Effect of Atm Disruption on Spontaneously Arising and Radiation-Induced Deletion Mutations in Mouse Liver

Radiation Research

Volumn 160, Issue 5, 2003, Pages 549-558

  Furuno Fukushi, Ikuko ^a   Masumura, Ken Ichi ^b   Furuse, Takeshi ^a   Noda, Yuko ^a   Takahagi, Masahiko ^a   Saito, Toshiyuki ^a   Hoki, Yuko ^a   Suzuki, Hiroshi ^c,e   Wynshaw Boris, Anthony ^d   Nohmi, Takehiko ^b   Tatsumi, Kouichi ^a  

^a NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^c CHUGAI PHARMACEUTICAL CO LTD   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN;

ANIMAL TISSUE; ARTICLE; ATAXIA TELANGIECTASIA; ATM GENE; CELL CULTURE; DNA REPAIR; DOSE RESPONSE; FEMALE; GAM GENE; GENE; GENE DELETION; GENE DISRUPTION; GENE FUNCTION; GENE MUTATION; HOMOZYGOSITY; MALE; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIVITY; RED GENE; STRUCTURE ANALYSIS; TRANSGENIC MOUSE; WHOLE BODY RADIATION; X IRRADIATION; X RAY;

ANIMALS; ATAXIA TELANGIECTASIA; CELL CYCLE PROTEINS; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, RADIATION; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; LIVER; MALE; MICE; MICE, TRANSGENIC; MUTATION; PROTEIN-SERINE-THREONINE KINASES; RADIATION DOSAGE; RADIATION TOLERANCE; TUMOR SUPPRESSOR PROTEINS;

MUS MUSCULUS; UNIDENTIFIED SHUTTLE VECTOR;

EID: 0348226538     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/RR3073     Document Type: Article

References (74)

