Degradation of transcription repressor ZBRK1 through the ubiquitin-proteasome pathway relieves repression of Gadd45a upon DNA damage

Molecular and Cellular Biology

Volumn 23, Issue 20, 2003, Pages 7305-7314

  Yun, Jeanho ^a   Lee, Wen Hwa ^a,b  

^a Mays Cancer Center at UT Health San Antonio   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BRCA1 PROTEIN; DNA; E3 LIGASE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45A; LIGASE; MESYLIC ACID METHYL ESTER; PROTEASOME INHIBITOR; PROTEIN ZBRK1; UBIQUITIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; DNA DAMAGE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; KRAB DOMAIN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; ULTRAVIOLET IRRADIATION;

BLOTTING, WESTERN; BRCA1 PROTEIN; CELL CYCLE PROTEINS; CELL LINE; CELL LINE, TUMOR; CYSTEINE ENDOPEPTIDASES; DNA; DNA DAMAGE; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; GENES, REPORTER; HUMANS; LUCIFERASES; MULTIENZYME COMPLEXES; MUTATION; NUCLEAR PROTEINS; PLASMIDS; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; UBIQUITIN; ULTRAVIOLET RAYS; ZINC FINGERS;

EID: 0141864358     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.20.7305-7314.2003     Document Type: Article

References (59)

