Ku86 deficiency leads to reduced intrachromosomal homologous recombination in vivo in mice

DNA Repair

Volumn 3, Issue 2, 2004, Pages 103-111

  Reliene, Ramune ^a   Bishop, Alexander J R ^b   Li, Gloria ^c   Schiestl, Robert H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Genetic instability; In vivo; Ku86; Mouse; pun Reversions

Indexed keywords

DNA; KU ANTIGEN; PROTEIN KU86; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DATA ANALYSIS; DILUTION; GENE DELETION; GENE DUPLICATION; GENE MUTATION; GENETIC RECOMBINATION; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN DEFICIENCY; QUANTITATIVE ANALYSIS;

EID: 0346729824     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2003.09.010     Document Type: Article

References (86)

1. van Gent D.C., Hoeijmakers J.H., Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2:2001;196-206.
2. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature. 411:2001;366-374.
3. Karran P. DNA double-strand break repair in mammalian cells. Curr. Opin. Genet. Dev. 10:2000;144-150.
4. Khanna K.K., Jackson S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27:2001;247-254.
5. Haber J.E. Partners and pathwaysrepairing a double-strand break. Trends Genet. 16:2000;259-264.
6. 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.
7. Smith G.C., Jackson S.P. The DNA-dependent protein kinase. Genes Dev. 13:1999;916-934.
8. Taccioli G.E., Gottlieb T.M., Blunt T., Priestley A., Demengeot J., Mizuta R., Lehmann A.R., Alt F.W., Jackson S.P., Jeggo P.A. Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science. 265:1994;1442-1445.
9. Rathmell W.K., Chu G. Involvement of the Ku autoantigen in the cellular response to DNA double-strand breaks. Proc. Natl. Acad. Sci. U.S.A. 91:1994;7623-7627.
10. Mimori T., Hardin J.A. Mechanism of interaction between Ku protein and DNA. J. Biol. Chem. 261:1986;10375-10379.
11. 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.
12. Kirchgessner C.U., Patil C.K., Evans J.W., Cuomo C.A., Fried L.M., Carter T., Oettinger M.A., Brown J.M. DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science. 267:1995;1178-1183.
13. Difilippantonio M.J., Zhu J., Chen H.T., Meffre E., Nussenzweig M.C., Max E.E., Ried T., Nussenzweig A. DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature. 404:2000;510-514.
14. Ferguson D.O., Sekiguchi J.M., Chang S., Frank K.M., Gao Y., DePinho R.A., Alt F.W. The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc. Natl. Acad. Sci. U.S.A. 97:2000;6630-6633.
15. d'Adda di Fagagna F., Hande M.P., Tong W.M., Roth D., Lansdorp P.M., Wang Z.Q., Jackson S.P. Effects of DNA nonhomologous end-joining factors on telomere length and chromosomal stability in mammalian cells. Curr. Biol. 11:2001;1192-1196.
16. Bailey S.M., Meyne J., Chen D.J., Kurimasa A., Li G.C., Lehnert B.E., Goodwin E.H. DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. U.S.A. 96:1999;14899-14904.
17. Hsu H.L., Gilley D., Galande S.A., Hande M.P., Allen B., Kim S.H., Li G.C., Campisi J., Kohwi-Shigematsu T., Chen D.J. Ku acts in a unique way at the mammalian telomere to prevent end joining. Genes Dev. 14:2000;2807-2812.
18. Nussenzweig A., Sokol K., Burgman P., Li L., Li G.C. Hypersensitivity of Ku80-deficient cell lines and mice to DNA damage: the effects of ionizing radiation on growth, survival, and development. Proc. Natl. Acad. Sci. U.S.A. 94:1997;13588-13593.
