Indirect mechanisms of genomic instability and the biological significance of mutations at tandem repeat loci

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 598, Issue 1-2, 2006, Pages 61-72

  Niwa, Ohtsura ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

ESTR; Genomic instability; p53; Pink eyed unstable allele; Repeat mutations

Indexed keywords

ALKYLATING AGENT; MITOMYCIN C; PROTEIN P53;

ALLELE; ARTICLE; CHROMATID; CHROMOSOME ABERRATION; DNA DAMAGE; DNA REPLICATION; DNA SEQUENCE; DNA STRAND BREAKAGE; DNA STRUCTURE; DNA SYNTHESIS; ENZYME ACTIVITY; EUKARYOTE; GENE DELETION; GENE MUTATION; GENE SEQUENCE; GENETIC DISORDER; GENOMIC INSTABILITY; GENOTYPE; HUMAN; IONIZING RADIATION; IRRADIATION; MEIOSIS; MITOSIS; MOUSE STRAIN; NEUROMUSCULAR DISEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RADIATION INJURY; RAT STRAIN; RNA INTERFERENCE; SISTER CHROMATID; SPERM; SPERMATOGENESIS; SPERMATOGONIUM; TANDEM REPEAT; VARIABLE NUMBER OF TANDEM REPEAT; ZYGOTE;

CHROMOSOME ABERRATIONS; DNA DAMAGE; DNA REPLICATION; GENES, P53; GENOMIC INSTABILITY; HUMANS; MALE; MICE; MUTATION; SPERMATOGENESIS; TANDEM REPEAT SEQUENCES;

EID: 33744903912     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2006.01.015     Document Type: Article

References (86)