1. A. M. Taylor, D. G. Harnden, C. F. Arlett, S. A. Harcourt, A. R. Lehmann, S. Stevens and B. A. Bridges, Ataxia telangiectasia: A human mutation with abnormal radiation sensitivity. Nature 258, 427-429 (1975).
2. T. J. Jorgensen and Y. Shiloh, The ATM gene and the radiobiology of ataxia-telangiectasia. Int. J. Radiat. Biol. 69, 527-537 (1996).
3. Y. Shiloh, E. Tabor and Y. Becker, Cellular hypersensitivity to neocarzinostatin in ataxia-telangiectasia skin fibroblasts. Cancer Res. 42, 2247-2249 (1982).
4. A. Aurias, B. Dutrillaux, D. Buriot and J. Lejeune, High frequencies of inversions and translocations of chromosomes 7 and 14 in ataxia telangiectasia. Mutat. Res. 69, 369-374 (1980).
5. J. Cole and C. F. Arlett, Cloning efficiency and spontaneous mutant frequency in circulating T-Iymphocytes in ataxia-telangiectasia patients. Int. J. Radiat. Biol. 66, S123-S131 (1994).
6. W. L. Bigbee, R. G. Langlois, M. Swift and R. H. Jensen, Evidence for an elevated frequency of in vivo somatic cell mutations in ataxia telangiectasia. Am. J. Hum. Genet. 44, 402-408 (1989).
7. K. Savitsky, A. Bar-Shira, S. Gilad, G. Rotman, Y. Ziv, L. Vanagaite, D. A. Tagle, S. Smith, T. Uziel and Y. Shiloh, A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268, 1749-1753 (1995).
8. K. S. Keegan, D. A. Holtzman, A. W. Plug, E. R. Christenson, E. E. Brainerd, G. Flaggs, N. J. Bentley, E. M. Taylor, M. S. Meyn and M. F. Hoekstra, The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev. 10, 2423-2437 (1996).
9. Y. Shiloh, ATM and related protein kinases: Safeguarding genome integrity. Nat. Rev. Cancer 3, 155-168 (2003).
10. M. B. Kastan and D. S. Lim, The many substrates and functions of ATM. Nat. Rev. Mol. Cell Biol. 1, 179-186 (2000).
11. S. Banin, L. Moyal, S. Shieh, Y. Taya, C. W. Anderson, L. Chessa, N. I. Smorodinsky, C. Prives, Y. Reiss and Y. Ziv, Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281, 1674-1677 (1998).
12. C. E. Canman, D. S. Lim, K. A. Cimprich, Y. Taya, K. Tamai, K. Sakaguchi, E. Appella, M. B. Kastan and J. D. Siliciano, Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281, 1677-1679 (1998).
13. R. Maya, M. Balass, S. T. Kim, D. Shkedy, J. F. Leal, O. Shifman, M. Moas, T. Buschmann, Z. Ronai and M. Oren, ATM-dependent phosphorylation of Mdm2 on serine 395: Role in p53 activation by DNA damage. Genes Dev. 15, 1067-1077 (2001).
14. S. Matsuoka, G. Rotman, A. Ogawa, Y. Shiloh, K. Tamai and S. J. Elledge, Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc. Natl. Acad. Sci. USA 97, 10389-10394 (2000).
15. S. T. Kim, D. S. Lim, C. E. Canman and M. B. Kastan, Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274, 37538-37543 (1999).
16. D. Cortez, Y. Wang, J. Qin and S. J. Elledge, Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science 286, 1162-1166 (1999).
17. E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova and W. M. Bonner, DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868 (1998).
18. W. K. Kaufmann and R. S. Paules, DNA damage and cell cycle checkpoints. FASEB J. 10, 238-247 (1996).
19. R. Khosravi, R. Maya, T. Gottlieb, M. Oren, Y. Shiloh and D. Shkedy, Rapid ATM-dependent phosphorylation of MDM2 precedes p53 accumulation in response to DNA damage. Proc. Natl. Acad. Sci. USA 96, 14973-14977 (1999).
20. R. B. Painter and B. R. Young, Radiosensitivity in ataxia-telangiectasia: A new explanation. Proc. Natl. Acad. Sci. USA 77, 7315-7317 (1980).
21. D. S. Lim, S. T. Kim, B. Xu, R. S. Maser, J. Lin, J. H. Petrini and M. B. Kastan, ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404, 613-617 (2000).
22. S. Zhao, Y. C. Weng, S. S. Yuan, Y. T. Lin, H. C. Hsu, S. C. Lin, E. Gerbino, M. H. Song, M. Z. Zdzienicka and E. Y. Lee, Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405, 473-477 (2000).
23. A. G. Paulovich and L. H. Hartwell, A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82, 841-847 (1995).
24. H. D. Lindsay, D. J. Griffiths, R. J. Edwards, P. U. Christensen, J. M. Murray, F. Osman, N. Walworth and A. M. Carr, S-phase-specific activation of Cds1 kinase defines a subpathway of the checkpoint response in Schizosaccharomyces pombe. Genes Dev. 12, 382-395 (1998).
25. H. Beamish and M. F. Lavin, Radiosensitivity in ataxia-telangiectasia: Anomalies in radiation-induced cell cycle delay. Int. J. Radiat. Biol. 65, 175-184 (1994).
26. M. B. Kastan, Q. Zhan, W. S. el-Deiry, F. Carrier, T. Jacks, W. V. Walsh, B. S. Plunkett, B. Vogelstein and A. J. Fornace, Jr., A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71, 587-597 (1992).
