The xeroderma pigmentosum group E gene product DDB2 activates nucleotide excision repair by regulating the level of p21Waf1/Cip1

Molecular and Cellular Biology

Volumn 28, Issue 1, 2008, Pages 177-187

  Stoyanova, Tanya ^a   Yoon, Taewon ^a,b   Kopanja, Dragana ^a   Mokyr, Margalit B ^a   Raychaudhuri, Pradip ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; GENE PRODUCT; PROTEIN P53; SERINE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP E COMPLEMENTING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA REPLICATION; EMBRYO; EXCISION REPAIR; FIBROBLAST; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; UBIQUITINATION;

ANIMALS; CELL LINE; CULLIN PROTEINS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; MICE; MICE, KNOCKOUT; NUCLEOTIDES; PROTEIN BINDING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS; XERODERMA PIGMENTOSUM;

EID: 37549061452     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00880-07     Document Type: Article

References (57)

1. Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177-2196.
2. Abrahams, P. J., R. Schouten, T. van Laar, A. Houweling, C. Terleth, and A. J. van der Eb. 1995. Different regulation of p53 stability in UV-irradiated normal and DNA repair deficient human cells. Mutat. Res. 336:169-180.
3. Alekseev, S., H. Kool, H. Rebel, M. Fousteri, J. Moser, C. Backendorf, F. R. de Gruijl, H. Vrieling, and L. H. Mullenders. 2005. Enhanced DDB2 expression protects mice from carcinogenic effects of chronic UV-B irradiation. Cancer Res. 65:10298-10306.
4. Arias, E. E., and J. C. Walter. 2006. PCNA functions as a molecular platform to trigger Cdt1 destruction and prevent re-replication. Nat. Cell Biol. 8:84-90.
5. Banks, D., M. Wu, L. A. Higa, J. Quan, T. Ye, R. Kobayashi, H. Sun, and H. Zhang. 2006. L2DTL/CDT2 and PCNA interact with p53 and regulate p53 polyubiquitination and protein stability through MDM2 and CUL4A/DDB1 complex. Cell Cycle 5:1719-1729.
6. Bech-Otschir, D., R. Kraft, X. Huang, P. Henklein, B. Kapelari, C. Pollmann, and W. Dubiel. 2001. COP9 signalosome-specific phosphorylation targets p53 to degradation by the ubiquitin system. EMBO J. 20:1630-1639.
7. WAF1 to promote DNA repair. Cell 114:599-610.
8. Cang, Y., J. Zhang, S. A. Nicholas, J. Bastien, B. Li, P. Zhou, and S. P. Goff. 2006. Deletion of DDB1 in mouse brain and lens leads to p53-dependent elimination of proliferating cells. Cell 127:929-940.
9. Chao, C., M. Hergenhahn, M. D. Kaeser, Z. Wu, S. Saito, R. Iggo, M. Hollstein, E. Appella, and Y. Xu. 2003. Cell type- and promoter-specific roles of Ser18 phosphorylation in regulating p53 responses. J. Biol. Chem. 278:41028-41033.
10. Chen, X., J. Zhang, J. Lee, P. S. Lin, J. M. Ford, N. Zheng, and P. Zhou. 2006. A kinase-independent function of c-Abl in promoting proteolytic destruction of damaged DNA binding proteins. Mol. Cell 22:489-499.
11. Cleaver, J. E. 2005. Cancer in xeroderma pigmentosum and related disorders of DNA repair. Nat. Rev. Cancer 5:564-573.
12. Cooper, M. P., A. S. Balajee, and V. A. Bohr. 1999. The C-terminal domain of p21 inhibits nucleotide excision repair in vitro and in vivo. Mol. Biol. Cell 10:2119-2129.
13. Datta, A., S. Bagchi, A. Nag, P. Shiyanov, G. R. Adami, T. Yoon, and P. Raychaudhuri. 2001. The p48 subunit of the damaged-DNA binding protein DDB associates with the CBP/p300 family of histone acetyltransferase. Mutat. Res. 486:89-97.
14. El-Mahdy, M. A., Q. Zhu, Q. E. Wang, G. Wani, M. Praetorius-Ibba, and A. A. Wani. 2006. Cullin 4A-mediated proteolysis of DDB2 protein at DNA damage sites regulates in vivo lesion recognition by XPC. J. Biol. Chem. 281:13404-13411.
15. Ford, J. M., and P. Hanawalt. 1997. Expression of wild-type p53 is required for efficient global genomic nucleotide excision repair in UV-irradiated human fibroblasts. J. Biol. Chem. 272:28073-28080.