1. Friedberg E.C., Walker G.C., and Siede W. DNA Repair and Mutagenesis (1995), ASM Press, Washington, DC pp. 59-61
2. Little J.B. Genomic instability and bystander effects: a historical perspective. Oncogene 22 (2003) 6978-6987
3. Morgan W.F. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat. Res. 159 (2003) 567-580
4. Fischhaber P.L., and Friedberg E.C. How are specialized (low-fidelity) eukaryotic polymerases selected and switched with high-fidelity polymerases during translesion DNA synthesis?. DNA Repair (Amst) 4 (2005) 279-283
5. Auerbach C. Mutat. Res. (1976)
6. Witkin E.M. Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol. Rev. 40 (1976) 869-907
7. Ohmori H., Friedberg E.C., Fuchs R.P., Goodman M.F., Hanaoka F., Hinkle D., Kunkel T.A., Lawrence C.W., Livneh Z., Nohmi T., Prakash L., Prakash S., Todo T., Walker G.C., Wang Z., and Woodgate R. The Y-family of DNA polymerases. Mol. Cell 8 (2001) 7-8
8. Fabre F., and Roman H. Genetic evidence for inducibility of recombination competence in yeast. Proc. Natl. Acad. Sci. USA 74 (1977) 1667-1671
9. Bridges B.A. Radiation and germline mutation at repeat sequences: are we in the middle of a paradigm shift?. Radiat. Res. 156 (2001) 631-641
10. Russell W.L., and Kelly E.M. Mutation frequencies in male mice and the estimation of genetic hazards of radiation in men. Proc. Natl. Acad. Sci. USA 79 (1982) 542-544
11. Eichler E.E. Repetitive conundrums of centromere structure and function. Hum. Mol. Genet. 8 (1999) 151-155
12. Collins K. Mammalian telomeres and telomerase. Curr. Opin. Cell. Biol. 12 (2000) 378-383
13. Blasco M.A. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6 (2005) 611-622
14. Richards R.I. Dynamic mutations: a decade of unstable expanded repeats in human genetic disease. Hum. Mol. Genet. 10 (2001) 2187-2194
15. Cleary J.D., and Pearson C.E. Replication fork dynamics and dynamic mutations: the fork-shift model of repeat instability. Trends Genet. 21 (2005) 272-280
16. Hunter J.M., Crouse A.B., Lesort M., Johnson G.V., and Detloff P.J. Verification of somatic CAG repeat expansion by pre-PCR fractionation. J. Neurosci. Methods 144 (2005) 11-17
17. Wyman A.R., and White R. A highly polymorphic locus in human DNA. Proc. Natl. Acad. Sci. USA 77 (1980) 6754-6758
18. Jeffreys A.J., Wilson V., and Thein S.L. Hypervariable 'minisatellite' regions in human DNA. Nature 314 (1985) 67-73
19. Jeffreys A.J. Spontaneous and induced minisatellite instability in the human genome. Clin. Sci. (London) 93 (1997) 383-390
20. Buard J., Shone A.C., and Jeffreys A.J. Meiotic recombination and flanking marker exchange at the highly unstable human minisatellite CEB1 (D2S90). Am. J. Hum. Genet. 67 (2000) 333-344
21. Jeffreys A.J., and Neumann R. Somatic mutation processes at a human minisatellite. Hum. Mol. Genet. 6 (1997) 129-132, 134-126
22. Kelly R., Bulfield G., Collick A., Gibbs M., and Jeffreys A.J. Characterization of a highly unstable mouse minisatellite locus: evidence for somatic mutation during early development. Genomics 5 (1989) 844-856
23. Mitani K., Takahashi Y., and Kominami R. A GGCAGG motif in minisatellites affecting their germline instability. J. Biol. Chem. 265 (1990) 15203-15210
24. Bois P.R., Southgate L., and Jeffreys A.J. Length of uninterrupted repeats determines instability at the unstable mouse expanded simple tandem repeat family MMS10 derived from independent SINE B1 elements. Mamm. Genome 12 (2001) 104-111
25. Yauk C.L. Advances in the application of germline tandem repeat instability for in situ monitoring. Mutat. Res. 566 (2004) 169-182
26. Paquette B., and Little J.B. In vivo enhancement of genomic instability in minisatellite sequences of mouse C3H/10T1/2 cells transformed in vitro by X-rays. Cancer Res. 54 (1994) 3173-3178