27. M. N. Cornforth and J. S. Bedford, On the nature of a defect in cells from individuals with ataxia-telangiectasia. Science 227, 1589-1591 (1985).
28. S. E. Morgan, C. Lovly, T. K. Pandita, Y. Shiloh and M. B. Kastan, Fragments of ATM which have dominant-negative or complementing activity. Mol. Cell. Biol. 17, 2020-2029 (1997).
29. R. R. Weichselbaum, J. Nove and J. B. Little, Deficient recovery from potentially lethal radiation damage in ataxia telangiectasia and xeroderma pigmentosum. Nature 271, 261-262 (1978).
30. R. Cox, A cellular description of the repair defect in ataxia-telangiectasia. In Ataxia-Telangiectasia-A Cellular and Molecular Link between Cancer, Neuropathology, and Immune Deficiency (B. A. Bridges and D. G. Harnden, Eds.), pp. 141-153. Wiley, New York, 1982.
31. C. F. Arlett and A. Priestley, Defective recovery from potentially lethal damage in some human fibroblast cell strains. Int. J. Radiat. Biol. 43, 157-167 (1983).
32. P. Baumann and S. C. West, Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem. Sci. 23, 247-251 (1998).
33. G. C. Smith and S. P. Jackson, The DNA-dependent protein kinase. Genes Dev. 13, 916-934 (1999).
34. T. K. Pandita and W. N. Hittelman, Initial chromosome damage but not DNA damage is greater in ataxia telangiectasia cells. Radiat. Res. 130, 94-103 (1992).
35. G. Chen, S. S. Yuan, W. Liu, Y. Xu, K. Trujillo, B. Song, F. Cong, S. P. Goff, Y. Wu and E. Y. Lee, Radiation-induced assembly of Rad51 and Rad52 recombination complex requires ATM and c-Abl. J. Biol. Chem. 274, 12748-12752 (1999).
36. C. Morrison, E. Sonoda, N. Takao, A. Shinohara, K. Yamamoto and S. Takeda, The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J. 19, 463-471 (2000).
37. J. S. Lee, K. M. Collins, A. L. Brown, C. H. Lee and J. H. Chung, hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature 404, 201-204 (2000).
38. P. A. Jeggo, A. M. Carr and A. R. Lehmann, Splitting the ATM: Distinct repair and checkpoint defects in ataxia-telangiectasia. Trends Genet. 14, 312-316 (1998).
39. P. Formichi, C. Battisti, S. A. Tripodi, P. Tosi and A. Federico, Apoptotic response and cell cycle transition in ataxia telangiectasia cells exposed to oxidative stress. Life Sci. 66, 1893-1903 (2000).
40. J. Karlseder, D. Broccoli, Y. Dai, S. Hardy and T. de Lange, p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283, 1321-1325 (1999).
41. M. J. Chong, M. R. Murray, E. C. Gosink, H. R. Russell, A. Srinivasan, M. Kapsetaki, S. J. Korsmeyer and P. J. McKinnon, Atm and Bax cooperate in ionizing radiation-induced apoptosis in the central nervous system. Proc. Natl. Acad. Sci. USA 97, 889-894 (2000).
42. D. P. Harkin, J. M. Bean, D. Miklos, Y. H. Song, V. B. Truong, C. Englert, F. C. Christians, L. W. Ellisen, S. Maheswaran and D. A. Haber, Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA 1. Cell 97, 575-586 (1999).
43. C. H. Westphal, C. Schmaltz, S. Rowan, A. Elson, D. E. Fisher and P. Leder, Genetic interactions between atm and p53 influence cellular proliferation and irradiation-induced cell cycle checkpoints. Cancer Res. 57, 1664-1667 (1997).
44. C. Barlow, S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J. N. Crawley, T. Ried and A. Wynshaw-Boris, Atm-deficient mice: A paradigm of ataxia telangiectasia. Cell 86, 159-171 (1996).
45. N. Takao, Y. Li and K. Yamamoto, Protective roles for ATM in cellular response to oxidative stress. FEBS Lett. 472, 133-136 (2000).
46. V. M. Maher, D. J. Dorney, A. L. Mendrala, B. Konze-Thomas and J. J. McCormick, DNA excision-repair processes in human cells can eliminate the cytotoxic and mutagenic consequences of ultraviolet irradiation. Mutat. Res. 62, 311-323 (1979).
47. K. Tatsumi, M. Toyoda, T. Hashimoto, J. Furuyama, T. Kurihara, M. Inoue and H. Takebe, Differential hypersensitivity of xeroderma pigmentosum lymphoblastoid cell lines to ultraviolet light mutagenesis. Carcinogenesis 8, 53-57 (1987).
48. C. F. Arlett, Mutagenesis in repair-deficient human cell strains. In Progress in Environmental Mutagenesis (M. Alacevic, Ed.), pp. 161-174. Elsevier-North Holland, Amsterdam, 1980.
49. J. W. I. M. Simons, Studies on survival and mutation in ataxia-telangiectasia cells after X-irradiation under oxic and anoxic conditions. In Ataxia-telangiectasia - A Cellular and Molecular Link between Cancer, Neuropathology, and Immune Deficiency (B. A. Bridges and D. G. Harnden, Eds.), pp. 155-167. Wiley, London, 1982.
50. B. A. Bridges, Some DNA-repair-deficient human syndromes and their implications for human health. Proc. R. Soc. Lond. B Biol. Sci. 212, 263-278 (1981).