19. Gu Y., Jin S., Gao Y., Weaver D.T., Alt F.W. Ku70-deficient embryonic stem cells have increased ionizing radiosensitivity, defective DNA end-binding activity, and inability to support V(D)J recombination. Proc. Natl. Acad. Sci. U.S.A. 94:1997;8076-8081.
20. Zhu C., Bogue M.A., Lim D.S., Hasty P., Roth D.B. Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell. 86:1996;379-389.
21. Nussenzweig A., Chen C., da Costa Soares V., Sanchez M., Sokol K., Nussenzweig M.C., Li G.C. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature. 382:1996;551-555.
22. Gu Y., Seidl K.J., Rathbun G.A., Zhu C., Manis J.P., van der Stoep N., Davidson L., Cheng H.L., Sekiguchi J.M., Frank K., Stanhope-Baker P., Schlissel M.S., Roth D.B., Alt F.W. Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity. 7:1997;653-665.
23. Vogel H., Lim D.S., Karsenty G., Finegold M., Hasty P. Deletion of Ku86 causes early onset of senescence in mice. Proc. Natl. Acad. Sci. U.S.A. 96:1999;10770-10775.
24. Jackson S.P., Jeggo P.A. DNA double-strand break repair and V(D)J recombination: involvement of DNA-PK. Trends Biochem. Sci. 20:1995;412-415.
25. Barnes D.E. Non-homologous end joining as a mechanism of DNA repair. Curr. Biol. 11:2001;R455-R457.
26. C.W. Schmid, N. Deka, A.G. Matera, Repetetive human DNA: the shape of things to come, in: A. KW (Ed.), Chromosomes: Eucaryotic, Procaryotic and Viral, CRC Press, Boca Raton, 1989, pp. 3-29.
27. Calabretta B., Robberson D.L., Barrera-Saldana H.A., Lambrou T.P., Saunders G.F. Genome instability in a region of human DNA enriched in Alu repeat sequences. Nature. 296:1982;219-225.
28. Liang F., Romanienko P.J., Weaver D.T., Jeggo P.A., Jasin M. Chromosomal double-strand break repair in Ku80-deficient cells. Proc. Natl. Acad. Sci. U.S.A. 93:1996;8929-8933.
29. Sargent R.G., Brenneman M.A., Wilson J.H. Repair of site-specific double-strand breaks in a mammalian chromosome by homologous and illegitimate recombination. Mol. Cell Biol. 17:1997;267-277.
30. Taghian D.G., Nickoloff J.A. Chromosomal double-strand breaks induce gene conversion at high frequency in mammalian cells. Mol. Cell Biol. 17:1997;6386-6393.
31. Moynahan M.E., Jasin M. Loss of heterozygosity induced by a chromosomal double-strand break. Proc. Natl. Acad. Sci. U.S.A. 94:1997;8988-8993.
32. 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. U.S.A. 95:1998;5172-5177.
33. 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. U.S.A. 90:1993;297-301.
34. Bishop A.J., 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.
35. 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.
36. Schiestl R.H., Aubrecht J., Khogali F., Carls N. Carcinogens induce reversion of the mouse pink-eyed unstable mutation. Proc. Natl. Acad. Sci. U.S.A. 94:1997;4576-4581.
37. Bishop A.J., Kosaras B., Sidman R.L., Schiestl R.H. Benzo(a)pyrene and X-rays induce reversions of the pink-eyed unstable mutation in the retinal pigment epithelium of mice. Mutat. Res. 457:2000;31-40.
38. Roth D.B., Wilson J.H. Relative rates of homologous and nonhomologous recombination in transfected DNA. Proc. Natl. Acad. Sci. U.S.A. 82:1985;3355-3359.
39. 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.
40. Pierce A.J., Hu P., Han M., Ellis N., Jasin M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15:2001;3237-3242.
41. Allen C., Kurimasa A., Brenneman M.A., Chen D.J., Nickoloff J.A. DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc. Natl. Acad. Sci. U.S.A. 99:2002;3758-3763.