27. Niwa O., Kamiya K., Furihata C., Nitta Y., Wang Z., Fan Y.J., Ninomiya Y., Kotomura N., Numoto M., and Kominami R. Association of minisatellite instability with c-myc amplification and K-ras mutation in methylcholanthrene-induced mouse sarcomas. Cancer Res. 55 (1995) 5670-5676
28. Imai H., Nakagama H., Komatsu K., Shiraishi T., Fukuda H., Sugimura T., and Nagao M. Minisatellite instability in severe combined immunodeficiency mouse cells. Proc. Natl. Acad. Sci. USA 94 (1997) 10817-10820
29. Dubrova Y.E., Jeffreys A.J., and Malashenko A.M. Mouse minisatellite mutations induced by ionizing radiation. Nat. Genet. 5 (1993) 92-94
30. Sadamoto S., Suzuki S., Kamiya K., Kominami R., Dohi K., and Niwa O. Radiation induction of germline mutation at a hypervariable mouse minisatellite locus. Int. J. Radiat. Biol. 65 (1994) 549-557
31. Kodaira M., Satoh C., Hiyama K., and Toyama K. Lack of effects of atomic bomb radiation on genetic instability of tandem-repetitive elements in human germ cells. Am. J. Hum. Genet. 57 (1995) 1275-1283
32. Dubrova Y.E., Nesterov V.N., Krouchinsky N.G., Ostapenko V.A., Neumann R., Neil D.L., and Jeffreys A.J. Human minisatellite mutation rate after the Chernobyl accident. Nature 380 (1996) 683-686
33. Gondo Y., Gardner J.M., Nakatsu Y., Durham-Pierre D., Deveau S.A., Kuper C., and Brilliant M.H. High-frequency genetic reversion mediated by a DNA duplication: the mouse pink-eyed unstable mutation. Proc. Natl. Acad. Sci. USA 90 (1993) 297-301
34. Brilliant M.H., King R., Francke U., Schuffenhauer S., Meitinger T., Gardner J.M., Durham-Pierre D., and Nakatsu Y. The mouse pink-eyed dilution gene: association with hypopigmentation in Prader-Willi and Angelman syndromes and with human OCA2. Pigment Cell Res. 7 (1994) 398-402
35. Schiestl R.H., Khogali F., and Carls N. Reversion of the mouse pink-eyed unstable mutation induced by low doses of X-rays. Science 266 (1994) 1573-1576
36. Niwa O. Induced genomic instability in irradiated germ cells and in the offspring; reconciling discrepancies among the human and animal studies. Oncogene 22 (2003) 7078-7086
37. Russell W.L., Bangham J.W., and Russell L.B. Differential response of mouse male germ-cell stages to radiation-induced specific-locus and dominant mutations. Genetics 148 (1998) 1567-1578
38. Nomura T. Parental exposure to X rays and chemicals induces heritable tumours and anomalies in mice. Nature 296 (1982) 575-577
39. Dubrova Y.E., Plumb M., Brown J., Fennelly J., Bois P., Goodhead D., and Jeffreys A.J. Stage specificity, dose response, and doubling dose for mouse minisatellite germ-line mutation induced by acute radiation. Proc. Natl. Acad. Sci. USA 95 (1998) 6251-6255
40. Barber R., Plumb M., Smith A.G., Cesar C.E., Boulton E., Jeffreys A.J., and Dubrova Y.E. No correlation between germline mutation at repeat DNA and meiotic crossover in male mice exposed to X-rays or cisplatin. Mutat. Res. 457 (2000) 79-91
41. Vilarino-Guell C., Smith A.G., and Dubrova Y.E. Germline mutation induction at mouse repeat DNA loci by chemical mutagens. Mutat. Res. 526 (2003) 63-73
42. Sotomayor R.E., and Sega G.A. Unscheduled DNA synthesis assay in mammalian spermatogenic cells: an update. Environ. Mol. Mutagen. 36 (2000) 255-265
43. Matsuda Y., Tobari I., Maemori M., and Seki N. Mechanism of chromosome aberration induction in the mouse egg fertilized with sperm recovered from postmeiotic germ cells treated with methyl methanesulfonate. Mutat. Res. 214 (1989) 165-180
44. Fan Y.J., Wang Z., Sadamoto S., Ninomiya Y., Kotomura N., Kamiya K., Dohi K., Kominami R., and Niwa O. Dose-response of a radiation induction of a germline mutation at a hypervariable mouse minisatellite locus. Int. J. Radiat. Biol. 68 (1995) 177-183
