Influences of p53 deficiency on the apoptotic response, DNA damage removal and mutagenesis in UVB-exposed mouse skin

Mutagenesis

Volumn 25, Issue 4, 2010, Pages 397-405

  Ikehata, Hironobu ^a   Okuyama, Ryuhei ^a,d   Ogawa, Eisaku ^a   Nakamura, Shingo ^a,e   Usami, Atsuko ^a   Mori, Toshio ^a,b   Tanaka, Kiyoji ^a,c   Aiba, Setsuya ^a   Ono, Tetsuya ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NARA MEDICAL UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e INSTITUTE FOR ENVIRONMENTAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; EPIDERMIS; EPIDERMIS HYPERPLASIA; EXCISION REPAIR; GENE MUTATION; GENOME; GENOTOXICITY; GENOTYPE; KNOCKOUT MOUSE; MALE; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RADIATION EXPOSURE; RADIATION INJURY; SKIN; SKIN DEFECT; ULTRAVIOLET B RADIATION; ANIMAL; DNA REPAIR; GENETICS; METABOLISM; MUTATION; PATHOLOGY; RADIATION RESPONSE; ULTRAVIOLET RADIATION;

MUS;

ANIMALS; APOPTOSIS; DNA DAMAGE; DNA REPAIR; MALE; MICE; MUTAGENESIS; MUTATION; SKIN; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

EID: 77954419686     PISSN: 02678357     EISSN: 14643804     Source Type: Journal    
DOI: 10.1093/mutage/geq019     Document Type: Article

References (48)

