Involvement of 5-methylcytosine in sunlight-induced mutagenesis

Journal of Molecular Biology

Volumn 293, Issue 3, 1999, Pages 493-503

  You, Young Hyun ^a   Li, Chun ^a   Pfeifer, Gerd P ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

5 Methylcytosine; Mutations; Skin cancer; Sunlight; UV

Indexed keywords

5 METHYLCYTOSINE; PROTEIN P53; PYRIMIDINE DIMER;

ANIMAL CELL; ARTICLE; FIBROBLAST; GENE MUTATION; MOUSE; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; SKIN CANCER; SUN EXPOSURE; TRANSGENE; ULTRAVIOLET C RADIATION; ULTRAVIOLET RADIATION;

ANIMALIA; MAMMALIA;

EID: 0032732425     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3174     Document Type: Article

References (57)

1. Adams W. T., Skopek T. R. Statistical test for the comparison of samples from mutational spectra. J. Mol. Biol. 194:1987;391-396.
2. Ananthaswamy H. N., Fourtanier A., Evans R. L., Tison S., Medaisko C., Ullrich S. E., Kripke M. L. p53 Mutations in hairless SKH-hr1 mouse skin tumors induced by a solar simulator. Photochem. Photobiol. 67:1998;227-232.
3. Barak Y., Cohen-Fix O., Livneh Z. Deamination of cytosine-containing pyrimidine photodimers in UV-irradiated DNA. J. Biol. Chem. 270:1995;24174-24179.
4. Bodak N., Queille S., Avril M. F., Bouadjar B., Drougard C., Sarasin A., Daya-Grosjean L. High levels of patched gene mutations in basal-cell carcinomas from patients with xeroderma pigmentosum. Proc. Natl Acad. Sci. USA. 96:1999;5117-5122.
5. Brash D. E., Haseltine W. A. UV-induced mutation hotspots occur at DNA damage hotspots. Nature. 298:1982;189-192.
6. Brash D. E., Rudolph J. A., Simon J. A., Lin A., McKenna G. J., Baden H. P., Halperin A. J., Pontén J. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl Acad. Sci. USA. 88:1991;10124-10128.
7. Cariello N. F., Piegorsch W. W., Adams W. T., Skopek T. R. Computer program for the analysis of mutational spectra: application to p53 mutations. Carcinogenesis. 15:1994;2281-2285.
8. Chandrasekhar D., Van Houten B. High resolution mapping of UV-induced photoproducts in the Escherichia coli lacI gene. J. Mol. Biol. 238:1994;319-332.
9. Cleaver J. E. Xeroderma pigmentosum: a human disease in which an initial stage of DNA repair is defective. Proc. Natl Acad. Sci. USA. 63:1969;428-435.
10. de Boer J. G., Glickman B. W. The lacI gene as a target for mutation in transgenic rodents and Escherichia coli. Genetics. 148:1998;1441-1451.
11. de Gruijl F. R., Forbes P. D. UV-induced skin cancer in a hairless mouse model. Bioessays. 17:1995;651-660.
12. Denissenko M. F., Chen J. X., Tang M. S., Pfeifer G. P. Cytosine methylation determines hot spots of DNA damage in the human P53 gene. Proc. Natl Acad. Sci. USA. 94:1997;3893-3898.
13. Drouin R., Therrien J.-P. UVB-induced cyclobutane pyrimidine dimer frequency correlates with skin cancer mutational hotspots in p53. Photochem. Photobiol. 66:1997;719-726.
14. Dumaz N., Drougard C., Sarasin A., Daya-Grosjean L. Specific UV-induced mutation spectrum in the p53 gene of skin tumors from DNA-repair-deficient xeroderma pigmentosum patients. Proc. Natl Acad. Sci. USA. 90:1993;10529-10533.
15. Dumaz N., van Kranen H. J., de Vries A., Berg R. J., Wester P. W., van Kreijl C. F., Sarasin A., Daya-Grosjean L., de Gruijl F. R. The role of UV-B light in skin carcinogenesis through the analysis of p53 mutations in squamous cell carcinomas of hairless mice. Carcinogenesis. 18:1997;897-904.
16. Gibbs P. E. M., Lawrence C. W. U-U and T-T cyclobutane dimers have different mutational properties. Nucl. Acids Res. 21:1993;4059-4065.
17. Glickman B. W., Schaaper R. M., Haseltine W. A., Dunn R. L., Brash D. E. The C-C (6-4) UV photoproduct is mutagenic in Escherichia coli. Proc. Natl Acad. Sci. USA. 83:1986;6945-6949.
