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Article

UV Radiation Induces Delayed Hyperrecombination Associated with Hypermutation in Human Cells

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Pages 6047-6055 | Received 14 Mar 2006, Accepted 02 Jun 2006, Published online: 27 Mar 2023

REFERENCES

  • Agar, N. S., G. M. Halliday, R. S. Barnetson, H. N. Ananthaswamy, M. Wheeler, and A. M. Jones. 2004. The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: a role for UVA in human skin carcinogenesis. Proc. Natl. Acad. Sci. USA 101:4954–4959.
  • Allen, C., C. A. Miller, and J. A. Nickoloff. 2003. The mutagenic potential of a single DNA double-strand break is not influenced by transcription. DNA Repair 2:1147–1156.
  • Arai, T., V. P. Kelly, O. Minowa, T. Noda, and S. Nishimura. 2002. High accumulation of oxidative DNA damage, 8-hydroxyguanine, in Mmh/Ogg1 deficient mice by chronic oxidative stress. Carcinogenesis 23:2005–2010.
  • Benjamin, M. B., and J. B. Little. 1992. X rays induce interallelic homologous recombination at the human thymidine kinase gene. Mol. Cell. Biol. 12:2730–2738.
  • Bjelland, S., and E. Seeberg. 2003. Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat. Res. 531:37–80.
  • Boyer, J. C., A. Umar, J. I. Risinger, J. R. Lipford, M. Kane, S. Yin, J. C. Barrett, R. D. Kolodner, and T. A. Kunkel. 1995. Microsatellite instability, mismatch repair deficiency, and genetic defects in human cancer cell lines. Cancer Res. 55:6063–6070.
  • Brash, D. E., J. A. Rudolph, J. A. Simon, A. Lin, G. J. McKenna, H. P. Baden, A. J. Halperin, and J. Ponten. 1991. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 88:10124–10128.
  • Brenneman, M. A. 2001. BRCA1 and BRCA2 in DNA repair and genome stability, p. 237–267. In J. A. Nickoloff and M. F. Hoekstra (ed.), DNA damage and repair, vol. 3: advances from phage to humans. Humana Press, Totowa, N.J.
  • Brose, M. S., P. Volpe, M. Feldman, M. Kumar, I. Rishi, R. Gerrero, E. Einhorn, M. Herlyn, J. Minna, A. Nicholson, J. A. Roth, S. M. Albelda, H. Davies, C. Cox, G. Brignell, P. Stephens, P. A. Futreal, R. Wooster, M. R. Stratton, and B. L. Weber. 2002. BRAF and RAS mutations in human lung cancer and melanoma. Cancer Res. 62:6997–7000.
  • Cao, J., S. E. DePrimo, and J. R. Stringer. 1997. Cell cycle dependence of radiation-induced homologous recombination in cultured monkey cells. Mutat. Res. 374:233–243.
  • Cariello, N. F., and T. R. Skopek. 1993. Analysis of mutations occurring at the human hprt locus. J. Mol. Biol. 231:41–57.
  • Chadwick, C. A., C. S. Potten, O. Nikaido, T. Matsunaga, C. Proby, and A. R. Young. 1995. The detection of cyclobutane thymine dimers, (6-4) photolesions and the Dewar photoisomers in sections of UV-irradiated human skin using specific antibodies, and the demonstration of depth penetration effects. J. Photochem. Photobiol. B 28:163–170.
  • Coates, P. J., S. A. Lorimore, and E. G. Wright. 2004. Damaging and protective cell signalling in the untargeted effects of ionizing radiation. Mutat. Res. 568:5–20.
  • Cornforth, M. N. 1989. On the nature of interactions leading to radiation-induced chromosomal exchange. Int. J. Radiat. Biol. 56:635–643.
  • Dahle, J., and E. Kvam. 2004. Increased level of oxidative stress in genomically unstable cell clones. J. Photochem. Photobiol. B 74:23–28.
  • Dahle, J., and E. Kvam. 2003. Induction of delayed mutations and chromosomal instability in fibroblasts after UVA-, UVB-, and X-radiation. Cancer Res. 63:1464–1469.
  • Dahle, J., E. Kvam, and T. Stokke. 2005. Bystander effects in UV-induced genomic instability: antioxidants inhibit delayed mutagenesis induced by ultraviolet A and B radiation. J. Carcinog. 4:11.
