DNA damage-induced activation of CUL4B targets HUWE1 for proteasomal degradation

Nucleic Acids Research

Volumn 43, Issue 9, 2015, Pages 4579-4590

  Yi, Juan ^a,b   Lu, Guang ^a   Li, Li ^a   Wang, Xiaozhen ^c   Cao, Li ^a   Lin, Ming ^a   Zhang, Sha ^a   Shao, Genze ^a,b  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b PEKING UNIVERSITY   (China)

^c JILIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CULLIN4B RING E3 LIGASE; HUWE1 PROTEIN; LIGASE; NEDD8 PROTEIN; PROTEASOME; PROTEIN MCL 1; UNCLASSIFIED DRUG; CUL4B PROTEIN, HUMAN; CULLIN; HUWE1 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; EMBRYO; ENZYME ACTIVATION; ENZYME INACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NEDDYLATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; SENSITIVITY ANALYSIS; UBIQUITINATION; UPREGULATION; CELL LINE; METABOLISM;

APOPTOSIS; CELL LINE; CULLIN PROTEINS; DNA DAMAGE; DOWN-REGULATION; ENZYME ACTIVATION; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84936806751     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv325     Document Type: Article

References (65)

1. Ciccia, A. and Elledge, S.J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell, 40, 179-204.
2. Harper, J.W. and Elledge, S.J. (2007) The DNA damage response: ten years after. Mol. Cell, 28, 739-745.
3. Silverman, J.S., Skaar, J.R. and Pagano, M. (2012) SCF ubiquitin ligases in the maintenance of genome stability. Trends Biochem. Sci., 37, 66-73.
4. Messick, T.E. and Greenberg, R.A. (2009) The ubiquitin landscape at DNA double-strand breaks. J. Cell Biol., 187, 319-326.
5. Wrighton, K.H. (2014) DNA damage response: a ligase makes sense of DNA damage. Nat. Rev. Mol. Cell Biol., 15, 76-77.
6. Pickart, C.M. (2004) Back to the future with ubiquitin. Cell, 116, 181-190.
7. Bhoj, V.G. and Chen, Z.J. (2009) Ubiquitylation in innate and adaptive immunity. Nature, 458, 430-437.
8. Zhong, Q., Gao, W., Du, F and Wang, X. (2005) Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell, 121, 1085-1095.
9. Parsons, J.L., Tait, P.S., Finch, D., Dianova, I.I., Edelmann, M.J., Khoronenkova, S.V., Kessler, B.M., Sharma, R.A., McKenna, W.G. and Dianov, G.L. (2009) Ubiquitin ligase ARF-BP1/Mule modulates base excision repair. EMBO J., 28, 3207-3215.
10. Hall, J.R., Kow, E., Nevis, K.R., Lu, C.K., Luce, K.S., Zhong, Q. and Cook, J.G. (2007) Cdc6 stability is regulated by the Huwe1 ubiquitin ligase after DNA damage. Mol. Biol. Cell, 18, 3340-3350.
11. Herold, S., Hock, A., Herkert, B., Berns, K., Mullenders, J., Beijersbergen, R., Bernards, R. and Eilers, M. (2008) Miz1 and HectH9 regulate the stability of the checkpoint protein, TopBP1. EMBO J., 27, 2851-2861.
12. Markkanen, E., van Loon, B., Ferrari, E., Parsons, J.L., Dianov, G.L. and Hubscher, U. (2012) Regulation of oxidative DNA damage repair by DNA polymerase lambda and MutYH by cross-talk of phosphorylation and ubiquitination. Proc. Natl Acad. Sci. U. S. A., 109, 437-442.
13. Wang, X., Lu, G., Li, L., Yi, J., Yan, K., Wang, Y., Zhu, B., Kuang, J., Lin, M., Zhang, S. et al. (2014) HUWE1 interacts with BRCA1 and promotes its degradation in the ubiquitin-proteasome pathway. Biochem. Biophys. Res. Commun., 444, 549-554.
14. Zhao, X., Heng, J.I., Guardavaccaro, D., Jiang, R., Pagano, M., Guillemot, F., Iavarone, A. and Lasorella, A. (2008) The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myconcoprotein. Nat. Cell Biol., 10, 643-653.