16. Friedberg, E. C. 2001. How nucleotide excision repair protects against cancer. Nat. Rev. Cancer 1:22-33.
17. Groisman, R., J. Polanowska, I. Kuraoka, J. Sawada, M. Saijo, R. Drapkin, A. F. Kisselev, K. Tanaka, and Y. Nakatani. 2003. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113:357-367.
18. Higa, L. A., I. S. Mihaylov, D. P. Banks, J. Zheng, and H. Zhang. 2003. Radiation-mediated proteolysis of CDT1 by CUL4-ROC1 and CSN complexes constitutes a new checkpoint. Nat. Cell Biol. 5:1008-1015.
19. Higa, L. A., M. Wu, T. Ye, R. Kobayashi, H. Sun, and H. Zhang. 2006. CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 8:1277-1283.
20. Hu, J., C. M. McCall, T. Ohta, and Y. Xiong. 2004. Targeted ubiquitination of Cdt1 by the DDB1-Cul4A-Roc1 ligase in response to DNA damage. Nat. Cell Biol. 6:1003-1009.
21. Hu, J., and Y. Xiong. 2006. An evolutionarily conserved function of proliferating cell nuclear antigen for Cdt1 degradation by the Cul4-Ddb1 ubiquitin ligase in response to DNA damage. J. Biol. Chem. 281:3753-3756.
22. Itoh, T., D. Cado, R. Kamide, and S. Linn. 2004. DDB2 gene disruption leads to skin tumors and resistance to apoptosis after exposure to ultraviolet light but not a chemical carcinogen. Proc. Natl. Acad. Sci. USA 101:2052-2057.
23. Itoh, T., and S. Linn. 2005. The fate of p21CDKN1A in cells surviving UV-irradiation. DNA Repair 4:1457-1462.
24. Kapetanaki, M. G., J. Guerrero-Santoro, D. C. Bisi, C. L. Hsieh, V. Rapic-Otrin, and A. S. Levine. 2006. The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc. Natl. Acad. Sci. USA 103:2588-2593.
25. Keeney, S., A. P. Eker, T. Brody, W. Vermeulen, D. Bootsma, J. H. Hoeijmakers, and S. Linn. 1994. Correction of the DNA repair defect in xeroderma pigmentosum group E by injection of a DNA damage-binding protein. Proc. Natl. Acad. Sci. USA 91:4053-4056.
26. Kulaksiz, G., J. T. Reardon, and A. Sancar. 2005. Xeroderma pigmentosum complementation group E protein (XPE/DDB2): purification of various complexes of XPE and analyses of their damaged DNA binding and putative DNA repair properties. Mol. Cell. Biol. 25:9784-9792.
27. Li, R., S. Waga, G. J. Hannon, D. Beach, and B. Stillman. 1994. Differential effects by the p21 CDK inhibitor on PCNA-dependent DNA replication and repair. Nature 371:534-537.
28. Liu, W., A. F. Nichols, J. A. Graham, R. Dualan, A. Abbas, and S. Linn. 2000. Nuclear transport of human DDB protein induced by ultraviolet light. J. Biol. Chem. 275:21429-21434.
29. Lovejoy, C. A., K. Lock, A. Yenamandra, and D. Cortez. 2006. DDB1 maintains genome integrity through regulation of Cdt1. Mol. Cell. Biol. 26:7977-7990.
30. Lu, X., B. Nannenga, and L. A. Donehower. 2005. PPM1D dephosphorylates Chk1 and p53 and abrogates cell cycle checkpoints. Genes Dev. 19:1162-1174.
31. Waf1/Cip1 in Gadd45-deficient keratinocytes restores DNA repair capacity. Carcinogenesis 26:1804-1810.
32. Waf1/Cip1-/- human cancer cells. Cancer Res. 56:2250-2256.
33. Nag, A., T. Bondar, S. Shiv, and P. Raychaudhuri. 2001. The XP-E gene product DDB2 is a specific target of cullin 4A in mammalian cell. Mol. Cell. Biol. 21:6738-6747.
34. Nag, A., A. Datta, K. Yoo, D. Bhattacharyya, A. Chakrabortty, X. Wang, B. L. Slagle, R. H. Costa, and P. Raychaudhuri. 2001. DDB2 induces nuclear accumulation of the hepatitis B virus X protein independently of binding to DDB1. J. Virol. 75:10383-10389.
35. Nag, A., S. Bagchi, and P. Raychaudhuri. 2004. Cul4A physically associates with MDM2 and participates in the proteolysis of p53. Cancer Res. 64:8152-8165.
36. Nichols, A. F., T. Itoh, J. A. Graham, W. Liu, M. Yamaizumi, and S. Linn. 2000. Human damage-specific DNA-binding protein p48. Characterization of XPE mutations and regulation following UV irradiation. J. Biol. Chem. 275:21422-21428.
37. Nichols, A. F., and A. Sancar. 1992. Purification of PCNA as a nucleotide excision repair protein. Nucleic Acids Res. 20:2441-2446.