  • Dahle, J., P. Noordhuis, T. Stokke, D. H. Svendsrud, and E. Kvam. 2005. Multiplex polymerase chain reaction analysis of UV-A- and UV-B-induced delayed and early mutations in V79 Chinese hamster cells. Photochem. Photobiol. 81:114–119.
  • Davies, H., G. R. Bignell, C. Cox, P. Stephens, S. Edkins, S. Clegg, J. Teague, H. Woffendin, M. J. Garnett, W. Bottomley, N. Davis, E. Dicks, R. Ewing, Y. Floyd, K. Gray, S. Hall, R. Hawes, J. Hughes, V. Kosmidou, A. Menzies, C. Mould, A. Parker, C. Stevens, S. Watt, S. Hooper, R. Wilson, H. Jayatilake, B. A. Gusterson, C. Cooper, J. Shipley, D. Hargrave, K. Pritchard-Jones, N. Maitland, G. Chenevix-Trench, G. J. Riggins, D. D. Bigner, G. Palmieri, A. Cossu, A. Flanagan, A. Nicholson, J. W. Ho, S. Y. Leung, S. T. Yuen, B. L. Weber, H. F. Seigler, T. L. Darrow, H. Paterson, R. Marais, C. J. Marshall, R. Wooster, M. R. Stratton, and P. A. Futreal. 2002. Mutations of the BRAF gene in human cancer. Nature 417:949–954.
  • Denault, C. M., T. R. Skopek, and H. L. Liber. 1993. The effects of hypoxia and cysteamine on X-ray mutagenesis in human cells. II. hprt mRNA expression and cDNA sequence analysis of induced mutants. Radiat. Res. 136:271–279.
  • Deng, W. P., and J. A. Nickoloff. 1994. Preferential repair of UV damage in highly transcribed DNA diminishes UV-induced intrachromosomal recombination in mammalian cells. Mol. Cell. Biol. 14:391–399.
  • Devi, P. U., and M. Satyamitra. 2005. Tracing radiation induced genomic instability in vivo in the haemopoietic cells from fetus to adult mouse. Br. J. Radiol. 78:928–933.
  • Diaz-Llera, S., A. Podlutsky, A. M. Osterholm, S. M. Hou, and B. Lambert. 2000. Hydrogen peroxide induced mutations at the HPRT locus in primary human T-lymphocytes. Mutat. Res. 469:51–61.
  • Dowling, K., C. Seymour, and C. Mothersill. 2005. Delayed cell death and bystander effects in the progeny of Chinook salmon embryo cells exposed to radiation and a range of aquatic pollutants. Int. J. Radiat. Biol. 81:89–96.
  • Efrati, E., G. Tocco, R. Eritja, S. H. Wilson, and M. F. Goodman. 1999. “Action-at-a-distance” mutagenesis. 8-Oxo-7, 8-dihydro-2′-deoxyguanosine causes base substitution errors at neighboring template sites when copied by DNA polymerase beta. J. Biol. Chem. 274:15920–15926.
  • Eskandarpour, M., J. Hashemi, L. Kanter, U. Ringborg, A. Platz, and J. Hansson. 2003. Frequency of UV-inducible NRAS mutations in melanomas of patients with germline CDKN2A mutations. J. Natl. Cancer Inst. 95:790–798.
  • Friedberg, E. C. 2001. How nucleotide excision repair protects against cancer. Nat. Rev. Cancer 1:22–33.
  • Gebow, D., N. Miselis, and H. L. Liber. 2000. Homologous and nonhomologous recombination resulting in deletion: effects of p53 status, microhomology, and repetitive DNA length and orientation. Mol. Cell. Biol. 20:4028–4035.
  • Glaab, W. E., K. R. Tindall, and T. R. Skopek. 1999. Specificity of mutations induced by methyl methanesulfonate in mismatch repair-deficient human cancer cell lines. Mutat. Res. 427:67–78.
  • Glaviano, A., V. Nayak, E. Cabuy, D. M. Baird, Z. Yin, R. Newson, D. Ladon, M. A. Rubio, P. Slijepcevic, F. Lyng, C. Mothersill, and C. P. Case. 2006. Effects of hTERT on metal ion-induced genomic instability. Oncogene 25:3424–3435.