15. Adhikary, S., Marinoni, F., Hock, A., Hulleman, E., Popov, N., Beier, R., Bernard, S., Quarto, M., Capra, M., Goettig, S. et al. (2005) The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell, 123, 409-421.
16. Yang, Y., Do, H., Tian, X., Zhang, C., Liu, X., Dada, L.A., Sznajder, J.I. and Liu, J. (2010) E3 ubiquitin ligase Mule ubiquitinates Miz1 and is required for TNFalpha-induced JNK activation. Proc. Natl Acad. Sci. U. S. A., 107, 13444-13449.
17. 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.
18. Chen, D., Kon, N., Li, M., Zhang, W., Qin, J. and Gu, W. (2005) ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell, 121, 1071-1083.
19. Leboucher, G.P., Tsai, Y.C., Yang, M., Shaw, K.C., Zhou, M., Veenstra, T.D., Glickman, M.H. and Weissman, A.M. (2012) Stress-induced phosphorylation and proteasomal degradation of mitofusin 2 facilitates mitochondrial fragmentation and apoptosis. Mol. Cell, 47, 547-557.
20. Zhou, X., Li, T.T., Feng, X., Hsiang, E., Xiong, Y., Guan, K.L. and Lei, Q.Y. (2012) Targeted polyubiquitylation of RASSF1C by the Mule and SCFbeta-TrCP ligases in response to DNA damage. Biochem. J., 441, 227-236.
21. Zhang, J., Kan, S., Huang, B., Hao, Z., Mak, T.W. and Zhong, Q. (2011) Mule determines the apoptotic response to HDAC inhibitors by targeted ubiquitination and destruction of HDAC2. Genes Dev., 25, 2610-2618.
22. Khoronenkova, S.V. and Dianov, G.L. (2013) USP7S-dependent inactivation of Mule regulates DNA damage signalling and repair. Nucleic Acids Res., 41, 1750-1756.
23. Sherr, C.J. (2001) The INK4a/ARF network in tumour suppression. Nat. Rev. Mol. Cell Biol., 2, 731-737.
24. Kamijo, T., van de Kamp, E., Chong, M.J., Zindy, F., Diehl, J.A., Sherr, C.J. and McKinnon, P.J. (1999) Loss of the ARF tumor suppressor reverses premature replicative arrest but not radiation hypersensitivity arising from disabled atm function. Cancer Res., 59, 2464-2469.
25. Petroski, M.D. and Deshaies, R.J. (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol., 6, 9-20.
26. Jackson, S. and Xiong, Y. (2009) CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem. Sci., 34, 562-570.
27. Liu, L., Lee, S., Zhang, J., Peters, S.B., Hannah, J., Zhang, Y., Yin, Y., Koff, A., Ma, L. and Zhou, P. (2009) CUL4A abrogation augments DNA damage response and protection against skin carcinogenesis. Mol. Cell, 34, 451-460.
28. Nakagawa, T. and Xiong, Y. (2011) X-linked mental retardation gene CUL4B targets ubiquitylation of H3K4 methyltransferase component WDR5 and regulates neuronal gene expression. Mol. Cell, 43, 381-391.
29. Zou, Y., Mi, J., Cui, J., Lu, D., Zhang, X., Guo, C., Gao, G., Liu, Q., Chen, B., Shao, C. et al. (2009) Characterization of nuclear localization signal in the N terminus of CUL4B and its essential role in cyclin E degradation and cell cycle progression. J. Biol. Chem., 284, 33320-33332.
30. Ohtake, F., Baba, A., Takada, I., Okada, M., Iwasaki, K., Miki, H., Takahashi, S., Kouzmenko, A., Nohara, K., Chiba, T. et al. (2007) Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature, 446, 562-566.
31. Isidor, B., Pichon, O., Baron, S, David, A. and Le Caignec, C. (2010) Deletion of the CUL4B gene in a boy with mental retardation, minor facial anomalies, short stature, hypogonadism, and ataxia. Am. J. Med. Genet. A, 152, 175-180.
32. Badura-Stronka, M., Jamsheer, A., Materna-Kiryluk, A., Sowinska, A., Kiryluk, K., Budny, B. and Latos-Bielenska, A. (2010) A novel nonsense mutation in CUL4B gene in three brothers with X-linked mental retardation syndrome. Clin. Genet., 77, 141-144.