45. Niwa O., Fan Y.J., Numoto M., Kamiya K., and Kominami R. Induction of a germline mutation at a hypervariable mouse minisatellite locus by 252Cf radiation. J. Radiat. Res. (Tokyo) 37 (1996) 217-224
46. Shimura T., Inoue M., Taga M., Shiraishi K., Uematsu N., Takei N., Yuan Z.M., Shinohara T., and Niwa O. p53-Dependent S-phase damage checkpoint and pronuclear cross talk in mouse zygotes with X-irradiated sperm. Mol. Cell. Biol. 22 (2002) 2220-2228
47. Matsuda Y., and Tobari I. Chromosomal analysis in mouse eggs fertilized in vitro with sperm exposed to ultraviolet light (UV) and methyl and ethyl methanesulfonate (MMS and EMS). Mutat. Res. 198 (1988) 131-144
48. Matsuda Y., Seki N., Utsugi-Takeuchi T., and Tobari I. X-ray- and mitomycin C (MMC)-induced chromosome aberrations in spermiogenic germ cells and the repair capacity of mouse eggs for the X-ray and MMC damage. Mutat. Res. 211 (1989) 65-75
49. Matsuda Y., and Tobari I. Repair capacity of fertilized mouse eggs for X-ray damage induced in sperm and mature oocytes. Mutat. Res. 210 (1989) 35-47
50. Zhou X.Y., Wang X., Hu B., Guan J., Iliakis G., and Wang Y. An ATM-independent S-phase checkpoint response involves CHK1 pathway. Cancer Res. 62 (2002) 1598-1603
51. Suzuki S., Mitani K., Kuwabara K., Takahashi Y., Niwa O., and Kominami R. Two mouse hypervariable minisatellites: chromosomal location and simultaneous mutation. J. Biochem. (Tokyo) 114 (1993) 292-296
52. Dubrova Y.E., Plumb M., Brown J., and Jeffreys A.J. Radiation-induced germline instability at minisatellite loci. Int. J. Radiat. Biol. 74 (1998) 689-696
53. Yauk C.L., Dubrova Y.E., Grant G.R., and Jeffreys A.J. A novel single molecule analysis of spontaneous and radiation-induced mutation at a mouse tandem repeat locus. Mutat. Res. 500 (2002) 147-156
54. Niwa O., and Kominami R. Untargeted mutation of the maternally derived mouse hypervariable minisatellite allele in F1 mice born to irradiated spermatozoa. Proc. Natl. Acad. Sci. USA 98 (2001) 1705-1710
55. Gibbs M., Collick A., Kelly R.G., and Jeffreys A.J. A tetranucleotide repeat mouse minisatellite displaying substantial somatic instability during early preimplantation development. Genomics 17 (1993) 121-128
56. Shiraishi K., Shimura T., Taga M., Uematsu N., Gondo Y., Ohtaki M., Kominami R., and Niwa O. Persistent induction of somatic reversions of the pink-eyed unstable mutation in F1 mice born to fathers irradiated at the spermatozoa stage. Radiat. Res. 157 (2002) 661-667
57. Ohashi M., Hatakeyama K., Aizawa S., and Kominami R. p53 Gene deficiency does not enhance instability of mouse minisatellites in somatic cells of normal tissues. Jpn. J. Cancer Res. 87 (1996) 696-701
58. Aubrecht J., Secretan M.B., Bishop A.J., and Schiestl R.H. Involvement of p53 in X-ray induced intrachromosomal recombination in mice. Carcinogenesis 20 (1999) 2229-2236
59. Bishop A.J., Hollander M.C., Kosaras B., Sidman R.L., Fornace Jr. A.J., and Schiestl R.H. Atm-, p53-, and Gadd45a-deficient mice show an increased frequency of homologous recombination at different stages during development. Cancer Res. 63 (2003) 5335-5343
60. Burr K.L., Smith A.G., and Dubrova Y.E. p53 Deficiency does not affect mutation rate in the mouse germline. Oncogene 24 (2005) 4315-4318
61. Iliakis G., Wang Y., Guan J., and Wang H. DNA dama ge checkpoint control in cells exposed to ionizing radiation. Oncogene 22 (2003) 5834-5847
62. Kobayashi J., Antoccia A., Tauchi H., Matsuura S., and Komatsu K. NBS1 and its functional role in the DNA damage response. DNA Repair (Amst) 3 (2004) 855-861
63. Kastan M.B., Lim D.S., Kim S.T., and Yang D. ATM-a key determinant of multiple cellular responses to irradiation. Acta Oncol. 40 (2001) 686-688
64. Lee J.H., and Paull T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308 (2005) 551-554