  • Goss, K. H., M. A. Risinger, J. J. Kordich, M. M. Sanz, J. E. Straughen, L. E. Slovek, A. J. Capobianco, J. German, G. P. Boivin, and J. Groden. 2002. Enhanced tumor formation in mice heterozygous for Blm mutation. Science 297:2051–2053.
  • Hickson, I. D. 2003. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3:169–178.
  • Huang, L., S. Grim, L. E. Smith, P. M. Kim, J. A. Nickoloff, O. G. Goloubeva, and W. F. Morgan. 2004. Ionizing radiation induces delayed hyperrecombination in mammalian cells. Mol. Cell. Biol. 24:5060–5068.
  • Kino, K., and H. Sugiyama. 2005. UVR-induced G-C to C-G transversions from oxidative DNA damage. Mutat. Res. 571:33–42.
  • Klungland, A., I. Rosewell, S. Hollenbach, E. Larsen, G. Daly, B. Epe, E. Seeberg, T. Lindahl, and D. E. Barnes. 1999. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl. Acad. Sci. USA 96:13300–13305.
  • Kolodner, R. D. 1995. Mismatch repair: mechanisms and relationship to cancer susceptibility. Trends Biochem. Sci. 20:397–401.
  • Kvam, E., and R. M. Tyrrell. 1997. Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation. Carcinogenesis 18:2379–2384.
  • Lankinen, M. H., L. M. Vilpo, and J. A. Vilpo. 1996. UV- and gamma-irradiation-induced DNA single-strand breaks and their repair in human blood granulocytes and lymphocytes. Mutat. Res. 352:31–38.
  • Larsen, E., K. Reite, G. Nesse, C. Gran, E. Seeberg, and A. Klungland. 2006. Repair and mutagenesis at oxidized DNA lesions in the developing brain of wild-type and Ogg1−/− mice. Oncogene 25:2425–2432.
  • Liber, H. L., and E. N. Phillips. 1998. Interrelationships between radiation-induced mutations and modifications in gene expression linked to cancer. Crit. Rev. Eukaryot. Gene Expr. 8:257–276.
  • Liber, H. L., D. W. Yandell, and J. B. Little. 1989. A comparison of mutation induction at the tk and hprt loci in human lymphoblastoid cells; quantitative differences are due to an additional class of mutations at the autosomal tk locus. Mutat. Res. 216:9–17.
  • Limoli, C. L., E. Giedzinski, W. M. Bonner, and J. E. Cleaver. 2002. UV-induced replication arrest in the xeroderma pigmentosum variant leads to DNA double-strand breaks, γ-H2AX formation, and Mre11 relocalization. Proc. Natl. Acad. Sci. USA 99:233–238.
  • Lin, Y., and A. S. Waldman. 2001. Capture of DNA sequences at double-strand breaks in mammalian chromosomes. Genetics 158:1665–1674.
  • Little, J. B., H. Nagasawa, T. Pfenning, and H. Vetrovs. 1997. Radiation-induced genomic instability: delayed mutagenic and cytogenetic effects of x-rays and α-particles. Radiat. Res. 148:299–307.
  • Little, K. C., and P. Chartrand. 2004. Genomic DNA is captured and amplified during double-strand break (DSB) repair in human cells. Oncogene 23:4166–4172.
  • Lutsenko, E. A., J. M. Carcamo, and D. W. Golde. 2002. Vitamin C prevents DNA mutation induced by oxidative stress. J. Biol. Chem. 277:16895–16899.
  • Marder, B. A., and W. F. Morgan. 1993. Delayed chromosomal instability induced by DNA damage. Mol. Cell. Biol. 13:6667–6677.
  • Morgan, W. F. 2003. Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation? Oncogene 22:7094–7099.
  • Morgan, W. F. 2003. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat. Res. 159:567–580.
  • Morgan, W. F. 2003. Non-targeted and delayed effects of exposure to ionizing radiation: II. Radiation-induced genomic instability and bystander effects in vivo, clastogenic factors and transgenerational effects. Radiat. Res. 159:581–596.
  • Myung, K., A. Datta, C. Chen, and R. D. Kolodner. 2001. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat. Genet. 27:113–116.