33. Pan, Z.Q., Kentsis, A., Dias, D.C., Yamoah, K. and Wu, K. (2004) Nedd8 on cullin: building an expressway to protein destruction. Oncogene, 23, 1985-1997.
34. Dye, B.T. and Schulman, B.A. (2007) Structural mechanisms underlying posttranslational modification by ubiquitin-like proteins. Annu. Rev. Biophys. Biomol. Struct., 36, 131-150.
35. Yeh, E.T., Gong, L. and Kamitani, T. (2000) Ubiquitin-like proteins: new wines in new bottles. Gene, 248, 1-14.
36. Rabut, G., Le Dez, G., Verma, R., Makhnevych, T., Knebel, A., Kurz, T., Boone, C., Deshaies, R.J. and Peter, M. (2011) The TFIIH subunit Tfb3 regulates cullinneddylation. Mol. Cell, 43, 488-495.
37. Kamura, T., Conrad, M.N., Yan, Q., Conaway, R.C. and Conaway, J.W. (1999) The Rbx1 subunit of SCF and VHL E3 ubiquitin ligase activates Rub1 modification of cullins Cdc53 and Cul2. Genes Dev., 13, 2928-2933.
38. Kurz, T., Ozlu, N., Rudolf, F., O'Rourke, S.M., Luke, B., Hofmann, K., Hyman, A.A., Bowerman, B. and Peter, M. (2005) The conserved protein DCN-1/Dcn1p is required for cullinneddylation in C. elegans and S. cerevisiae. Nature, 435, 1257-1261.
39. Meyer-Schaller, N., Chou, Y.C., Sumara, I., Martin, D.D., Kurz, T., Katheder, N., Hofmann, K., Berthiaume, L.G., Sicheri, F. and Peter, M. (2009) The human Dcn1-like protein DCNL3 promotes Cul3 neddylation at membranes. Proc. Natl Acad. Sci. U. S. A., 106, 12365-12370.
40. Kurz, T., Chou, Y.C., Willems, A.R., Meyer-Schaller, N., Hecht, M.L., Tyers, M., Peter, M. and Sicheri, F. (2008) Dcn1 functions as a scaffold-type E3 ligase for cullinneddylation. Mol. Cell, 29, 23-35.
41. Ma, T., Shi, T., Huang, J., Wu, L., Hu, F., He, P., Deng, W., Gao, P., Zhang, Y., Song, Q. et al. (2008) DCUN1D3, a novel UVC-responsive gene that is involved in cell cycle progression and cell growth. Cancer Sci., 99, 2128-2135.
42. Hu, J., McCall, C.M., Ohta, T. and Xiong, Y. (2004) Targeted ubiquitination of CDT1 by the DDB1-CUL4A-ROC1 ligase in response to DNA damage. Nat. Cell Biol., 6, 1003-1009.
43. Ma, T., Chen, Y., Zhang, F., Yang, C.Y., Wang, S. and Yu, X. (2013) RNF111-dependent neddylation activates DNA damage-induced ubiquitination. Mol. Cell, 49, 897-907.
44. Lee, J. and Zhou, P. (2007) DCAFs, the missing link of the CUL4-DDB1 ubiquitin ligase. Mol. Cell, 26, 775-780.
45. Kravtsova-Ivantsiv, Y. and Ciechanover, A. (2011) Ubiquitination and degradation of proteins. Methods Mol. Biol., 753, 335-357.
46. Huang, T.T. and D'Andrea, A.D. (2006) Regulation of DNA repair by ubiquitylation. Nat. Rev. Mol. Cell Biol., 7, 323-334.
47. Al-Hakim, A., Escribano-Diaz, C., Landry, M.C., O'Donnell, L., Panier, S., Szilard, R.K. and Durocher, D. (2010) The ubiquitous role of ubiquitin in the DNA damage response. DNA Repair (Amst), 9, 1229-1240.
48. Wang, H., Zhai, L., Xu, J., Joo, H.Y., Jackson, S., Erdjument-Bromage, H., Tempst, P., Xiong, Y. and Zhang, Y. (2006) Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell, 22, 383-394.
49. Higa, L.A., Yang, X., Zheng, J., Banks, D., Wu, M., Ghosh, P., Sun, H. and Zhang, H. (2006) Involvement of CUL4 ubiquitin E3 ligases in regulating CDK inhibitors Dacapo/p27Kip1 and cyclin E degradation. Cell Cycle, 5, 71-77.
50. Hori, T., Osaka, F., Chiba, T., Miyamoto, C., Okabayashi, K., Shimbara, N., Kato, S. and Tanaka, K. (1999) Covalent modification of all members of human cullin family proteins by NEDD8. Oncogene, 18, 6829-6834.