1. Nigro, J. M., Baker, S. J., Preisinger, A. C. et al. (1989) Mutations in the p53 gene occur in diverse human tumour types. Nature, 342, 705-708.
2. Brash, D. E., Rudolph, J. A., Simon, J. A., Lin, A., McKenna, G. J., Baden, H. P., Halperin, A. L. and Pontén, J. (1991) A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl Acad. Sci. USA, 88, 10124-10128 (Pubitemid 21915787)
3. De Gruijl, F. R. (1999) Skin cancer and solar UV radiation. Eur. J. Cancer, 35, 2003-2009.
4. Kraemer, K. H. (1997) Sunlight and skin cancer: another link revealed. Proc. Natl Acad. Sci. USA, 94, 11-14. (Pubitemid 27027155)
5. Bielas, J. H. and Heddle, J. A. (2004) Quiescent murine cells lack global genomic repair but are proficient in transcription-coupled repair. DNA Repair, 3, 711-717.
6. Konze-Thomas, B., Hazard, R. M., Maher, V. M. and McCormick, J. J. (1982) Extent of excision repair before DNA synthesis determines the mutagenic but not the lethal effect of UV radiation. Mutat. Res., 94, 421-434. (Pubitemid 12074549)
7. Carty, M. P., Hauser, J., Levine, A. S. and Dixon, K. (1993) Replication and mutagenesis of UV-damaged DNA templates in human and monkey cell extracts. Mol. Cell. Biol., 13, 533-542. (Pubitemid 23006930)
8. Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A. and Ellenberger, T. (2005) DNA Repair and Mutagenesis. 2nd edn. ASM Press, Washington, DC, USA.
9. Ford, J. M. and Hanawalt, P. C. (1995) Li-Fraumeni syndrome fibroblasts homozygous for p53 mutations are deficient in global DNA repair but exhibit normal transcription-coupled repair and enhanced UV resistance. Proc. Natl Acad. Sci. USA, 92, 8876-8880.
10. Ford, J. M. and Hanawalt, P. C. (1997) Expression of wild-type p53 is required for efficient global genomic nucleotide repair in UV-irradiated human fibroblasts. J. Biol. Chem., 272, 28073-28080.
11. El-Mahdy, M. A., Hamada, F. M., Wani, M. A., Zhu, Q. and Wani, A. A. (2000) p53-Degradation by HPV-16 E6 preferentially affects the removal of cyclobutane pyrimidine dimers from non-transcribed strand and sensitizes mammary epithelial cells to UV-irradiation. Mutat. Res., 459, 135-145. (Pubitemid 30139462)
12. Hwang, B. J., Ford, J. M., Hanawalt, P. C. and Chu, G. (1999) Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl Acad. Sci. USA, 96, 424-428. (Pubitemid 29061224)
13. Adimoolan, S. and Ford, J. M. (2002) p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc. Natl Acad. Sci. USA, 99, 12985-12990.
14. Smith, M. L., Ford, J. M., Hollander, M. C. et al. (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.
15. Rubbi, C. P. and Milner, J. (2003) p53 is a chromatin accessibility factor for nucleotide excision repair of DNA damage. EMBO J., 22, 975-986. (Pubitemid 36227799)
16. Lane, D. P. (1992) p53, guardian of the genome. Nature, 385, 15-16.
17. Lu, X. and Lane, D. P. (1993) Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndrome? Cell, 75, 765-778. (Pubitemid 2015642)
18. Olsen, W. M. (1988) Early cell kinetic effects of a single dose of monochromatic ultraviolet B irradiation on hairless mouse epidermis. J. Invest. Dermatol., 91, 585-589.
19. Danno, K. and Horio, T. (1987) Sunburn cell: factors involved in its formation. Photochem. Photobiol., 45, 683-690.
20. Cox, L. S. and Lane, D. P. (1995) Tumour suppressors, kinases and clamps: how p53 regulates the cell cycle in response to DNA damage. Bioessays, 17, 501-508.
21. Christmann, M., Tomicic, M. T., Origer, J. and Kaina, B. (2005) Fen1 is induced p53 dependently and involved in the recovery from UV-light-induced replication inhibition. Oncogene, 24, 8304-8313. (Pubitemid 43250922)
22. Ziegler, A., Jonason, A. S., Leffell, D. J., Simon, J. A., Sharma, H. W., Kimmelman, J., Remington, L., Jacks, T. and Brash, D. E. (1994) Sunburn and p53 in the onset of skin cancer. Nature, 372, 773-776.
23. McKay, B. C., Becerril, C. and Ljungman, M. (2001) P53 plays a protective role against UV-and cisplatin-induced apoptosis in transcription-coupled repair proficient fibroblasts. Oncogene, 20, 6805-6808. (Pubitemid 33020609)
24. De Santis, L. P., Balajee, A. S., Garcia, C. L., Pepe, G., Worboys, A. M. and Palitti, F. (2003) Inhibition of p53, p21 and Bax by pifithrin-a does not affect UV induced apoptotic response in CS-B cells. DNA Repair, 2, 891-900. (Pubitemid 37297453)
25. L reduction thereby enhancing UV-light induced apoptosis. Oncogene, 24, 5299-5312. (Pubitemid 43080100)
26. Clément, V., Dunand-Sauthier, I., Wiznerowicz, M. and Clarkson, S. G. (2007) UV-induced apoptosis in XPG-dependent fibroblasts involves activation of CD95 and caspases but not p53. DNA Repair, 6, 602-614. (Pubitemid 46518329)
27. Suzuki, T., Tsuzuku, J., Kawakami, K., Miyasaka, T. and Yamamoto, T. (2009) Proteasome-mediated degradation of Tob is pivotal for triggering UV-induced apoptosis. Oncogene, 28, 401-411.