18. Hanawalt P. C., Sarasin A. Cancer-prone hereditary diseases with DNA processing abnormalities. Trends Genet. 2:1986;124-129.
19. Heddle J. A. On clonal expansion and its effects on mutant frequencies, mutation spectra and statistics for somatic mutations in vivo. Mutagenesis. 14:1999;257-260.
20. Horsfall M. J., Lawrence C. W. Accuracy of replication past the T-C (6-4) adduct. J. Mol. Biol. 235:1994;465-471.
21. Hsia H. C., Lebkowski J. S., Leong P. M., Calos M. P., Miller J. H. Comparison of ultraviolet irradiation-induced mutagenesis of the lacI gene in Escherichia coli and human 293 cells. J. Mol. Biol. 205:1989;103-113.
22. Jiang N., Taylor J.-S. In vivo evidence that UV-induced C-T mutations at dipyrimidine sites could result from the replicative bypass of cis-syn cyclobutane dimers or their deamination products. Biochemistry. 32:1993;472-481.
23. Jonason A. S., Kunala S., Price G. J., Restifo R. J., Spinelli H. M., Persing J. A., Leffell D. J., Tarone R. E., Brash D. E. Frequent clones of p53-mutated keratinocytes in normal human skin. Proc. Natl Acad. Sci. USA. 93:1996;14025-14029.
24. Jones P. A. DNA methylation errors and cancer. Cancer Res. 56:1996;2463-2467.
25. Koehler D. R., Awadallah S. S., Glickman B. W. Sites of preferential induction of cyclobutane pyrimidine dimers in the nontranscribed strand of lacI correspond with sites of UV-induced mutation in Escherichia coli. J. Biol. Chem. 266:1991;11766-11773.
26. Kraemer K. H. Sunlight and skin cancer: another link revealed. Proc. Natl Acad. Sci. USA. 94:1997;11-14.
27. LeClerc J. E., Christensen J. R., Tata P. V., Christensen R. B., Lawrence C. W. Ultraviolet light induces different spectra of lacI sequence changes in vegetative and conjugating cells of Escherichia coli. J. Mol. Biol. 203:1988;619-633.
28. Miller J. H. Mutagenic specificty of ultraviolet light. J. Mol. Biol. 182:1985;45-68.
29. Mitchell D. L., Nairn R. S. The biology of the (6-4) photoproduct. Photochem. Photobiol. 49:1989;805-819.
30. Nataraj A. J., Trent J. C. II, Ananthaswamy H. N. p53 gene mutations and photocarcinogenesis. Photochem. Photobiol. 62:1995;218-230.
31. Nishino H., Buettner V. L., Haavik J., Schaid D. J., Sommer S. S. Spontaneous mutation in Big Blue transgenic mice: Analysis of age, gender, and tissue type. Environ. Mol. Mutagen. 28:1996;299-312.
32. O'Neill J. P., Finette B. A. Transition mutations at CpG dinucleotides are the most frequent in vivo spontaneous single-base substitution mutation in the human HPRT gene. Environ. Mol. Mutagen. 32:1998;188-191.
33. Peng W., Shaw B. R. Accelerated deamination of cytosine residues in UV-induced cyclobutane pyrimidine dimers leads to CC to TT transitions. Biochemistry. 35:1996;10172-10181.
34. Pfeifer G. P. Formation and processing of UV photoproducts: effects of DNA sequence and chromatin environment. Photochem. Photobiol. 65:1997;270-283.
35. Pfeifer G. P., Drouin R., Riggs A. D., Holmquist G. P. In vivo mapping of a DNA adduct at nucleotide resolution: detection of pyrimidine (6-4) pyrimidone photoproducts by ligation-mediated polymerase chain reaction. Proc. Natl Acad. Sci. USA. 88:1991;1374-1378.
36. Provost G. S., Kretz P. L., Hamner R. T., Matthews C. D., Rogers B. J., Lundberg K. S., Dycaico M. J., Short J. M. Transgenic systems for in vivo mutation analysis. Mutat. Res. 288:1993;133-149.
37. Queille S., Seite S., Tison S., Medaisko C., Drougard C., Fourtanier A., Sarasin A., Daya-Grosjean L. p53 mutations in cutaneous lesions induced in the hairless mouse by a solar ultraviolet light simulator. Mol. Carcinogen. 22:1998;167-174.
38. Ren Z. P., Hedrum A., Pontén F., Nister M., Ahmadian A., Lundeberg J., Uhlén M., Pontén J. Human epidermal cancer and accompanying precursors have identical p53 mutations different from p53 mutations in adjacent areas of clonally expanded non-neoplastic keratinocytes. Oncogene. 12:1996;765-773.
