Role of homologous recombination in carcinogenesis

Experimental and Molecular Pathology

Volumn 74, Issue 2, 2003, Pages 94-105

  Bishop, Alexander J R ^a   Schiestl, Robert H ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer; Carcinogen induced deletions; Genomic instability diseases; Homologous recombination; Loss of heterozygosity

Indexed keywords

DNA;

CANCER GROWTH; CARCINOGENESIS; CARCINOMA; CELL PROLIFERATION; DNA REPAIR; GENE DELETION; GENE FREQUENCY; GENE MUTATION; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC DISORDER; HETEROZYGOSITY LOSS; HOMOLOGOUS RECOMBINATION; HUMAN; MAMMAL CELL; REVIEW; SIGNAL TRANSDUCTION;

EID: 0037390770     PISSN: 00144800     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4800(03)00010-8     Document Type: Review

References (184)

1. Aaltonen L.A., Peltomaki P., Leach F.S., Sistonen P., Pylkkanen L., Mecklin J.P., Jarvinen H., Powell S.M., Jen J., Hamilton S.R., et al. Clues to the pathogenesis of familial colorectal cancer. Science. 260:1993;812-816.
2. Aardema M.J., Albertini S., Arni P., Henderson L.M., Kirsch-Volders M., Mackay J.M., Sarrif A.M., Stringer D.A., Taalman R.D. Aneuploidy a report of an ECETOC task force. Mutat. Res. 410:1998;3-79.
3. Agarwal M.L., Taylor W.R., Chernov M.V., Chernova O.B., Stark G.R. The p53 network. J. Biol. Chem. 273:1998;1-4.
4. Ames B.N., Gold L.S. Chemical carcinogenesis too many rodent carcinogens. Proc Natl. Acad. Sci. USA. 87:1990;7772-7776.
5. Ames B.N., Gold L.S. Too many rodent carcinogens mitogenesis increases mutagenesis [published erratum appears in Science 1990 Sept 28;249(4976):1487]. Science. 249:1990;970-971.
6. Angele S., Hall J. The ATM gene and breast cancer is it really a risk factor. Mutat. Res. 462:2000;167-178.
7. Aubrecht J., Rugo R., Schiestl R.H. Carcinogens induce intrachromosomal, recombination in human cells. Carcinogenesis. 16:1995;2841-2846.
8. Aubrecht J., Secretan M.B., Bishop A.J., Schiestl R.H. Involvement of p53 in X-ray induced intrachromosomal recombination in mice. Carcinogenesis. 20:1999;2229-2236.
9. Ballabio A., Bardoni B., Guioli S., Basler E., Camerino G. Two families of low-copy-number repeats are interspersed on Xp22.3 implications for the high frequency of deletions in this region. Genomics. 8:1990;263-270.
10. Ban S., Shinohara T., Hirai Y., Moritaku Y., Cologne J.B., MacPhee D.G. Chromosomal instability in BRCA1- or BRCA2-defective human cancer cells detected by spontaneous micronucleus assay. Mutat. Res. 474:2001;15-23.
11. Baskaran R., Wood L.D., Whitaker L.L., Canman C.E., Morgan S.E., Xu Y., Barlow C., Baltimore D., Wynshaw-Boris A., Kastan M.B., Wang J.Y. Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature. 387:1997;516-519.
12. Baumann P., West S.C. Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem. Sci. 23:1998;247-251.
13. Bertrand P., Rouillard D., Boulet A., Levalois C., Soussi T., Lopez B.S. Increase of spontaneous intrachromosomal homologous recombination in mammalian cells expressing a mutant p53 protein. Oncogene. 14:1997;1117-1122.
14. Bezzubova O., Silbergleit A., Yamaguchi-Iwai Y., Takeda S., Buerstedde J.M. Reduced X-ray resistance and homologous recombination frequencies in a RAD54-/- mutant of the chicken DT40 cell line. Cell. 89:1997;185-193.
15. Bishop A.J., Kosaras B., Carls N., Sidman R.L., Schiestl R.H. Susceptibility of proliferating cells to benzo[a]pyrene induced homologous recombination in mice. Carcinogenesis. 22:2001;641-649.
16. Bishop A.J.R., Barlow C., Wynshaw-Boris A.J., Schiestl R.H. Atm deficiency causes an increased frequency of intrachromosomal homologous recombination in mice. Cancer Res. 60:2000;395-399.
17. Boulton S.J., Jackson S.P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17:1998;1819-1828.
18. Buchhop S., Gibson M.K., Wang X.W., Wagner P., Sturzbecher H.W., Harris C.C. Interaction of p53 with the human Rad51 protein. Nucleic Acids Res. 25:1997;3868-3874.
19. Buettner R., Mora L.B., Jove R. Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin. Cancer Res. 8:2002;945-954.
20. Carls N., Schiestl R.H. Evaluation of the yeast DEL assay with 10 compounds selected by the International Program on Chemical Safety for the evaluation of short-term tests for carcinogens. Mutat. Res. 320:1994;293-303.