65. Toyoshima M., Shimura T., Adiga S.K., Taga M., Shiraishi K., Inoue M., Yuan Z.M., and Niwa O. Transcription-independent suppression of DNA synthesis by p53 in sperm-irradiated mouse zygotes. Oncogene 24 (2005) 3229-3235
66. Fei P., and El-Deiry W.S. p53 and radiation responses. Oncogene 22 (2003) 5774-5783
67. Agarwal M.L., Agarwal A., Taylor W.R., Chernova O., Sharma Y., and Stark G.R. A p53-dependent S-phase checkpoint helps to protect cells from DNA damage in response to starvation for pyrimidine nucleotides. Proc. Natl. Acad. Sci. USA 95 (1998) 14775-14780
68. Harrouk W., Codrington A., Vinson R., Robaire B., and Hales B.F. Paternal exposure to cyclophosphamide induces DNA damage and alters the expression of DNA repair genes in the rat preimplantation embryo. Mutat. Res. 461 (2000) 229-241
69. Raff J.W., and Glover D.M. Nuclear and cytoplasmic mitotic cycles continue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin. J. Cell Biol. 107 (1988) 2009-2019
70. Ikegami R., Rivera-Bennetts A.K., Brooker D.L., and Yager T.D. Effect of inhibitors of DNA replication on early zebrafish embryos: evidence for coordinate activation of multiple intrinsic cell-cycle checkpoints at the mid-blastula transition. Zygote 5 (1997) 153-175
71. Clute P., and Masui Y. Microtubule dependence of chromosome cycles in Xenopus laevis blastomeres under the influence of a DNA synthesis inhibitor, aphidicolin. Dev. Biol. 185 (1997) 1-13
72. Jeong Y.J., Choi H.W., Shin H.S., Cui X.S., Kim N.H., Gerton G.L., and Jun J.H. Optimization of real time RT-PCR methods for the analysis of gene expression in mouse eggs and preimplantation embryos. Mol. Reprod. Dev. 71 (2005) 284-289
73. Waga S., and Stillman B. The DNA replication fork in eukaryotic cells. Annu. Rev. Biochem. 67 (1998) 721-751
74. Lahiri M., Gustafson T.L., Majors E.R., and Freudenreich C.H. Expanded CAG repeats activate the DNA damage checkpoint pathway. Mol. Cell 15 (2004) 287-293
75. Katahira M., Fukuda H., Kawasumi H., Sugimura T., Nakagama H., and Nagao M. Intramolecular quadruplex formation of the G-rich strand of the mouse hypervariable minisatellite Pc-1. Biochem. Biophys. Res. Commun. 264 (1999) 327-333
76. Fukuda H., Katahira M., Tanaka E., Enokizono Y., Tsuchiya N., Higuchi K., Nagao M., and Nakagama H. Unfolding of higher DNA structures formed by the d(CGG) triplet repeat by UP1 protein. Genes Cells 10 (2005) 953-962
77. Hashem V.I., Rosche W.A., and Sinden R.R. Genetic recombination destabilizes (CTG)n.(CAG)n repeats in E. coli. Mutat. Res. 554 (2004) 95-109
78. Wassenegger M. The role of the RNAi macninery in heterochromatin formation. Cell 122 (2005) 13-16
79. Lippman Z., and Martienssen R. The role of RNA interference in heterochromatic silencing. Nature 431 (2004) 364-370
80. Martienssen R.A. Maintenance of heterochromatin by RNA interference of tandem repeats. Nat. Genet. 35 (2003) 213-214
81. Raser J.M., and O'Shea E.K. Noise in gene expression: origins, consequences, and control. Science 309 (2005) 2010-2013
82. Elowitz M.B., Levine A.J., Siggia E.D., and Swain P.S. Stochastic gene expression in a single cell. Science 297 (2002) 1183-1186
83. Fry J.D. On the rate and linearity of viability declines in Drosophila mutation-accumulation experiments: genomic mutation rates and synergistic epistasis revisited. Genetics 166 (2004) 797-806
84. Searle A.G. Mutation induction in mice. Adv. Radiat. Biol. 4 (1974) 131-207
85. Hasegawa M., Wilson G., Russell L.D., and Meistrich M.L. Radiation-induced cell death in the mouse testis: relationship to apoptosis. Radiat. Res. 147 (1997) 457-467
86. Takanami T., Zhang Y., Aoki H., Abe T., Yoshida S., Takahashi H., Horiuchi S., and Higashitani A. Efficient repair of DNA damage induced by heavy ion particles in meiotic prophase I nuclei of Caenorhabditis elegans. J. Radiat. Res. (Tokyo) 44 (2003) 271-276