  • Nagar, S., L. E. Smith, and W. F. Morgan. 2005. Variation in apoptosis profiles in radiation-induced genomically unstable cell lines. Radiat. Res. 163:324–331.
  • Nickoloff, J. A. 2002. Recombination: mechanisms and roles in tumorigenesis, p. 49–59. In J. R. Bertino (ed.), Encyclopedia of cancer, 2nd ed., vol. 4. Elsevier Science, San Diego, Calif.
  • Papp, T., H. Pemsel, R. Zimmermann, R. Bastrop, D. G. Weiss, and D. Schiffmann. 1999. Mutational analysis of the N-ras, p53, p16INK4a, CDK4, and MC1R genes in human congenital melanocytic naevi. J. Med. Genet. 36:610–614.
  • Pascucci, B., A. Versteegh, A. van Hoffen, A. A. van Zeeland, L. H. Mullenders, and E. Dogliotti. 1997. DNA repair of UV photoproducts and mutagenesis in human mitochondrial DNA. J. Mol. Biol. 273:417–427.
  • Pfeifer, G. P., Y. H. You, and A. Besaratinia. 2005. Mutations induced by ultraviolet light. Mutat. Res. 571:19–31.
  • Prakash, S., R. E. Johnson, and L. Prakash. 2005. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74:317–353.
  • Sekiguchi, M., and T. Tsuzuki. 2002. Oxidative nucleotide damage: consequences and prevention. Oncogene 21:8895–8904.
  • Shi, H., L. G. Hudson, W. Ding, S. Wang, K. L. Cooper, S. Liu, Y. Chen, X. Shi, and K. J. Liu. 2004. Arsenite causes DNA damage in keratinocytes via generation of hydroxyl radicals. Chem. Res. Toxicol. 17:871–878.
  • Somodi, Z., N. A. Zyuzikov, G. Kashino, K. R. Trott, and K. M. Prise. 2005. Radiation-induced genomic instability in repair deficient mutants of Chinese hamster cells. Int. J. Radiat. Biol. 81:929–936.
  • Stamato, T. D., and M. L. Perez. 1998. EMS and UV-light-induced colony sectoring and delayed mutation in Chinese hamster cells. Int. J. Radiat. Biol. 74:739–745.
  • Stamato, T. D., E. Richardson, and M. L. Perez. 1995. UV-light induces delayed mutations in Chinese hamster cells. Mutat. Res. 328:175–181.
  • Storz, P., H. Doppler, and A. Toker. 2005. Protein kinase D mediates mitochondrion-to-nucleus signaling and detoxification from mitochondrial reactive oxygen species. Mol. Cell. Biol. 25:8520–8530.
  • Suzuki, K., M. Ojima, S. Kodama, and M. Watanabe. 2003. Radiation-induced DNA damage and delayed induced genomic instability. Oncogene 22:6988–6993.
  • Tauchi, H., S. Matsuura, J. Kobayashi, S. Sakamoto, and K. Komatsu. 2002. Nijmegen breakage syndrome gene, NBS1, and molecular links to factors for genome stability. Oncogene 58:8967–8980.
  • Tornaletti, S., D. Rozek, and G. P. Pfeifer. 1993. The distribution of UV photoproducts along the human p53 gene and its relation to mutations in skin cancer. Oncogene 8:2051–2057.
  • Tutt, A., D. Bertwistle, J. Valentine, A. Gabriel, S. Swift, G. Ross, C. Griffin, J. Thacker, and A. Ashworth. 2001. Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J. 20:4704–4716.
  • Vreeswijk, M. P., A. van Hoffen, B. E. Westland, H. Vrieling, A. A. van Zeeland, and L. H. Mullenders. 1994. 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. 269:31858–31863.
  • Ward, J. 1998. The nature of lesions formed by ionizing radiation, p. 65–84. In J. A. Nickoloff and M. F. Hoekstra (ed.), DNA damage and repair: DNA repair in higher eukaryotes, vol. 2. Humana Press, Totowa, N.J.
  • Winn, L. M., P. M. Kim, and J. A. Nickoloff. 2003. Oxidative stress-induced homologous recombination as a novel mechanism for phenytoin-initiated toxicity. J. Pharmacol. Exp. Ther. 306:523–527.

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