21. Carney J.P., Maser R.S., Olivares H., Davis E.M., Le Beau M., Yates J.R. III, Hays L., Morgan W.F., Petrini J. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome linkage of double-strand break repair to the cellular DNA damage response. Cell. 93.H. 1998;477-486.
22. Chance P.F., Alderson M.K., Leppig K.A., Lensch M.W., Matsunami N., Smith B., Swanson P.D., Odelberg S.J., Disteche C.M., Bird T.D. DNA deletion associated with hereditary neuropathy with liability to pressure palsies. Cell. 72:1993;143-151.
23. Chen C., Kolodner R.D. Gross chromosomal rearrangements in Saccharomyces cerevisia replication and recombination defective mutants. Nature Genet. 23:1999;81-85.
24. Chen F., Nastasi A., Shen Z., Brenneman M., Crissman H., Chen D.J. Cell cycle-dependent protein expression of mammalian homologs of yeast DNA double-strand break repair genes Rad51 and Rad52. Mutat. Res. 384:1997;205-211.
25. Chen G., Yuan S.S., Liu W., Xu Y., Trujillo K., Song B., Cong F., Goff S.P., Wu Y., Arlinghaus R., et al. Radiation-induced assembly of Rad51 and, Rad52 recombination complex requires ATM and c-Abl. J. Biol. Chem. 274:1999;12748-12752.
26. Cohen M.M., Levy H.P. Chromosome instability syndromes. Adv. Human Genet. 18:1989;43-149.
27. Coleman W.B., Tsongalis G.J. The role of genomic instability in human carcinogenesis. Anticancer Res. 19:1999;4645-4664.
28. Cortez D., Wang Y., Qin J., Elledge S.J. Requirement of ATM-dependent phosphorylation of breal in the DNA damage response to double-strand breaks. Science. 286:1999;1162-1166.
29. Critchlow S.E., Jackson S.P. DNA end-joining from yeast to man. Trends Biochem. Sci. 23:1998;394-398.
30. de la Chapelle A., Herva R., Koivisto M., Aula P. A deletion in chromosome 22 can cause DiGeorge syndrome. Human Genet. 57:1981;253-256.
31. De Leon Matsuda M.L., Liede A., Kwan E., Mapua C.A., Cutiongco E.M., Tan A., Borg A., Narod S.A. BRCA1 and BRCA2 mutations among breast cancer patients from the Philippines. Int. J. Cancer. 98:2002;596-603.
32. Digweed M. Molecular basis of Fanconi's anemia. Klin. Padiatr. 211:1999;192-197.
33. Donehower L.A., Godley L.A., Aldaz C.M., Pyle R., Shi Y.P., Pinkel D., Gray J., Bradley A., Medina D., Varmus H.E. Deficiency of p53 accelerates mammary tumorigenesis in Wnt-1 transgenic mice and promotes chromosomal instability. Genes Dev. 9:1995;882-895.
34. Easton D.F. Cancer risks in A-T heterozygotes. Int. J. Radiat. Biol. 66:1994;S177-S182.
35. Ellis N.A. Mutation-causing mutations. Nature. 381:1996;110-111.
36. Ellis N.A., Groden J., Ye T.-Z., Straughen J., Lennon D.J., Ciocci S., Proytcheva M., German J. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell. 83:1995;655-666.
37. Ensch-Simon I., Burgers P.M., Taylor J.S. Bypass of a site-specific cis-Syn thymine dimer in an SV40 vector during in vitro replication by HeLa and XPV cell-free extracts. Biochemistry. 37:1998;8218-8226.
38. Epstein C.J., Martin G.M., Schultz A.L., Motulsky A.G. Werner's syndrome a review of its symptomatology, natural history, pathologic features, genetics and relationship to the natural aging process. Medicine (Baltimore). 45:1966;177-221.
39. Essers J., Hendriks R.W., Swagemakers S.M., Troelstra C., de Wit J., Bootsma D., Hoeijmakers J.H., Kanaar R. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell. 89:1997;195-204.
40. Fogel S., Mortimer R.K. Fidelity of meiotic gene conversion in yeast. Mol. Gen. Genet. 109:1970;177-185.
41. Folias A., Matkovic M., Bruun D., Reid S., Hejna J., Grompe M., D'Andrea A., Moses R. BRCA1 interacts directly with the Fanconi anemia protein FANCA. Human Mol. Genet. 11:2002;2591-2597.
42. Franchitto A., Pichierri P. Bloom's syndrome protein is required for correct relocalization of RAD50/MRE11/NBS1 complex after replication fork arrest. J. Cell Biol. 157:2002;19-30.
43. Friedberg, E.C., Walker, G.C., Siede, W., 1995. DNA repair and mutagenesis, Washington, D.C., American Society for Microbiology.
