Enhanced DDB2 expression protects mice from carcinogenic effects of chronic UV-B irradiation

Cancer Research

Volumn 65, Issue 22, 2005, Pages 10298-10306

  Alekseev, Sergey ^a   Kool, Hanneke ^a   Rebel, Heggert ^b   Fousteri, Maria ^a   Moser, Jill ^a   Backendorf, Claude ^c   De Gruijl, Frank R ^b   Vrieling, Harry ^a,b   Mullenders, Leon H F ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DAMAGED DNA BINDING PROTEIN 2; DNA BINDING PROTEIN; PYRIMIDINE DERIVATIVE; PYRIMIDINE(6-4)PYRIMIDONE PHOTOPRODUCT; PYRIMIDINONE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENICITY; CELL CULTURE; CONTROLLED STUDY; DNA REPAIR; KERATINOCYTE; LONG TERM EXPOSURE; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIATION INJURY; SKIN CARCINOGENESIS; SKIN FIBROBLAST; SQUAMOUS CELL CARCINOMA; TRANSGENIC MOUSE; ULTRAVIOLET B RADIATION;

ANIMALS; APOPTOSIS; DNA REPAIR; DNA-BINDING PROTEINS; FEMALE; FIBROBLASTS; MALE; MICE; MICE, INBRED HRS; MICE, TRANSGENIC; PEPTIDES; PYRIMIDINE DIMERS; RADIATION TOLERANCE; SKIN; SKIN NEOPLASMS; ULTRAVIOLET RAYS;

EID: 28544434877     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-2295     Document Type: Article

References (48)