1. Aberle, H., A. Bauer, J. Stappert, A. Kispert, and R. Kemler. 1997. β-Catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16:3797-3804.
2. Bellefroid, E. J., D. A. Poncelet, P. J. Lecocq, O. Revelant, and J. A. Martial. 1991. The evolutionarily conserved Kruppel-associated box domain defines a subfamily of eukaryotic multifingered proteins. Proc. Natl. Acad. Sci. USA 88:3608-3612.
3. Bignell, G. R., W. Warren, S. Seal, M. Takahashi, E. Rapley, R. Barfoot, H. Green, C. Brown, P. J. Biggs, S. R. Lakhani, C. Jones, J. Hansen, E. Blair, B. Hofmann, R. Siebert, G. Turner, D. G. Evans, C. Schrander-Stumpel, F. A. Beemer, A. van den Ouweland, D. Halley, B. Delpech, M. G. Cleveland, I. Leigh, J. Leisti, and S. Rasmussen. 2000. Identification of the familial cylindromatosis tumour-suppressor gene. Nat. Genet. 25:160-165.
4. Chen, A., F. E. Kleiman, J. L. Manley, T. Ouchi, and Z. Q. Pan. 2002. Auto-ubiquitination of the BRCA1/BARD1 RING ubiquitin ligase. J. Biol. Chem. 277:22085-22092.
5. Coux, O., K. Tanaka, and A. L. Goldberg. 1996. Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65:801-847.
6. Fan, S., J. Wang, R. Yuan, Y. Ma, Q. Meng, M. R. Erdos, R. G. Pestell, F. Yuan, K. J. Auborn, I. D. Goldberg, and E. M. Rosen. 1999. BRCA1 inhibition of estrogen receptor signaling in transfected cells. Science 284:1354-1356.
7. Friedman, J. R., W. J. Fredericks, D. E. Jensen, D. W. Speicher, X. P. Huang, E. G. Neilson, and F. J. Rauscher III. 1996. KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev. 10:2067-2078.
8. Glotzer, M., A. W. Murray, and M. W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature 349:132-138.
9. Harkin, D. P., J. M. Bean, D. Miklos, Y. H. Song, V. B. Truong, C. Englert, F. C. Christians, L. W. Ellisen, S. Maheswaran, J. D. Oliner, and D. A. Haber. 1999. Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1. Cell 97:575-586.
10. Hashizume, R., M. Fukuda, I. Maeda, H. Nishikawa, D. Oyake, Y. Yabuki, H. Ogata, and T. Ohta. 2001. The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 276:14537-14540.
11. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
12. Hofmann, F., F. Martelli, D. M. Livingston, and Z. Wang. 1996. The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes Dev. 10:2949-2959.
13. Hollander, M. C., M. S. Sheikh, D. V. Bulavin, K. Lundgren, L. Augeri-Henmueller, R. Shehee, T. A. Molinaro, K. E. Kim, E. Tolosa, J. D. Ashwell, M. P. Rosenberg, Q. Zhan, P. M. Fernandez-Salguero, W. F. Morgan, C. X. Deng, and A. J. Fornace, Jr. 1999. Genomic instability in Gadd45a-deficient mice. Nat. Genet. 23:176-184.
14. Jin, S., M. J. Antinore, F. D. Lung, X. Dong, H. Zhao, F. Fan, A. B. Colchagie, P. Blanck, P. P. Roller, A. J. Fornace, Jr., and Q. Zhan. 2000. The GADD45 inhibition of Cdc2 kinase correlates with GADD45-mediated growth suppression. J. Biol. Chem. 275:16602-16608.
15. Jin, S., F. Fan, W. Fan, H. Zhao, T. Tong, P. Blanck, I. Alomo, B. Rajasekaran, and Q. Zhan. 2001. Transcription factors Oct-1 and NF-YA regulate the p53-independent induction of the GADD45 following DNA damage. Oncogene 20:2683-2690.
16. Jin, Y., X. L. Xu, M. C. Yang, F. Wei, T. C. Ayi, A. M. Bowcock, and R. Baer. 1997. Cell cycle-dependent colocalization of BARD1 and BRCA1 proteins in discrete nuclear domains. Proc. Natl. Acad. Sci. USA 94:12075-12080.
17. Kastan, M. B., Q. Zhan, W. S. El-Deiry, F. Carrier, T. Jacks, W. V. Walsh, B. S. Plunkett, B. Vogelstein, and A. J. Fornace, Jr. 1992. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxiatelangiectasia. Cell 71:587-597.
18. Kearsey, J. M., P. J. Coates, A. R. Prescott, E. Warbrick, and P. A. Hall. 1995. Gadd45 is a nuclear cell cycle regulated protein which interacts with p21Cip1. Oncogene 11:1675-1683.
19. Khanna, K. K., and S. P. Jackson. 2001. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27:247-254.
20. Kim, S. S., Y. M. Chen, E. O'Leary, R. Witzgall, M. Vidal, and J. V. Bonventre. 1996. A novel member of the RING finger family, KRIP-1, associates with the KRAB-A transcriptional repressor domain of zinc finger proteins. Proc. Natl. Acad. Sci. USA 93:15299-15304.
21. Kim, S. T., D. S. Lim, C. E. Canman, and M. B. Kastan. 1999. Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274:37538-37543.
22. King, R. W., M. Glotzer, and M. W. Kirschner. 1996. Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol. Biol. Cell 7:1343-1357.
23. Lechner, M. S., G. E. Begg, D. W. Speicher, and F. J. Rauscher III. 2000. Molecular determinants for targeting heterochromatin protein 1-mediated gene silencing: direct chromoshadow domain-KAP-1 corepressor interaction is essential. Mol. Cell. Biol. 20:6449-6465.
24. Li, C. D., C. Larsson, A. Futreal, J. Lancaster, C. Phelan, U. Aspenblad, B. Sundelin, Y. Liu, P. Ekman, G. Auer, and U. S. R. Bergerheim. 1998. Identification of two distinct deleted regions on chromosome 13 in prostate cancer. Oncogene 16:481-487.
25. Li, S., P. L. Chen, T. Subramanian, G. Chinnadurai, G. Tomlinson, C. K. Osborne, Z. D. Sharp, and W. H. Lee. 1999. Binding of CtIP to the BRCT repeats of BRCA1 involved in the transcription regulation of p21 disrupted upon DNA damage. J. Biol. Chem. 274:11334-11338.
26. Li, S., N. S. Ting, L. Zheng, P. L. Chen, Y. Ziv, Y. Shiloh, E. Y. Lee, and W. H. Lee. 2000. Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature 406:210-215.
27. Loda, M., B. Cukor, S. W. Tam, P. Lavin, M. Florentino, G. F. Draetta, J. M. Jessup, and M. Pagano. 1997. Increased proteasome-dependent degradation of the cyclin-dependent kinase inhibitor p27 in aggressive colorectal carcinomas. Nat. Med. 3:231-234.