44. Fukuchi K., Martin G.M., Monnat R.J. Jr. Mutator phenotype of Werner syndrome is characterized by extensive deletions [published erratum appears in Proc. Natl. Acad. Sci. USA 1989 Oct;86(20):7994]. Proc. Natl. Acad. Sci. USA. 86:1989;5893-5897.
45. Galli A., Schiestl R.H. Effects of DNA double-strand and single-strand breaks on intrachromosomal recombination events in cell-cycle-arrested yeast cells. Genetics. 149:1998;1235-1250.
46. Galli A., Schiestl R.H. Cell division transforms mutagenic lesions into deletion-recombinagenic lesions in yeast cells. Mutat. Res. 429:1999;13-26.
47. Garcia-Higuera I., Kuang Y., D'Andrea A.D. The molecular and cellular biology of Fanconi anemia. Curr. Opin. Hematol. 6:1999;83-88.
48. Gatei M., Young D., Cerosaletti K.M., Desai-Mehta A., Spring K., Kozlov S., Lavin M.F., Gatti R.A., Concannon P., Khanna K. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat. Genet. 25:2000;115-119.
49. Gebow D., Miselis N., Liber H.L. Homologous and nonhomologous recombination resulting in deletion effects of p53 status, microhomology, and repetitive DNA length and orientation. Mol. Cell. Biol. 20:2000;4028-4035.
50. German J. Bloom syndrome a mendelian prototype of somatic mutational disease. Medicine (Baltimore). 72:1993;393-406.
51. German J. Bloom's syndrome. Dermatologic Clinics. 13:1995;7-18.
52. Gondo Y., Gardner J.M., Nakatsu Y., Durham-Pierre D., Deveau S.A., Kuper C., 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.
53. Greller L.D., Tobin F.L., Poste G. Tumor heterogeneity and progression conceptual foundations for modeling. Invasion Metastasis. 16:1996;177-208.
54. Gretarsdottir S., Thorlacius S., Valgardsdottir R., Gudlaugsdottir S., Sigurdsson S., Steinarsdottir M., Jonasson J.G., Anamthawat- Jonsson K., Eyfjord J.E. BRCA2 and p53 mutations in primary breast cancer in relation to genetic instability. Cancer Res. 58:1998;859-862.
55. Haaf T., Golub E.I., Reddy G., Radding C.M., Ward D.C. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl. Acad. Sci. USA. 92:1995;2298-2302.
56. Haber J.E. Exploring the pathways of homologous recombination. Curr. Opin. Cell Biol. 4:1992;401-412.
57. Haber J.E. Partners and pathwaysrepairing a double-strand break. Trends Genet. 16:2000;259-264.
58. Harvey M., Sands A.T., Weiss R.S., Hegi M.E., Wiseman R.W., Pantazis P., Giovanella B.C., Tainsky M.A., Bradley A., Donehower L.A. In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene. 8:1993;2457-2467.
59. Heppner G.H., Miller F.R. The cellular basis of tumor progression. Int. Rev. Cytol. 177:1998;1-56.
60. Hisada M., Garber J.E., Fung C.Y., Fraumeni J.F. Jr., Li F.P. Multiple primary cancers in families with Li-Fraumeni syndrome. J. Natl. Cancer Inst. 90:1998;606-611.
61. Hongslo J.K., Christensen T., Brunborg G., Bjornstad C., Holme J.A. Genotoxic effects of paracetamol in V79 Chinese hamster cells. Mutat. Res. 204:1988;333-341.
62. Hoogendijk J.E., Hensels G.W., Gabreels-Festen A.A., Gabreels F.J., Janssen E.A., de Jonghe P., Martin J.J., van Broeckhoven C., Valentijn L.J., Baas F., et al. De-novo mutation in hereditary motor and sensory neuropathy type I. Lance. 339:1992;1081-1082.
63. Howlett N.G., Taniguchi T., Olson S., Cox B., Waisfisz Q., De Die-Smulders C., Persky N., Grompe M., Joenje H., Pals G., et al. Biallelic inactivation, of BRCA2 in Fanconi anemia. Science. 297:2002;606-609.
64. Ionov Y., Peinado M.A., Malkhosyan S., Shibata D., Perucho M. Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature. 363:1993;558-561.
65. Jeffs A.R., Benjes S.M., Smith T.L., Sowerby S.J., Morris C.M. The BCR gene recombines preferentially with Alu elements in complex BCR-ABL translocations of chronic myeloid leukaemia. Human Mol. Genet. 7:1998;767-776.
66. Johnson R.D., Jasin M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19:2000;3398-3407.
67. Kanaar R., Hoeijmakers J.H., van Gent D.C. Molecular mechanisms of DNA double strand break repair. Trends Cell Biol. 8:1998;483-489.