1. Fujiwara Y, Masutani C, Mizukoshi T, Kondo J, Hanaoka F, Iwai S. Characterization of DNA recognition by the human UV-damaged DNA-binding protein. J Biol Chem 1999;274:20027-33.
2. Chu G, Chang E. Xeroderma pigmentosum group E cells lack a nuclear factor that binds to damaged DNA. Science 1988;242:564-7.
3. - phenotype. J Biol Chem 1996;271:24317-20.
4. Lehmann AR. DNA repair-deficient diseases xeroderma pigmentosum, Cockayne syndrome, and trichothiodystrophy. Biochimie 2003;85:1101-11.
5. Hwang BJ, Ford JM, Hanawalt PC, Chu G. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc Natl Acad Sci U S A 1999;96:424-8.
6. Itoh T, Mori T, Ohkubo H, Yamaidzumi MA. A newly identified patient with clinical xeroderma pigmentosum phenotype has a non-sense mutation in the DDB2 gene and incomplete repair in (6-4) photoproducts. J Invest Dermatol 1999;113:251-7.
7. Moser J, Volker M, Kool H, et al. The UV-damaged DNA-binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair 2005;4:571-82.
8. Wakasugi M, Shimizu M, Morioka H, Linn S, Nikaido O, Matsunaga T. Damaged DNA-binding protein DDB stimulates the excision of cyclobutane pyrimidine dimers in vitro in concert with XPA and replication protein A. J Biol Chem 2001;276:15434-40.
9. Sugasawa K, Okuda Y, Saijo M, et al. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 2005;121:387-400.
10. Reardon JT, Sancar A. Recognition and repair of the cyclobutane thymine dimer, a major cause of skin cancers, by the human excision nuclease. Genes Dev 2003;17:2539-51.
11. Rapić-Otrin V, Kuraoka I, Nardo T, et al. 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 1998;18:3182-90.
12. Kazantsev A, Mu D, Nichols AF, Zhao X, Linn S, Sancar A. Functional complementation of xeroderma pigmentosum complementation group E by replication protein A in an in vitro system. Proc Natl Acad Sci U S A 1996;93:5014-8.
13. Keeney S, Eker AP, Brody T, et al. Correction of the DNA repair defect in xeroderma pigmentosum group E by injection of a DNA damage-binding protein. Proc Natl Acad Sci U S A 1994;91:4053-6.
14. Wakasugi M, Kawashima A, Morioka H, et al. DDB accumulates at DNA damage sites immediately after UV irradiation and directly stimulates nucleotide excision repair. J Biol Chem 2002;277:1637-40.
15. Wang QE, Zhu Q, Wani G, Chen J, Wani AA. UV radiation-induced XPC translocation within chromatin is mediated by damaged-DNA binding protein DDB2. Carcinogenesis 2004;25:1033-43.
16. Datta A, Bagchi S, Nag A, et al. The p48 subunit of the damaged-DNA binding protein DDB associates with the CBP/p300 family of histone acetyltransferase. Mutat Res 2001;486:89-97.
17. Groisman R, Polanowska J, Kuraoka I, et al. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 2003;113:357-67.
18. Bohr VA, Smith CA, Okumoto DS, Hanawalt PC. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 1985;40:359-69.
19. Vreeswijk MP, van Hoffen A, Westland BE, Vrieling H, van Zeeland AA, Mullenders LHF. Analysis of repair of cyclobutane pyrimidine dimers and pyrimidine 6-4 pyrimidone photoproducts in transcriptionally active and inactive genes in Chinese hamster cells. J Biol Chem 1994;269:31858-63.
20. Cheo DL, Ruven HJ, Meira LB, et al. Characterization of defective nucleotide excision repair in XPC mutant mice. Mutat Res 1997;374:1-9.
21. Ruven HJ, Berg RJ, Seelen CM, et al. Ultraviolet-induced cyclobutane pyrimidine dimers are selectively removed from transcriptionally active genes in the epidermis of the hairless mouse. Cancer Res 1993;53:1642-5.
22. Tang JY, Hwang BJ, Ford JM, Hanawalt PC, Chu G. Xeroderma pigmentosum p48 gene enhances global genomic repair and suppresses UV-induced mutagenesis. Mol Cell 2000;5:737-44.
23. Tan T, Chu G. p53 binds and activates the xeroderma pigmentosum DDB2 gene in humans but not mice. Mol Cell Biol 2002;22:3247-54.
24. Itoh T, Cado D, Kamide R, Linn S. DDB2 gene disruption leads to skin tumors and resistance to apoptosis after exposure to ultraviolet light but not a chemical carcinogenesis. Proc Natl Acad Sci U S A 2004;101:2052-7.
25. Yoon T, Chakrabortty A, Franks R, Valli T, Kiyokawa H, Raychaudhuri P. Tumor-prone phenotype of the DDB2-deficient mice. Oncogene 2005;24:469-78.
26. Itoh T, O'Shea C, Linn S. Impaired regulation of tumor suppressor p53 caused by mutations in the xeroderma pigmentosum DDB2 gene: mutual regulatory interactions between p48 (DDB2) and p53. Mol Cell Biol 2003;23:7540-53.
27. Schul W, Jans J, Rijksen YM, et al. Enhanced repair of cyclobutane pyrimidine dimers and improved UV resistance in photolyase transgenic mice. EMBO J 2002;21:4719-29.
28. Nagy A, Gertsenstein M, Vintersten K, Behringer R. Manipulating the mouse embryo. A laboratory manual. 3rd ed. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2003.
29. Berg RJ, Rebel H, van der Horst GT, et al. Impact of global genome repair versus transcription-coupled repair on ultraviolet carcinogenesis in hairless mice. Cancer Res 2000;60:2858-63.
30. Rebel H, Mosnier LO, Berg RJ, et al. Early p53-positive foci as indicators of tumor risk in ultraviolet-exposed hairless mice: kinetics of induction effects of DNA repair deficiency and p53 heterozygosity. Cancer Res 2001;61:977-83.
31. Mimmack ML, Brooking J, Bahn S. Quantitative polymerase chain reaction: validation of microarray results from postmortem brain studies. Biol Psychiatry 2004;55:337-45.
32. Schreiber E, Matthias P, Müller MM, Schaffner W. Rapid detection of octamer binding proteins with "mini-extracts" prepared from a small number of cells. Nucleic Acids Res 1989;17:6419.
33. Venema J, van Hoffen A, Karcagi V, Natarajan AT, van Zeeland AA, Mullenders LHF. Xeroderma pigmentosum complementation group C cells remove pyrimidine dimers selectively from the transcribed strand of active genes. Mol Cell Biol 1991;11:4128-34.
34. Mone MJ, Volker M, Nikaido O, et al. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep 2001;2:1013-7.
35. Volker M, Mone MJ, Karmakar P, et al. Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell 2001;8:213-24.
36. 2 arrest and apoptosis in mouse epidermis. Proc Natl Acad Sci U S A 2000;97:11268-73.
37. de Gruijl FR. Health effects from solar UV radiation. Radiat Prot Dosimetry 1997;72:177-96.
38. Rapić-Otrin V, McLenigan MP, Bisi DC, Gonzalez M, Levine AS. Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res 2002;30:2588-98.
39. de Vries A, van Oostrom CT, Hofhuis FM, et al. Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 1995;377:169-73.
40. Kazantsev A, Bullock SK, Sancar A, Cordeiro-Stone M. Generation and characterization of an immortal cell line of xeroderma pigmentosum group E. Mutat Res 1998;407:55-65.
41. Rapic-Otrin V, Navazza V, Nardo T, et al. True XP group E patients have a defective UV-damaged DNA binding protein complex and mutations in DDB2 which reveal the functional domains of its p48 product. Hum Mol Genet 2003;12:1507-22.
42. Sun CL, Chao CC. Cross-resistance to death ligand-induced apoptosis in cisplatin-selected HeLa cells associated with overexpression of DDB2 and subsequent induction of cFLIP. Mol Pharmacol 2005;67:1307-14.
43. Lu YP, Lou YR, Peng QY, Xie JG, Conney AH. Stimulatory effect of topical application of caffeine on UVB-induced apoptosis in the epidermis of p53 and Bax knockout mice. Cancer Res 2004;64:5020-7.
44. Kanjilal S, Pierceall WE, Cummings KK, Kripke ML, Ananthaswamy HN. High frequency of p53 mutations in ultraviolet radiation-induced murine skin tumors: evidence for strand bias and tumor heterogeneity. Cancer Res 1993;53:2961-4.
45. Jans J, Schul W, Sert YG, et al. Powerful skin cancer protection by a CPD-photolyase transgene. Curr Biol 2005;15:105-15.
46. Gentil A, Le Page F, Margot A, Lawrence CW, Borden A, Sarasin A. Mutagenicity of a unique thymine-thymine dimer or thymine-thymine pyrimidine pyrimidone (6-4) photoproduct in mammalian cells. Nucleic Acids Res 1996;24:1837-40.
47. Riou L, Eveno E, van Hoffen A, van Zeeland AA, Sarasin A, Mullenders LHF. Differential repair of the two major UV-induced photolesions in trichothiodystrophy fibroblasts. Cancer Res 2004;64:889-94.
48. van der Horst GT, Meira L, Gorgels TG, et al. UVB radiation-induced cancer predisposition in Cockayne syndrome group A Csa mutant mice. DNA Repair 2002;1:143-57.