28. Maki, C. G., J. M. Huibregtse, and P. M. Howley. 1996. In vivo ubiquitination and proteasome-mediated degradation of p531. Cancer Res. 56:2649-2654.
29. Mallery, D. L., C. J. Vandenberg, and K. Hiom. 2002. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. EMBO J. 21:6755-6762.
30. Margolin, J. F., J. R. Friedman, W. K. Meyer, H. Vissing, H. J. Thiesen, and F. J. Rauscher III. 1994. Kruppel-associated boxes are potent transcriptional repression domains. Proc. Natl. Acad. Sci. USA 91:4509-4513.
31. Maxwell, P. H., M. S. Wiesener, G. W. Chang, S. C. Clifford, E. C. Vaux, M. E. Cockman, C. C. Wykoff, C. W. Pugh, E. R. Maher, and P. J. Ratcliffe. 1999. The turnout suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271-275.
32. Moosmann, P., O. Georgiev, B. Le Douarin, J. P. Bourquin, and W. Schaffner. 1996. Transcriptional repression by RING finger protein TIF1 β that interacts with the KRAB repressor domain of KOX1. Nucleic Acids Res. 24:4859-4867.
33. Palombella, V. J., O. J. Rando, A. L. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor protein and the activation of NF-κB. Cell 78:773-785.
34. Pickart, C. M. 2001. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70:503-533.
35. Pickart, C. M. 2000. Ubiquitin in chains. Trends Biochem. Sci. 25:544-548.
36. Rechsteiner, M., and S. W. Rogers. 1996. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21:267-271.
37. Ruffner, H., C. A. Joazeiro, D. Hemmati, T. Hunter, and I. M. Verma. 2001. Cancer-predisposing mutations within the RING domain of BRCA1: loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. Proc. Natl. Acad. Sci. USA 98:5134-5139.
38. Schultz, D. C., K. Ayyanathan, D. Negorev, G. G. Maul, and F. J. Rauscher III. 2002. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16:919-932.
39. Schultz, D. C., J. R. Friedman, and F. J. Rauscher III. 2001. Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2α subunit of NURD. Genes Dev. 15:428-443.
40. Smith, M. L., I. T. Chen, Q. Zhan, L. Bae, C. Y. Chen, T. M. Gilmer, M. B. Kastan, P. M. O'Connor, and A. J. Fornace, Jr. 1994. Interaction of the p53-regulated protein Gadd45 with proliferating cell nuclear antigen. Science 266:1376-1380.
41. WAF1/CiP1. Nature 389:187-190.
42. Thompson, L. H., and D. Schild. 2002. Recombinational DNA repair and human disease. Mutat. Res. 509:49-78.
43. Tomlinson, G. E., T. T. Chen, V. A. Stastny, A. K. Virmani, M. A. Spillman, V. Tonk, J. L. Blum, N. R. Schneider, I. I. Wistuba, J. W. Shay, J. D. Minna, and A. F. Gazdar. 1998. Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res. 58:3237-3242.
44. Treier, M., L. M. Staszewski, and D. Bohmann. 1994. Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78:787-798.
45. Venkitaraman, A. R. 2002. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108:171-182.
46. Vissing, H., W. K. Meyer, L. Aagaard, N. Tommerup, and H. J. Thiesen. 1995. Repression of transcriptional activity by heterologous KRAB domains present in zinc finger proteins. FEBS Lett. 369:153-157.
47. Wang, Q., H. Zhang, K. Kajino, and M. I. Greene. 1998. BRCA1 binds c-Myc and inhibits its transcriptional and transforming activity in cells. Oncogene 17:1939-1948.
48. 2/M cell cycle checkpoint. Proc. Natl. Acad. Sci. USA 96:3706-3711.
49. Witzgall, R., E. O'Leary, A. Leaf, D. Onaldi, and J. V. Bonventre. 1994. The Kruppel-associated box-A (KRAB-A) domain of zinc finger proteins mediates transcriptional repression. Proc. Natl. Acad. Sci. USA 91:4514-4518.
50. Xia, Y., G. M. Pao, H. W. Chen, I. M. Verma, and T. Hunt. 2003. Enhancement of Brca1 E3 ubiquitin ligase activity through direct interaction with the BARD1 protein. J. Biol. Chem. 278:5255-5263.
51. Yamano, H., J. Gannon, and T. Hunt. 1996. The role of proteolysis in cell cycle progression in S. pombe. EMBO J. 15:5268-5279.
52. Yarden, R. I., and L. C. Brody. 1999. BRCA1 interacts with components of the histone deacetylase complex. Proc. Natl. Acad. Sci. USA 96:4983-4988.
53. Zhan, Q., M. J. Antinore, X. W. Wang, F. Carrier, M. L. Smith, C. C. Harris, and A. J. Fornace, Jr. 1999. Association with Cdc2 and inhibition of Cdc2/Cyclin B1 kinase activity by the p53-regulated protein Gadd45. Oncogene 18:2892-2900.
54. Zhan, Q., I. Bae, M. B. Kastan, and A. J. Fornace, Jr. 1994. The p53-dependent gamma-ray response of GADD45. Cancer Res. 54:2755-2760.
55. Zhan, Q., I. T. Chen, M. J. Antinore, and A. J. Fornace, Jr. 1998. Tumor suppressor p53 can participate in transcriptional induction of the Gadd45 promoter in the absence of direct DNA binding. Mol. Cell. Biol. 18:2768-2778.
56. Zhan, Q., S. Fan, M. L. Smith, I. Bae, K. Yu, I. Alamo, Jr., P. M. O'Connor, and A. J. Fornace, Jr. 1996. Abrogation of p53 function affects gadd gene responses to DNA base-damaging agents and starvation. DNA Cell Biol. 15:805-815.
57. Zheng, L., L. A. Annab, C. A. Afshari, W. H. Lee, and T. G. Boyer. 2001. BRCA1 mediates ligand-independent transcriptional repression of the estrogen receptor. Proc. Natl. Acad. Sci. USA 98:9587-9592.
58. Zheng, L., S. Li, T. G. Boyer, and W. H. Lee. 2000. Lessons learned from BRCA1 and BRCA2. Oncogene 19:6159-6175.
59. Zheng, L., H. Pan, S. Li, A. Flesken-Nikitin, P. L. Chen, T. G. Boyer, and W. H. Lee. 2000. Sequence-specific transcriptional corepressor function for BRCA1 through a novel zinc finger protein. ZBRK1. Mol. Cell 6:757-768.