68. Kanaar R., Troelstra C., Swagemakers S.M., Essers J., Smit B., Franssen J.H., Pastink A., Bezzubova O.Y., Buerstedde J.M., Clever B., et al. Human and mouse homologs of the Saccharomyces cerevisiae RAD54 DNA repair gene evidence for functional conservation. Curr. Biol. 6:1996;828-838.
69. Kaufmann W.K., Paules R.S. DNA damage and cell cycle checkpoints. FASEB J. 10:1996;238-247.
70. Knudson A.G. Antioncogenes and human cancer. Proc. Natl. Acad. Sci. US. 90:1993;10914-10921.
71. Kojis T.L., Gatti R.A., Sparkes R.S. The cytogenetics of ataxia, telangiectasia. Cancer Genet. Cytogenet. 56:1991;143-156.
72. Kokoska R.J., Stefanovic L., Tran H.T., Resnick M.A., Gordenin D.A., Petes T.D. Destabilization of yeast micro- and minisatellite DNA sequences by mutations affecting a nuclease involved in Okazaki fragment processing (rad27) and DNA polymerase delta (pol3-t). Mol. Cell. Biol. 18:1998;2779-2788.
73. Kowalczykowski S.C. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25:2000;156-165.
74. Langston A.A., Malone K.E., Thompson J.D., Daling J.R., Ostrander E.A. BRCA1 mutations in a population-based sample of young women with breast cancer. N. Engl. J. Med. 334:1996;137-142.
75. Larson K.L., Strauss B.S. Influence of template strandedness on in vitro replication of mutagen-damaged DNA. Biochemistry. 26:1987;2471-2479.
76. Lebel M. Increased frequency of DNA deletions in pink-eyed unstable mice carrying a mutation in the Werner syndrome gene homologue. Carcinogenesis. 23:2002;213-216.
77. Ledbetter D.H., Riccardi V.M., Airhart S.D., Strobel R.J., Keenan B.S., Crawford J.D. Deletions of chromosome 15 as a cause of the Prader-Willi syndrome. N. Engl. J. Med. 304:1981;325-329.
78. Lehmann A.R. The relationship between pyrimidine dimers and replicating DNA in UV-irradiated human fibroblasts. Nucleic Acids Res. 7:1979;1901-1912.
79. Lehrman M.A., Schneider W.J., Sudhof T.C., Brown M.S., Goldstein J.L., Russell D.W. Mutation in LDL receptor Alu-Alu recombination deletes exons encoding transmembrane and cytoplasmic domains. Science. 227:1985;140-146.
80. Lengauer C., Kinzler K.W., Vogelstein B. Genetic instabilities in human cancers. Nature. 396:1998;643-649.
81. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell. 88:1997;323-331.
82. Levinson G., Gutman G.A. High frequencies of short frameshifts in poly-CA/TG tandem repeats borne by bacteriophage M13 in Escherichia coli K-12. Nucleic Acids Res. 15:1987;5323-5338.
83. Levinson G., Gutman G.A. Slipped-strand mispairing a major mechanism, for DNA sequence evolution. Mol. Biol. Evol. 4:1987;203-221.
84. Li B., Comai L. Functional interaction between Ku and the Werner syndrome protein in DNA end processing. J. Biol. Chem. 275:2000;28349-28352.
85. Liang F., Han M., Romanienko P.J., Jasin M. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl. Acad. Sci. USA. 95:1998;5172-5177.
86. Lieber M.R. Warner-Lambert/Parke-Davis Award Lecture. Pathological and physiological double-strand breaks roles in cancer, aging, and the immune system. Am. J. Pathol. 153:1998;1323-1332.
87. Liede A., Jack E., Hegele R.A., Narod S.A. A BRCA1 mutation in Native North American families. Human Mutat. 19:2002;460.
88. Lim D.S., Hasty P. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16:1996;7133-7714.
89. Lim D.S., Kim S.T., Xu B., Maser R.S., Lin J., Petrini J.H., Kastan M.B. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature. 404:2000;613-617.
90. Livingstone L.R., White A., Sprouse J., Livanos E., Jacks T., Tlsty T.D. Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53. Cell. 70:1992;923-935.
91. Loeb K.R., Loeb L.A. Significance of multiple mutations in cancer. Carcinogenesis. 21:2000;379-385.
92. Luo C.M., Tang W., Mekeel K.L., DeFrank J.S., Anne P.R., Powell S.N. High frequency and error-prone DNA recombination in ataxia telangiectasia cell lines. J. Biol. Chem. 271:1996;4497-4503.
93. Macleod K. Tumor suppressor genes. Curr. Opin. Genet. Dev. 10:2000;81-93.
94. Malone K.E., Daling J.R., Neal C., Suter N.M., O'Brien C., Cushing-Haugen K., Jonasdottir T.J., Thompson J.D., Ostrander E.A. Frequency of BRCA1/BRCA2 mutations in a population-based sample of young breast carcinoma cases. Cancer. 88:2000;1393-1402.