39. Ruzcicska B. P., Lemaire D. G. E. DNA photochemistry. Horspool W. M., Song P.-S. CRC Handbook of Organic Photochemistry and Photobiology. 1995;1289-1317 CRC Press, Boca Raton.
40. Sage E., Lamolet B., Brulay E., Moustacchi E., Chteauneuf A., Drobetsky E. A. Mutagenic specificity of solar UV light in nucleotide excision repair- deficient rodent cells. Proc. Natl Acad. Sci. USA. 93:1996;176-180.
41. Schaaper R. M., Dunn R. L., Glickman B. W. Mechanisms of ultraviolet-induced mutation. Mutational spectra in the Escherichia coli lacI gene for a wild-type and an excision-repair-deficient strain. J. Mol. Biol. 198:1987;187-202.
42. Setlow R. B. The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc. Natl Acad. Sci. USA. 71:1974;3363-3366.
43. Setlow R. B., Carrier W. L. Pyrimidine dimers in ultraviolet-irradiated DNA's. J. Mol. Biol. 17:1966;237-254.
44. Skopek T., Marino D., Kort K., Miller J., Trumbauer M., Gopal S., Chen H. Effect of target gene CpG content on spontaneous mutation in transgenic mice. Mutat. Res. 400:1998;77-88.
45. Smith C. A., Wang M., Jiang N., Che L., Zhao X., Taylor J.-S. Mutation spectra of M13 vectors containing site-specific cis-syn, trans-syn-I, (6-4), and Dewar pyrimidone photoproducts of thymidylyl-(3′-5′)-thymidine in Escherichia coli under SOS conditions. Biochemistry. 35:1996;4146-4154.
46. Tessman I., Liu S. K., Kennedy M. A. Mechanism of SOS mutagenesis of UV-irradiated DNA: mostly error-free processing of deaminated cytosine. Proc. Natl Acad. Sci. USA. 89:1992;1159-1163.
47. Todd P. A., Glickman B. W. Mutational specificity of UV light in Escherichia coli: indications for a role of DNA secondary structure. Proc. Natl Acad. Sci. USA. 79:1982;4123-4127.
48. Tommasi S., Denissenko M. F., Pfeifer G. P. Sunlight induces pyrimidine dimers preferentially at 5-methylcytosine bases. Cancer Res. 57:1997;4727-4730.
49. Tornaletti S., Pfeifer G. P. Complete and tissue-independent methylation of CpG sites in the p53 gene: implications for mutations in human cancers. Oncogene. 10:1995a;1493-1499.
50. Tornaletti S., Pfeifer G. P. UV light as a footprinting agent: modulation of UV-induced DNA damage by transcription factors bound at the promoters of three human genes. J. Mol. Biol. 249:1995b;714-728.
51. Tu Y., Dammann R., Pfeifer G. P. Sequence and time-dependent deamination of cytosine bases in UV-B-induced cyclobutane pyrimidine dimers in vivo. J. Mol. Biol. 284:1998;297-311.
52. van Kranen H. J., de Gruijl F. R., de Vries A., Sontag Y., Wester P. W., Senden H. C., Rozemuller E., van Kreijl C. F. Frequent p53 alterations but low incidence of ras mutations in UV-B-induced skin tumors of hairless mice. Carcinogenesis. 16:1995;1141-1147.
53. Williams C., Pontén F., Ahmadian A., Ren Z. P., Ling G., Rollman O., Ljung A., Jaspers N. G., Uhlén M., Lundeberg J., Pontén J. Clones of normal keratinocytes and a variety of simultaneously present epidermal neoplastic lesions contain a multitude of p53 gene mutations in a xeroderma pigmentosum patient. Cancer Res. 58:1998;2449-2455.
54. Wood R. D., Skopek T. R., Hutchison F. Changes in DNA base sequence induced by targeted mutagenesis of lambda phage by ultraviolet light. J. Mol. Biol. 173:1984;273-291.
55. Yajima H., Takao M., Yasuhira S., Zhao J. H., Ishii C., Inoue H., Yasui A. A eukaryotic gene encoding an endonuclease that specifically repairs DNA damaged by ultraviolet light. EMBO J. 14:1995;2393-2399.
56. ® transgenic mouse. Mutat. Res. 420:1998;55-65.
57. Ziegler A., Jonason A. S., Leffell D. J., Simon J. A., Sharma H. W., Kimmelman J., Remington L., Jacks T., Brash D. E. Sunburn and p53 in the onset of skin cancer. Nature. 372:1994;773-776.