51. Kerzendorfer, C., Whibley, A., Carpenter, G., Outwin, E., Chiang, S.C., Turner, G., Schwartz, C., El-Khamisy, S., Raymond, F.L. and O'Driscoll, M. (2010) Mutations in Cullin 4B result in a human syndrome associated with increased camptothecin-induced topoisomerase I-dependent DNA breaks. Hum. Mol. Genet., 19, 1324-1334.
52. He, F., Lu, D., Jiang, B., Wang, Y., Liu, Q., Liu, Q., Shao, C., Li, X. and Gong, Y. (2013) X-linked intellectual disability gene CUL4B targets Jab1/CSN5 for degradation and regulates bone morphogenetic protein signaling. Biochim. Biophys. Acta, 1832, 595-605.
53. Li, X., Lu, D., He, F., Zhou, H., Liu, Q., Wang, Y., Shao, C. and Gong, Y. (2011) Cullin 4B protein ubiquitin ligase targets peroxiredoxin III for degradation. J. Biol. Chem., 286, 32344-32354.
54. Deffenbaugh, A.E., Scaglione, K.M., Zhang, L., Moore, J.M., Buranda, T., Sklar, L.A. and Skowyra, D. (2003) Release of ubiquitin-charged Cdc34-S-Ub from the RING domain is essential for ubiquitination of the SCF(Cdc4)-bound substrate Sic1. Cell, 114, 611-622.
55. Higa, L.A., Wu, M., Ye, T., Kobayashi, R., Sun, H. and Zhang, H. (2006) CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol., 8, 1277-1283.
56. Angers, S., Li, T., Yi, X., MacCoss, M.J., Moon, R.T. and Zheng, N. (2006) Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature, 443, 590-593.
57. Sugasawa, K., Okuda, Y., Saijo, M., Nishi, R., Matsuda, N., Chu, G., Mori, T., Iwai, S., Tanaka, K., Tanaka, K. et al. (2005) UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell, 121, 387-400.
58. Hu, H., Yang, Y., Ji, Q., Zhao, W., Jiang, B., Liu, R., Yuan, J., Liu, Q., Li, X., Zou, Y. et al. (2012) CRL4B catalyzes H2AK119 monoubiquitination and coordinates with PRC2 to promote tumorigenesis. Cancer Cell, 22, 781-795.
59. Chen, L.C., Manjeshwar, S., Lu, Y., Moore, D., Ljung, B.M., Kuo, W.L., Dairkee, S.H., Wernick, M., Collins, C. and Smith, H.S. (1998) The human homologue for the Caenorhabditiselegans cul-4 gene is amplified and overexpressed in primary breast cancers. Cancer Res., 58, 3677-3683.
60. Pan, W.W., Zhou, J.J., Yu, C., Xu, Y., Guo, L.J., Zhang, H.Y., Zhou, D., Song, F.Z. and Fan, H.Y. (2013) Ubiquitin E3 ligase CRL4(CDT2/DCAF2) as a potential chemotherapeutic target for ovarian surface epithelial cancer. J. Biol. Chem., 288, 29680-29691.
61. Jiang, T., Tang, H.M., Wu, Z.H., Chen, J., Lu, S., Zhou, C.Z., Yan, D.W. and Peng, Z.H. (2013) Cullin 4B is a novel prognostic marker that correlates with colon cancer progression and pathogenesis. Med. Oncol., 30, 534.
62. Soucy, T.A., Smith, P.G., Milhollen, M.A., Berger, A.J., Gavin, J.M., Adhikari, S., Brownell, J.E., Burke, K.E., Cardin, D.P., Critchley, S. et al. (2009) An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature, 458, 732-736.
63. Yang, D., Tan, M., Wang, G. and Sun, Y. (2012) The p21-dependent radiosensitization of human breast cancer cells by MLN4924, an investigational inhibitor of NEDD8 activating enzyme. PLoS One, 7, e34079.
64. Soucy, T.A., Dick, L.R., Smith, P.G., Milhollen, M.A. and Brownell, J.E. (2010) The NEDD8 conjugation pathway and its relevance in cancer biology and therapy. Genes Cancer, 1, 708-716.
65. Zhao, Y., Xiong, X., Jia, L. and Sun, Y. (2012) Targeting Cullin-RING ligases by MLN4924 induces autophagy via modulating the HIF1-REDD1-TSC1-mTORC1-DEPTOR axis. Cell Death Dis., 3, e386.