95. Malone K.E., Daling J.R., Thompson J.D., O'Brien C.A., Francisco L.V., Ostrander E.A. BRCA1 mutations and breast cancer in the general population analyses in women before age 35 years and in women before age 45 years with first-degree family history. JAMA. 279:1998;922-929.
96. Marians K.J. Replication and recombination intersect. Curr. Opin. Genet. Dev. 10:2000;151-156.
97. Martinelli G., Terragna C., Amabile M., Montefusco V., Testoni N., Ottaviani E., de Vivo A., Mianulli A., Saglio G., Tura S. Alu and translisin recognition site sequences flanking translocation sites in a novel type of chimeric bcr-abl transcript suggest a possible general mechanism for bcr-abl breakpoints. Haematologica. 85:2000;40-46.
98. Maser R.S., Monsen K.J., Nelms B.E., Petrini J.H. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol. Cell. Biol. 17:1997;6087-6096.
99. McNulty J.M., Jerkovic B., Bolton P.H., Basu A.K. Replication inhibition and miscoding properties of DNA templates containing a site-specific cis-thymine glycol or urea residue. Chem. Res. Toxicol. 11:1998;666-673.
100. Mekeel K.L., Tang W., Kachnic L.A., Luo C.M., DeFrank J.S., Powell S.N. Inactivation of p53 results in high rates of homologous recombination. Oncogene. 14:1997;1847-1857.
101. Meyn M.S. High spontaneous intrachromosomal recombination rates in ataxia-telangiectasia. Science. 260:1993;1327-1330.
102. Michel B., Flores M.J., Viguera E., Grompone G., Seigneur M., Bidnenko V. Rescue of arrested replication forks by homologous recombination. Proc. Natl. Acad. Sci. USA. 98:2001;8181-8188.
103. Milne G.T., Jin S., Shannon K.B., Weaver D.T. Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:1996;4189-4198.
104. Mitchell M.B. Aberrant recombinations of pyridoxine mutants of Neurospora. Proc. Natl. Acad. Sci. USA. 41:1955;215.
105. Mitchell M.B. Further evidence of aberrant recombination in Neurospora. Proc. Natl. Acad. Sci. USA. 41:1955;935-993.
106. Mitelman F. Chromosomes, genes, and cancer. CA Cancer J. Clin. 44:1994;133-135.
107. Morrison C., Sonoda E., Takao N., Shinohara A., Yamamoto K., Takeda S. The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J. 19:2000;463-471.
108. Moynahan M.E., Chiu J.W., Koller B.H. Jasin, Brcal controls homology-directed DNA repair. Mol. Cell. 4 M. 1999;511-518.
109. Moynahan M.E., Jasin M. Loss of heterozygosity induced by a chromosomal double-strand break. Proc. Natl. Acad. Sci. USA. 94:1997;8988-8993.
110. Moynahan M.E., Pierce A.J., Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell. 7:2001;263-272.
111. Nedelcu R., Liede A., Aube J., Finch A., Kwan E., Jack E., Narod S.A., Randall S., Hugel L., Clark K. BRCA mutations in Italian breast/ovarian cancer families. Eur. J. Human Genet. 10:2002;150-152.
112. Nelis E., Van Broeckhoven C., De Jonghe P., Lofgren A., Vandenberghe A., Latour P., Le Guern E., Brice A., Mostacciuolo M.L., Schiavon F., et al. Estimation of the mutation frequencies in Charcot-Marie-Tooth disease type 1 and hereditary neuropathy with liability to pressure palsies a European collaborative study. Eur. J. Human Genet. 4:1996;25-33.
113. O'Day C.L., Burgers P.M., Taylor J.S. PCNA-induced DNA synthesis, past cis-syn and trans-syn-I thymine dimers by calf thymus DNA polymerase delta in vitro. Nucleic Acids Res. 20:1992;5403-5406.
114. Offer H., Wolkowicz R., Matas D., Blumenstein S., Livneh Z., Rotter V. Direct involvement of p53 in the base excision repair pathway of the DNA repair machinery. FEBS Lett. 450:1999;197-204.
115. Parsons C.A., Baumann P., Van Dyck E., West S.C. Precise binding of single-stranded DNA termini by human RAD52 protein. EMBO J. 19:2000;4175-4181.
116. Parsons R., Li G.M., Longley M.J., Fang W.H., Papadopoulos N., Jen J., de la Chapelle A., Kinzler K.W., Vogelstein B., Modrich P. Hypermutability and mismatch repair deficiency in RER+ tumor cells. Cell. 75:1993;1227-1236.
117. Patel K.J., Yu V.P., Lee H., Corcoran A., Thistlethwaite F.C., Evans M.J., Colledge W.H., Friedman L.S., Ponder B.A., Venkitaraman A.R. Involvement of Brca2 in DNA repair. Mol. Cell. 1:1998;347-357.