28. Jiang, W., Ananthaswamy, H. N., Muller, H. K. and Kripke, M. L. (1999) p53 protects against skin cancer induction by UV-B radiation. Oncogene, 18, 4247-4253. (Pubitemid 29377855)
29. Gossen, J. A., de Leeuw, W. J. F., Tan, C. H. T., Zwarthoff, E. C., Berends, F., Lohman, P. H. M., Knook, D. L. and Vijg, J. (1989) Efficient rescue of integrated shuttle vectors from transgenic mice: a model for studying mutations in vivo. Proc. Natl Acad. Sci. USA, 86, 7971-7975. (Pubitemid 19265301)
30. Tsukada, T., Tomooka, Y., Takai, S. et al. (1993) Enhanced proliferative potential in culture of cells from p53-deficient mice. Oncogene, 8, 3313-3322. (Pubitemid 23342629)
31. Ohashi, M., Hatakeyama, K., Aizawa, S. and Kominami, R. (1996) p53 gene deficiency does not enhance instability of mouse minisatellites in somatic cells of normal tissues. Jpn. J. Cancer Res., 87, 696-701. (Pubitemid 26261690)
32. Ikehata, H., Yanase, F., Mori, T., Nikaido, O., Tanaka, K. and Ono, T. (2007) Mutation spectrum in UVB-induced skin epidermis of Xpa-knockout mice: frequent recovery of triplet mutations. Environ. Mol. Mutagen., 48, 1-13. (Pubitemid 46238553)
33. Ikehata, H. and Ono, T. (2002) Mutation induction with UVB in mouse skin epidermis is suppressed in acute high-dose exposure. Mutat. Res., 508, 41-47.
34. Cariello, N. F., Piegorsch, W. W., Adams, W. T. and Skopek, T. R. (1994) Computer program for the analysis of mutational spectra: application to p53 mutations. Carcinogenesis, 15, 2281-2285. (Pubitemid 24317493)
35. Tan, T. and Chu, G. (2002) p53 binds and activates the xeroderma pigmentosum DDB2 gene in humans but not mice. Mol. Cell. Biol., 22, 3247-3254. (Pubitemid 34453967)
36. Ikehata, H., Masuda, T., Sakata, H. and Ono, T. (2003) Analysis of mutation spectra in UVB-exposed mouse skin epidermis and dermis: frequent occurrence of C/T transition at methylated CpG-associated dipyrimidine sites. Environ. Mol. Mutagen., 41, 280-292. (Pubitemid 36529775)
37. Ikehata, H., Ono, T., Tanaka, K. and Todo, T. (2007) A model for triplet mutation formation based on error-prone translesional DNA synthesis opposite UV photolesions. DNA Repair, 6, 658-668. (Pubitemid 46518335)
38. Dumaz, N., Drougard, C., Sarasin, A. and Daya-Grosjean, L. (1993) Specific UV-induced mutation spectrum in the p53 gene of skin tumors from DNA-repair-deficient xeroderma pigmentosum patients. Proc. Natl Acad. Sci. USA, 90, 10529-10533. (Pubitemid 23347075)
39. Takeuchi, S., Nakatsu, Y., Nakane, H., Murai, H., Hirota, S., Kitamura, Y., Okuyama, A. and Tanaka, K. (1998) Strand specificity and absence of hot spots for p53 mutations in Ultraviolet B-induced skin tumors of XPA-deficient mice. Cancer Res., 58, 641-646. (Pubitemid 28099472)
40. Yuan, J., Yeasky, T. M., Havre, P. A. and Glazer, P. M. (1995) Induction of p53 in mouse cells decreases mutagenesis by UV radiation. Carcinogen-esis, 16, 2295-2300.
41. Corbet, S. W., Clarke, A. R., Gledhill, S. and Wyllie, A. H. (1999) P53-dependent and-independent links between DNA-damage, apoptosis and mutation frequency in ES cells. Oncogene, 18, 1537-1544. (Pubitemid 29108053)
42. Lu, Y., Lou, Y., Peng, Q., Xie, J. and Conney, A. H. (2004) Stimulatory effect of topical application of caffeine on UVB-induced apoptosis in the epidermis of p53 and Bax knockout mice. Cancer Res., 64, 5020-5027. (Pubitemid 38924551)
43. Knezevic, D., Zhang, W., Rochette, P. J. and Brash, D. E. (2007) Bcl-2 is the target of a UV-inducible apoptosis switch and a node for UV signaling. Proc. Natl Acad. Sci. USA, 104, 11286-11291. (Pubitemid 47175133)
44. Mathonnet, G., Léger, C., Desnoyers, J., Drouin, R., Therrien, J.-P. and Drobetsky, E. A. (2003) UV wavelength-dependent regulation of transcription-coupled nucleotide excision repair in p53-deficient human cells. Proc. Natl Acad. Sci. USA, 100, 7219-7224. (Pubitemid 36706419)
45. Wang, Q., Zhu, Q., Wani, M. A., Wani, G., Chen, J. and Wani, A. A. (2003) Tumor suppressor p53 dependent recruitment of nucleotide excision repair factors XPC and TFIIH to DNA damage. DNA Repair, 2, 483-499. (Pubitemid 36507120)
46. Bohr, V. A., Okumoto, D. S. and Hanawalt, P. C. (1986) Survival of UV-irradiated mammalian cells correlates with efficient DNA repair in an essential gene. Proc. Natl Acad. Sci. USA, 83, 3830-3833.
47. Ikehata, H.,Nakamura, S.,Asamura,T.andOno,T.(2004) Mutation spectrum in sunlight-exposed skin epidermis: small but appreciable contribution of oxidative stress-induced mutagenesis. Mutat. Res., 556, 11-24.
48. Ikehata, H., Kawai, K., Komura, J. et al. (2008) UVA1 genotoxicity is mediated not by oxidative damage but by cyclobutane pyrimidine dimers in normal mouse skin. J. Invest. Dermatol., 128, 2289-2296.