SEQUENCE; CELL LINE, TUMOR; CYSTEINE ENDOPEPTIDASES; DNA DAMAGE; FEMALE; HUMANS; LYSINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OVARIAN NEOPLASMS; PROTEIN BINDING; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION;

EID: 84894462315     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.533109     Document Type: Article

References (42)

1. Devine, T., and Dai, M. S. (2013) Targeting the ubiquitin-mediated proteasome degradation of p53 for cancer therapy. Curr. Pharm. Des. 19, 3248-3262
2. Kruse, J. P., and Gu, W. (2009) Modes of p53 regulation. Cell 137, 609-622
3. Fang, S., Jensen, J. P., Ludwig, R. L., Vousden, K. H., and Weissman, A. M. (2000) Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J. Biol. Chem. 275, 8945-8951
4. Momand, J., Zambetti, G. P., Olson, D. C., George, D., and Levine, A. J. (1992) The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69, 1237-1245
5. Haupt, Y., Maya, R., Kazaz, A., and Oren, M. (1997) Mdm2 promotes the rapid degradation of p53. Nature 387, 296-299
6. Honda, R., Tanaka, H., and Yasuda, H. (1997) Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420, 25-27
7. Kubbutat, M. H., Jones, S. N., and Vousden, K. H. (1997) Regulation of p53 stability by Mdm2. Nature 387, 299-303
8. Vogelstein, B., Lane, D., and Levine, A. J. (2000) Surfing the p53 network. Nature 408, 307-310
9. Zhang, Y., and Lu, H. (2009) Signaling to p53. Ribosomal proteins find their way. Cancer Cell 16, 369-377
10. Nijman, S. M., Luna-Vargas, M. P., Velds, A., Brummelkamp, T. R., Dirac, A. M., Sixma, T. K., and Bernards, R. (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786
11. Li, M., Chen, D., Shiloh, A., Luo, J., Nikolaev, A. Y., Qin, J., and Gu, W. (2002) Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 416, 648-653
12. Meulmeester, E., Maurice, M. M., Boutell, C., Teunisse, A. F., Ovaa, H., Abraham, T. E., Dirks, R. W., and Jochemsen, A. G. (2005) Loss of HAUSP-mediated deubiquitination contributes toDNAdamage-induced destabilization of Hdmx and Hdm2. Mol. Cell 18, 565-576
13. Cummins, J. M., Rago, C., Kohli, M., Kinzler, K. W., Lengauer, C., and Vogelstein, B. (2004) Tumour suppression. Disruption of HAUSP gene stabilizes p53. Nature 428, 1 p following 486
14. Li, M., Brooks, C. L., Kon, N., and Gu, W. (2004)Adynamic role ofHAUSP in the p53-Mdm2 pathway. Mol. Cell 13, 879-886
15. Yuan, J., Luo, K., Zhang, L., Cheville, J. C., and Lou, Z. (2010) USP10 regulates p53 localization and stability by deubiquitinating p53. Cell 140, 384-396
16. Liu, J., Chung, H. J., Vogt, M., Jin, Y., Malide, D., He, L., Dundr, M., and Levens, D. (2011) JTV1 co-activates FBP to induce USP29 transcription and stabilize p53 in response to oxidative stress. EMBO J. 30, 846-858
17. Hock, A. K., Vigneron, A. M., Carter, S., Ludwig, R. L., and Vousden, K. H. (2011) Regulation of p53 stability and function by the deubiquitinating enzyme USP42. EMBO J. 30, 4921-4930
18. Allende-Vega, N., Sparks, A., Lane, D. P., and Saville, M. K. (2010) MdmX is a substrate for the deubiquitinating enzyme USP2a. Oncogene 29, 432-441
19. Stevenson, L. F., Sparks, A., Allende-Vega, N., Xirodimas, D. P., Lane, D. P., and Saville, M. K. (2007) The deubiquitinating enzyme USP2a regulates the p53 pathway by targeting Mdm2. EMBO J. 26, 976-986
20. Zhang, X., Berger, F. G., Yang, J., and Lu, X. (2011) USP4 inhibits p53 through deubiquitinating and stabilizing ARF-BP1. EMBO J. 30, 2177-2189
21. Sun, X. X., Challagundla, K. B., and Dai, M. S. (2012) Positive regulation of p53 stability and activity by the deubiquitinating enzyme Otubain 1. EMBO J. 31, 576-592
22. Nakada, S., Tai, I., Panier, S., Al-Hakim, A., Iemura, S., Juang, Y. C., O'Donnell, L., Kumakubo, A., Munro, M., Sicheri, F., Gingras, A. C., Natsume, T., Suda, T., and Durocher, D. (2010) Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466, 941-946
23. Zulkifle, N. (2013) Systematic yeast two-hybrid analysis of human E2 ubiquitin-conjugating enzyme and deubiquitin (DUB) protein interaction. Int. J. Biol. Chem. 7, 1-14