118. Pentao L., Wise C.A., Chinault A.C., Patel P.I., Lupski J.R. Charcot-Marie-Tooth type 1A duplication appears to arise from recombination at repeat sequences flanking the 1.5 Mb monomer unit. Nat. Genet. 2:1992;292-300.
119. Peto J., Collins N., Barfoot R., Seal S., Warren W., Rahman N., Easton D.F., Evans C., Deacon J., Stratton M.R. Prevalence of BRCA1 and BRCA2 gene mutations in patients with early-onset breast cancer. J. Natl. Cancer Inst. 91:1999;943-949.
120. Petrini J.H., Bressan D.A., Yao M.S. The RAD52 epistasis group in mammalian double strand break repair. Semin. Immunol. 9:1997;181-188.
121. Pichierri P., Franchitto A., Mosesso P., Palitti F. Werner's syndrome protein is required for correct recovery after replication arrest and DNA damage induced in S-phase of cell cycle. Mol. Biol. Cell. 12:2001;2412-2421.
122. Purdie C.A., Harrison D.J., Peter A., Dobbie L., White S., Howie S.E., Salter D.M., Bird C.C., Wyllie A.H., Hooper M.L., et al. Tumour incidence, spectrum and ploidy in mice with a large deletion in the p53 gene. Oncogene. 9:1994;603-609.
123. Ramsden D.A., Gellert M. Ku protein stimulates DNA end joining by mammalian DNA ligases a direct role for Ku in repair of DNA double-strand breaks. EMBO J. 17:1998;609-614.
124. Rasnick D., Duesberg P.H. How aneuploidy affects metabolic control and causes cancer. Biochem J. 340:1999;621-630.
125. Rebbeck T.R. Inherited predisposition and breast cancer modifiers of BRCA1/2-associated breast cancer risk. Environ. Mol. Mutagen. 39:2002;228-234.
126. Richardson C., Moynahan M.E., Jasin M. Double-strand break repair by interchromosomal recombination suppression of chromosomal translocations. Genes Dev. 12:1998;3831-3842.
127. Roman H. Studies of gene conversion in Saccharomyces. Cold Spring Harb. Symp. Quant. Biol. 21:1957;175-185.
128. Rothstein R., Michel B., Gangloff S. Replication fork pausing and recombination or "gimme a break" Genes Dev. 14:2000;1-10.
129. Saintigny Y., Delacote F., Vares G., Petitot F., Lambert S., Averbeck D., Lopez B.S. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 20:2001;3861-3870.
130. Schichman S.A., Caligiuri M.A., Strout M.P., Carter S.L., Gu Y., Canaani E., Bloomfield C.D., Croce C.M. ALL-1 tandem duplication in acute myeloid leukemia with a normal karyotype involves homologous recombination between Alu elements. Cancer Res. 54:1994;4277-4280.
131. Schiestl R.H. Nonmutagenic carcinogens induce intrachromosomal recombination in yeast. Nature. 337:1989;285-288.
132. Schiestl R.H., Aubrecht J., Khogali F., Carls N. Carcinogens induce reversion of the mouse pink-eyed unstable mutation. Proc. Natl. Acad. Sci. USA. 94:1997;4576-4581.
133. Schiestl R.H., Aubrecht J., Yap W.Y., Kandikonda S., Sidhom S. Polychlorinated biphenyls and TCDD induce intrachromosomal recombination in vitro and in vivo. Cancer Res. 57:1997;4378-4383.
134. Schiestl R.H., Gietz R.D., Hastings P.J., Wintersberger U. Interchromosomal and intrachromosomal recombination in rad 18 mutants of Saccharomyces cerevisiae. Mol. Gen. Genet. 222:1990;25-32.
135. Schiestl R.H., Gietz R.D., Mehta R.D., Hastings P.J. Carcinogens induce intrachromosomal recombination in yeast. Carcinogenesis. 10:1989;1445-1455.
136. Schiestl R.H., Igarashi S., Hastings P.J. Analysis of the mechanism for reversion of a disrupted gene. Genetics. 119:1988;237-247.
137. Schiestl R.H., Khogali F., Carls N. Reversion of the mouse pink-eyed unstable mutation induced by low doses of x-rays. Science. 266:1994;1573-1576.
138. Schiestl R.H., Zhu J., Petes T.D. Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 14:1994;4493-4500.
139. Schlotterer C., Tautz D. Slippage synthesis of simple sequence DNA. Nucleic Acids Res. 20:1992;211-215.
140. Schmutte C., Fishel R. Genomic instability first step to carcinogenesis. Anticancer Res. 19:1999;4665-4696.
141. Scully R., Chen J., Ochs R.L., Keegan K., Hoekstra M., Feunteun J., Livingston D.M. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell. 90:1997;425-435.
142. Shafman T., Khanna K.K., Kedar P., Spring K., Kozlov S., Yen T., Hobson K., Gatei M., Zhang N., Watters D., et al. Interaction between ATM protein and c-Abl in response to DNA damage. Nature. 387:1997;520-523.