38. Pan, Z. Q., J. T. Reardon, Li, L., H. Flores-Rozas, R. Legerski, A. Sancar, and J. Hurwitz. 1995. Inhibition of nucleotide excision repair by the cyclin-dependent kinase inhibitor p21. J. Biol. Chem. 270:22008- 22016.
39. Rapi ć Otrin, V., I. Kuraoka, T. Nardo, M. McLenigan, A. P. Eker, M. Stefanini, A. S. Levine, and R. D. Wood. 1998. Relationship of the xeroderma pigmentosum group E DNA repair defect to the chromatin and DNA binding proteins UV-DDB and replication protein A. Mol. Cell. Biol. 18:3182-3190.
40. Reardon, J. T., and A. Sancar. 2003. Recognition and repair of the cyclobutane thymine dimer, a major cause of skin cancers, by the human excision nuclease. Genes Dev. 17:2539-2551.
41. Sancar, A., L. A. Lindsey-Boltz, K. Unsal-Kacmaz, and S. Linn. 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73:39-85.
42. Senga, T., U. Sivaprasad, W. Zhu, J. H. Park, E. E. Arias, J. C. Walter, and A. Dutta. 2006. PCNA is a cofactor for Cdt1 degradation by CUL4/DDB1-mediated N-terminal ubiquitination. J. Biol. Chem. 281:6246-6252.
43. Shivji, M. K., S. J. Grey, U. P. Strausfeld, R. D. Wood, and J. J. Blow. 1994. Cip1 inhibits DNA replication but not PCNA-dependent nucleotide excision-repair. Curr. Biol. 4:1062-1068.
44. Shivji, M. K., E. Ferrari, K. Ball, U. Hubscher, and R. D. Wood. 1998. Resistance of human nucleotide repair synthesis in vitro to p21Cdn1. Oncogene 17:2827-2838.
45. Shiyanov, P., S. A. Hayes, M. Donepudi, A. F. Nichols, S. Linn, B. L. Slagle, and P. Raychaudhuri. 1999. The naturally occurring mutants of DDB are impaired in stimulating nuclear import of the p125 subunit and E2F1-activated transcription. Mol. Cell. Biol. 19:4935-4943.
46. Shiyanov, P., A. Nag, and P. Raychaudhuri. 1999. Cullin 4A associates with the UV-damaged DNA-binding protein DDB. J. Biol. Chem. 274:35309-35312.
47. Smith, M. L., J. M. Ford, M. C. Hollander, R. A. Bortnick, S. A. Amundson, Y. R. Seo, C. X. Deng, P. C. Hanawalt, and A. J. Fornace, Jr. 2000. p53-mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21, and/or gadd45 genes. Mol. Cell. Biol. 20:3705-3714.
48. Tang, J., and G. Chu. 2002. Xeroderma pigmentosum complementation group E and UV-damaged DNA-binding protein. DNA Repair 1:601-616.
49. Toledo, F., and G. M. Wahl. 2006. Regulating the p53 pathways: in vitro hypotheses, in vivo veritas. Nat. Rev. Cancer 6:909-923.
50. Wahl, G. M., and A. M. Carr. 2001. The evolution of diverse biological responses to DNA damage: insight from yeast and p53. Nat. Cell Biol. 3:E277-E284.
51. Wakasugi, M., A. Kawashima, H. Morioka, S. Linn, A. Sancar, T. Mori, O. Nikaido, and T. Matsunaga. 2002. DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J. Biol. Chem. 277:1637-1640.
52. Wang, H., L. Zhai, J. Xu, H. Y. Joo, S. Jackson, H. Erdjument-Bromage, P. Tempst, Y. Xiong, and Y. Zhang. 2006. Histone H3 and H4 Ubiquitylation by the CUL4-DDB-ROC1 Ubiquitin Ligase Facilitates Cellular Response to DNA Damage. Mol. Cell 22:383-394.
53. Xirodimas, D., M. K. Seville, C. Edling, D. P. Lane, and S. Lain. 2001. Different effects of p14ARF on the levels of ubiquitinated p53 and Mdm2 in vivo. Oncogene 20:4972-4983.
54. Yoon, T., A. Chakrabortty, R. Franks, T. Valli, H. Kiyokawa, and P. Raychaudhuri. 2005. Tumor-prone phenotype of the DDB2-deficient mice. Oncogene 24:469-478.
55. Zhang, Y.-W., D. M. Otterness, G. G. Chiang, W. Xie, Y.-C. Liu, F. Mercurio, and R. T. Abraham. 2005. Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol. Cell 19:607-618.
56. Zhou, B. B., and S. J. Elledge. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433-439.
57. Zotter, A., M. S. Luisjsterburg, D. O. Warmerdam, S. Ibrahim, A. Nigg, W. A. van Cappellen, J. H. J. Hoeijmakers, R. van Driel, W. Vermeulen, and A. B. Houtsmuller. 2006. Recruitment of the nucleotide excision repair endonuclease XPG to site of UV-induced DNA damage depends on functional TFIIH. Mol. Cell. Biol. 26:8868-8879.