51. K. Tatsumi and H. Takebe, Gamma-irradiation induces mutation in ataxia-telangiectasia lymphoblastoid cells. Gann 75, 1040-1043 (1984).
52. A. Tachibana, T. Ohbayashi, H. Takebe and K. Tatsumi, Molecular changes in UV-induced and gamma-ray-induced mutations in human lymphoblastoid cells. Mutat. Res. 230, 159-166 (1990).
53. J. Thacker, J. Chalk, A. Ganesh and P. North, A mechanism for deletion formation in DNA by human cell extracts: the involvement of short sequence repeats. Nucleic Acids Res. 20, 6183-6188 (1992).
54. A. Tachibana, K. Tatsumi, I. Furuno-Fukushi and M. S. Sasaki, High frequency of deletions at the hypoxanthine-guanine phosphoribosyl-transferase locus in an ataxia-telangiectasia lymphoblastoid cell line irradiated with gamma-rays. Jpn. J. Cancer Res. 92, 1190-1198 (2001).
55. - and 6-thioguanine selections. Environ. Mol. Mutagen. 28, 465-470 (1996).
56. C. Barlow, M. Liyanage, P. B. Moens, M. Tarsounas, K. Nagashima, K. Brown, S. Rottinghaus, S. P. Jackson, D. Tagle and A. Wynshaw-Boris, Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development 125, 4007-4017 (1998).
57. K. Masumura, M. Matsui, M. Katoh, N. Horiya, O. Ueda, H. Tanabe, M. Yamada, H. Suzuki, T. Sofuni and T. Nohmi, Spectra of gpt mutations in ethylnitrosourea-treated and untreated transgenic mice. Environ. Mol. Mutagen. 34, 1-8 (1999).
58. E. J. Gunther, N. E. Murray and P. M. Glazer, High efficiency, restriction-deficient in vitro packaging extracts for bacteriophage lambda DNA using a new E. coli lysogen. Nucleic Acids Res. 21, 3903-3904 (1993).
59. W. W. Piegorsch, A. M. Lockhart, B. H. Margolin, K. R. Tindall, N. J. Gorelick, J. M. Short, G. J. Carr, E. D. Thompson and M. D. Shelby, Sources of variability in data from a lacI transgenic mouse mutation assay. Environ. Mol. Mutagen. 23, 17-31 (1994).
60. - selection: An efficient method to detect gamma-ray-induced deletions in transgenic mice. Environ. Mol. Mutagen. 34, 9-15 (1999).
61. - selection. Environ. Mol. Mutagen. 34, 106-111 (1999).
62. K. Masumura, K. Matsui, M. Yamada, M. Horiguchi, K. Ishida, M. Watanabe, K. Wakabayashi and T. Nohmi, Characterization of mutations induced by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine in the colon of gpt delta transgenic mouse: novel G:C deletions beside runs of identical bases. Carcinogenesis 21, 2049-2056 (2000).
63. L. S. Ripley, Frameshift mutation: Determinants of specificity. Annu. Rev. Genet. 24, 189-213 (1990).
64. E. M. Webber, J. C. Wu, L. Wang, G. Merlino and N. Fausto, Over-expression of transforming growth factor-alpha causes liver enlargement and increased hepatocyte proliferation in transgenic mice. Am. J. Pathol. 145, 398-408 (1994).
65. T. Sakamoto, Z. Liu, N. Murase, T. Ezure, S. Yokomuro, V. Poli and A. J. Demetris, Mitosis and apoptosis in the liver of interleukin-6-deficient mice after partial hepatectomy. Hepatology 29, 403-411 (1999).
66. J. A. Gossen, H. J. Martus, J. Y. Wei and J. Vijg, Spontaneous and X-ray-induced deletion mutations in a LacZ plasmid-based transgenic mouse model. Mutat. Res. 331, 89-97 (1995).
67. T. Ono, H. Ikehata, Y. Hosoi, B. S. Shung, A. Kurishita, X. Wang, K. Yamamoto, T. Suzuki and T. Sofuni, X-ray- and ultraviolet-radiation-induced mutations in Muta™ mouse. Radiat. Res. 148, 123-128 (1997).
68. 89Sr or the external gamma-ray irradiation. J. Radiat. Res. (Tokyo) 39, 53-60 (1998).
69. A. Klungland, I. Rosewell, S. Hollenbach, E. Larsen, G. Daly, B. Epe, E. Seeberg, T. Lindahl and D. E. Barnes, Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl. Acad. Sci. USA 96, 13300-13305 (1999).
70. T. Ono, H. Ikehata, S. Nakamura, Y. Saito, J. Komura, Y. Hosoi and K. Yamamoto, Molecular nature of mutations induced by a high dose of x-rays in spleen, liver, and brain of the lacZ-transgenic mouse. Environ. Mol. Mutagen. 34, 97-105 (1999).
71. K. P. Hoyes, P. J. Wadeson, H. L. Sharma, J. H. Hendry and I. D. Morris, Mutation studies in lacI transgenic mice after exposure to radiation or cyclophosphamide. Mutagenesis 13, 607-612 (1998).
72. R. A. Winegar, L. H. Lutze, J. D. Hamer, K. G. O'Loughlin and J. C. Mirsalis, Radiation-induced point mutations, deletions and micronuclei in lacI transgenic mice. Mutat. Res. 307, 479-487 (1994).
73. K. S. Tao, C. Urlando and J. A. Heddle, Comparison of somatic mutation in a transgenic versus host locus. Proc. Natl. Acad. Sci. USA 90, 10681-10685 (1993).
74. T. Hara, H. Sui, K. Kawakami, Y. Shimada and T. Shibuya, Partial hepatectomy strongly increased the mutagenicity of N-ethyl-N-nitro-sourea in Muta™ mouse liver. Environ. Mol. Mutagen. 34, 121-123 (1999).