143. Shieh S.Y., Ikeda M., Taya Y., Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell. 91:1997;325-334.
144. Sia E.A., Kokoska R.J., Dominska M., Greenwell P., Petes T.D. Microsatellite instability in yeast dependence on repeat unit size and DNA mismatch repair genes. Mol. Cell. Biol. 17:1997;2851-2858.
145. Siliciano J.D., Canman C.E., Taya Y., Sakaguchi K., Appella E., Kastan M.B. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev. 11:1997;3471-3481.
146. Slupianek A., Hoser G., Majsterek I., Bronisz A., Malecki M., Blasiak J., Fishel R., Skorski T. Fusion tyrosine kinases induce drug resistance by stimulation of homology-dependent recombination repair, prolongation of G(2)/M phase, and protection from apoptosis. Mol. Cell. Biol. 22:2002;4189-4201.
147. Sonoda E., Sasaki M.S., Buerstedde J.M., Bezzubova O., Shinohara A., Ogawa H., Takata M., Yamaguchi-Iwai Y., Takeda S. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17:1998;598-608.
148. Sonoda E., Sasaki M.S., Morrison C., Yamaguchi-Iwai Y., Takata M., Takeda S. Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol. 19:1999;5166-5169.
149. Stewart G.S., Maser R.S., Stankovic T., Bressan D.A., Kaplan M.I., Jaspers N.G., Raams A., Byrd P.J., Petrini J.H., Taylor A.M. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell. 99:1999;577-587.
150. Strong L.C., Williams W.R., Tainsky M.A. The Li-Fraumeni syndrome from clinical epidemiology to molecular genetics. Am. J. Epidemiol. 135:1992;190-199.
151. Sturzbecher H.W., Donzelmann B., Henning W., Knippschild U., Buchhop S. p53 is linked directly to homologous recombination processes via RAD51/RecA protein interaction. EMBO J. 15:1996;1992-2002.
152. Takata M., Sasaki M.S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17:1998;5497-5508.
153. Tan T.L., Essers J., Citterio E., Swagemakers S.M., de Wit J., Benson F.E., Hoeijmakers J.H., Kanaar R. Mouse Rad54 affects DNA conformation and DNA-damage-induced Rad51 foci formation. Curr. Biol. 9:1999;325-328.
154. Thein S.L., Jeffreys A.J., Gooi H.C., Cotter F., Flint J., O'Connor N.T., Weatherall D.J., Wainscoat J.S. Detection of somatic changes in human cancer DNA by DNA fingerprint analysis. Br. J. Cancer. 55:1987;353-356.
155. Thibodeau S.N., Bren G., Schaid D. Microsatellite instability in cancer of the proximal colon. Science. 260:1993;816-819.
156. Thomas D.C., Veaute X., Kunkel T.A., Fuchs R.P. Mutagenic replication in human cell extracts of DNA containing site-specific N-2-acetylaminofluorene adducts. Proc. Natl. Acad. Sci. USA. 91:1994;7752-7756.
157. Thyagarajan B., Campbell C. Elevated homologous recombination activity in fanconi anemia fibroblasts. J. Biol. Chem. 272:1997;23328-23333.
158. Tirkkonen M., Johannsson O., Agnarsson B.A., Olsson H., Ingvarsson S., Karhu R., Tanner M., Isola J., Barkardottir R.B., Borg A., Kallioniemi O.P. Distinct somatic genetic changes associated with tumor progression in carriers of BRCA1 and BRCA2 germ-line mutations. Cancer Res. 57:1997;1222-1227.
159. Tlsty T.D. Genomic instability and its role in neoplasia. Curr. Topics Microbiol. Immunol. 221:1997;37-46.
160. Todd R., Wong D.T. Oncogenes. Anticancer Res. 19:1999;4729-4746.
161. Tonin P., Weber B., Offit K., Couch F., Rebbeck T.R., Neuhausen S., Godwin A.K., Daly M., Wagner-Costalos J., Berman D., et al. Frequency of recurrent BRCA1 and BRCA2 mutations in Ashkenazi Jewish breast cancer families. Nat. Med. 2:1996;1179-1183.
162. Tsuzuki T., Fujii Y., Sakumi K., Tominaga Y., Nakao K., Sekiguchi M., Matsushiro A., Yoshimura Y., Morita T. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. USA. 93:1996;6236-6240.
163. Turker M.S., Gage B.M., Rose J.A., Ponomareva O.N., Tischfield J.A., Stambrook P.J., Barlow C., Wynshaw-Boris A. Solid tissues removed from Atm homozygous deficient mice do not exhibit a mutator phenotype for second-step autosomal mutations. Cancer Res. 59:1999;4781-4783.
164. Tutt A., Bertwistle D., Valentine J., Gabriel A., Swift S., Ross G., Griffin C., Thacker J., Ashworth A. Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J. 20:2001;4704-4716.