24. Juang, Y. C., Landry, M. C., Sanches, M., Vittal, V., Leung, C. C., Ceccarelli, D. F., Mateo, A. R., Pruneda, J. N., Mao, D. Y., Szilard, R. K., Orlicky, S., Munro, M., Brzovic, P. S., Klevit, R. E., Sicheri, F., and Durocher, D. (2012) OTUB1 co-opts Lys48-linked ubiquitin recognition to suppress E2 enzyme function. Mol. Cell 45, 384-397
25. Wiener, R., Zhang, X., Wang, T., and Wolberger, C. (2012) The mechanism of OTUB1-mediated inhibition of ubiquitination. Nature 483, 618-622
26. Sun, X. X., DeVine, T., Challagundla, K. B., and Dai, M. S. (2011) Interplay between ribosomal protein S27a and MDM2 protein in p53 activation in response to ribosomal stress. J. Biol. Chem. 286, 22730-22741
27. Dai, M. S., Zeng, S. X., Jin, Y., Sun, X. X., David, L., and Lu, H. (2004) Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition. Mol. Cell Biol. 24, 7654-7668
28. Yan, F. F., Pratt, E. B., Chen, P. C., Wang, F., Skach, W. R., David, L. L., and Shyng, S. L. (2010) Role of Hsp90 in biogenesis of thecell ATP-sensitive potassium channel complex. Mol. Biol. Cell 21, 1945-1954
29. Wilmarth, P. A., Riviere, M. A., and David, L. L. (2009) Techniques for accurate protein identification in shotgun proteomic studies of human, mouse, bovine, and chicken lenses. J. Ocul. Biol. Dis. Infor. 2, 223-234
30. Baker, R., Lewis, S. M., Sasaki, A. T., Wilkerson, E. M., Locasale, J. W., Cantley, L. C., Kuhlman, B., Dohlman, H. G., and Campbell, S. L. (2013) Site-specific monoubiquitination activates Ras by impeding GTPase-activating protein function. Nat. Struct. Mol. Biol. 20, 46-52
31. Denuc, A., Bosch-Comas, A., Gonzàlez-Duarte, R., and Marfany, G. (2009) The UBA-UIM domains of the USP25 regulate the enzyme ubiquitination state and modulate substrate recognition. PLoS ONE 4, e5571
32. Dimova, N. V., Hathaway, N. A., Lee, B. H., Kirkpatrick, D. S., Berkowitz, M. L., Gygi, S. P., Finley, D., and King, R. W. (2012) APC/C-mediated multiple monoubiquitylation provides an alternative degradation signal for cyclin B1. Nat. Cell Biol. 14, 168-176
33. Ju, D., and Xie, Y. (2006) Identification of the preferential ubiquitination site and ubiquitin-dependent degradation signal of Rpn4. J. Biol. Chem. 281, 10657-10662
34. Sakata, E., Satoh, T., Yamamoto, S., Yamaguchi, Y., Yagi-Utsumi, M., Kurimoto, E., Tanaka, K., Wakatsuki, S., and Kato, K. (2010) Crystal structure of UbcH5bubiquitin intermediate. Insight into the formation of the selfassembled E2Ub conjugates. Structure 18, 138-147
35. Brzovic, P. S., Lissounov, A., Christensen, D. E., Hoyt, D. W., and Klevit, R. E. (2006) A UbcH5/ubiquitin noncovalent complex is required for processive BRCA1-directed ubiquitination. Mol. Cell 21, 873-880
36. Saha, A., Lewis, S., Kleiger, G., Kuhlman, B., and Deshaies, R. J. (2011) Essential role for ubiquitin-ubiquitin-conjugating enzyme interaction in ubiquitin discharge from Cdc34 to substrate. Mol. Cell 42, 75-83
37. Herhaus, L., Al-Salihi, M., Macartney, T., Weidlich, S., and Sapkota, G. P. (2013) OTUB1 enhances TGF signalling by inhibiting the ubiquitylation and degradation of active SMAD2/3. Nat. Commun. 4, 2519
38. Soares, L., Seroogy, C., Skrenta, H., Anandasabapathy, N., Lovelace, P., Chung, C. D., Engleman, E., and Fathman, C. G. (2004) Two isoforms of otubain 1 regulate T cell anergy via GRAIL. Nat Immunol. 5, 45-54
39. Goncharov, T., Niessen, K., de Almagro, M. C., Izrael-Tomasevic, A., Fedorova, A. V., Varfolomeev, E., Arnott, D., Deshayes, K., Kirkpatrick, D. S., and Vucic, D. (2013) OTUB1 modulates c-IAP1 stability to regulate signalling pathways. EMBO J. 32, 1103-1114
40. Stanisi, V., Malovannaya, A., Qin, J., Lonard, D. M., and O'Malley, B. W. (2009) OTU Domain-containing ubiquitin aldehyde-binding protein 1 (OTUB1) deubiquitinates estrogen receptor (ER) and affects ER transcriptional activity. J. Biol. Chem. 284, 16135-16145
41. Li, S., Zheng, H., Mao, A. P., Zhong, B., Li, Y., Liu, Y., Gao, Y., Ran, Y., Tien, P., and Shu, H. B. (2010) Regulation of virus-triggered signaling by OTUB1-and OTUB2-mediated deubiquitination of TRAF3 and TRAF6. J. Biol. Chem. 285, 4291-4297
42. Wickliffe, K. E., Lorenz, S., Wemmer, D. E., Kuriyan, J., and Rape, M. (2011) The mechanism of linkage-specific ubiquitin chain elongation by a single-subunit E2. Cell 144, 769-781