165. Tutt A., Gabriel A., Bertwistle D., Connor F., Paterson H., Peacock J., Ross G., Ashworth A. Absence of Brca2 causes genome instability by chromosome breakage and loss associated with centrosome amplification. Curr. Biol. 9:1999;1107-1110.
166. van Beerendonk G.J., van Gog F.B., Vrieling H., Pearson P.G., Nelson S.D., Meerman J.H. Blocking of in vitro DNA replication by deoxycytidine adducts of the mutagen and clastogen 2-bromoacrolein. Cancer Res. 54:1994;679-684.
167. Van Dyck E., Stasiak A.Z., Stasiak A., West S.C. Binding of double-strand breaks in DNA by human Rad52 protein. Nature. 398:1999;728-731.
168. Vessey C.J., Norbury C.J., Hickson I.D. Genetic disorders associated with cancer predisposition and genomic instability. Prog. Nucleic Acid Res. Mol. Biol. 63:1999;189-221.
169. Vispe S., Cazaux C., Lesca C., Defais M. Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucleic Acids Res. 26:1998;2859-2864.
170. Wang X.W., Yeh H., Schaeffer L., Roy R., Moncollin V., Egly J.M., Wang Z., Freidberg E.C., Evans M.K., Taffe B.G., et al. p53 modulation of TFIIH-associated nucleotide excision repair activity. Nat. Genet. 10:1995;188-195.
171. Wang Y., Cortez D., Yazdi P., Neff N., Elledge S.J., Qin J. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14:2000;927-939.
172. Warner E., Foulkes W., Goodwin P., Meschino W., Blondal J., Paterson C., Ozcelik H., Goss P., Allingham-Hawkins D., Hamel N., et al. Prevalence and penetrance of BRCA1 and BRCA2 gene mutations in unselected Ashkenazi Jewish women with breast cancer. J. Natl. Cancer Inst. 91:1999;1241-1247.
173. Willers H., McCarthy E.E., Wu B., Wunsch H., Tang W., Taghian D.G., Xia F., Powell S.N. Dissociation of p53-mediated suppression of homologous recombination from G1/S cell cycle checkpoint control. Oncogene. 19:2000;632-639.
174. Winkler, H., 1930. Die Kon version der Gene, Gustav Fischer, Jena.
175. Wise C.A., Garcia C.A., Davis S.N., Heju Z., Pentao L., Patel P.I., Lupski J.R. Molecular analyses of unrelated Charcot-Marie-Tooth (CMT) disease patients suggest a high frequency of the CMTIA duplication. Am. J. Human Genet. 53:1993;853-863.
176. Wu X., Ranganathan V., Weisman D.S., Heine W.F., Ciccone D.N., O'Neill T.B., Crick K.E., Pierce K.A., Lane W.S., Rathbun G., et al. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature. 405:2000;477-482.
177. Xu J., Bubley G.J., Detrick B., Blankenship L.J., Patierno S.R. Chromium(VI) treatment of normal human lung cells results in guanine-specific DNA polymerase arrest, DNA-DNA cross-links and S-phase blockade of cel cycle. Carcinogenesis. 17:1996;1511-1517.
178. Xu X., Weaver Z., Linke S.P., Li C., Gotay J., Wang X.W., Harris C.C., Ried T., Deng C.X. Centrosome amplification and a defective G2-M cell cycle
179. Yamamoto A., Taki T., Yagi H., Habu T., Yoshida K., Yoshimura Y., Yamamoto K., Matsushiro A., Nishimune Y., Morita T. Cell cycle-dependent expression of the mouse Rad51 gene in proliferating cells. Mol. Gen. Genet. 251:1996;1-12.
180. Yen P.H., Li X.M., Tsai S.P., Johnson C., Mohandas T., Shapiro L.J. Frequent deletions of the human X chromosome distal short arm result from recombination between low copy repetitive elements. Cell. 61:1990;603-610.
181. Yin Y., Tainsky M.A., Bischoff F.Z., Strong L.C., Wahl G.M. Wild-type p53 restores cell cycle control and inhibits gene amplification in cells with mutant p53 alleles. Cell. 70:1992;937-948.
182. Yu C.E., Oshima J., Fu Y.H., Wijsman E.M., Hisama F., Alisch R., Matthews S., Nakura J., Miki T., Ouais S., et al. Positional cloning of the Werner's syndrome gene. Science. 272:1996;258-262.
183. Yuan Z.M., Huang Y., Ishiko T., Nakada S., Utsugisawa T., Kharbanda S., Wang R., Sung P., Shinohara A., Weichselbaum R., Kufe D. Regulation of Rad51 function by c-Ab1 in response to DNA damage. J. Biol. Chem. 273:1998;3799-3802.
184. Zhao S., Weng Y.C., Yuan S.S., Lin Y.T., Hsu H.C., Lin S.C., Gerbino E., Song M.H., Zdzienicka M.Z., Gatti R.A., et al. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature. 405:2000;473-477.