42. Cervelli T., Galli A. Effects of HDF1 (Ku70) and HDF2 (Ku80) on spontaneous and DNA damage-induced intrachromosomal recombination in Saccharomyces cerevisiae. Mol. Gen. Genet. 264:2000;56-63.
43. Mages G.J., Feldmann H.M., Winnacker E.L. Involvement of the Saccharomyces cerevisiae HDF1 gene in DNA double-strand break repair and recombination. J. Biol. Chem. 271:1996;7910-7915.
44. Brilliant M.H., Gondo Y., Eicher E.M. Direct molecular identification of the mouse pink-eyed unstable mutation by genome scanning. Science. 252:1991;566-569.
45. Rosemblat S., Durham-Pierre D., Gardner J.M., Nakatsu Y., Brilliant M.H., Orlow S.J. Identification of a melanosomal membrane protein encoded by the pink-eyed dilution (type II oculocutaneous albinism) gene. Proc. Natl. Acad. Sci U.S.A. 91:1994;12071-12075.
46. Lyon M.F., King T.R., Gondo Y., Gardner J.M., Nakatsu Y., Eicher E.M., Brilliant M.H. Genetic and molecular analysis of recessive alleles at the pink-eyed dilution (p) locus of the mouse. Proc. Natl. Acad. Sci. U.S.A. 89:1992;6968-6972.
47. Jalili T., Murthy G.G., Schiestl R.H. Cigarette smoke induces DNA deletions in the mouse embryo. Cancer Res. 58:1998;2633-2638.
48. Bodenstein L., Sidman R.L. Growth and development of the mouse retinal pigment epithelium. Part II. Cell patterning in experimental chimaeras and mosaics. Dev. Biol. 121:1987;205-219.
49. Bodenstein L., Sidman R.L. Growth and development of the mouse retinal pigment epithelium. Part I. Cell and tissue morphometrics and topography of mitotic activity. Dev. Biol. 121:1987;192-204.
50. A.J.R. Bishop, M.C. Hollander, B. Kosaras, R.L. Sidman, J. Fornace, R.H. Schiestl, Atm, p53 and Gadd45 deficient mice have an increased frequency of homologous recombination at different times during development, Cancer Res. 63 (2003) 5335-5343.
51. 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.
52. Gardner J.M., Nakatsu Y., Gondo Y., Lee S., Lyon M.F., King R.A., Brilliant M.H. The mouse pink-eyed dilution gene: association with human Prader-Willi and Angelman syndromes. Science. 257:1992;1121-1124.
53. Oakey R.J., Keiper N.M., Ching A.S., Brilliant M.H. Molecular analysis of the cDNAs encoded by the pun and pJ alleles of the pink-eyed dilution locus. Mamm. Genome. 7:1996;315-316.
54. Galli A., Schiestl R.H. On the mechanism of UV and gamma-ray-induced intrachromosomal recombination in yeast cells synchronized in different stages of the cell cycle. Mol. Gen. Genet. 248:1995;301-310.
55. Schiestl R.H., Igarashi S., Hastings P.J. Analysis of the mechanism for reversion of a disrupted gene. Genetics. 119:1988;237-247.
56. 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.
57. Nakayama A., Nguyen M.T., Chen C.C., Opdecamp K., Hodgkinson C.A., Arnheiter H. Mutations in microphthalmia, the mouse homolog of the human deafness gene MITF, affect neuroepithelial and neural crest-derived melanocytes differently. Mech. Dev. 70:1998;155-166.
58. Kong Y., Usuda N., Morita T., Hanai T., Nagata T. Study on RNA synthesis in the retina and retinal pigment epithelium of mice by light microscopic radioautography. Cell. Mol. Biol. (Noisy-le-grand). 38:1992;669-678.
59. Manivasakam P., Aubrecht J., Sidhom S., Schiestl R.H. Restriction enzymes increase efficiencies of illegitimate DNA integration but decrease homologous integration in mammalian cells. Nucleic Acids Res. 29:2001;4826-4833.
60. 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.
61. Belmaaza A., Chartrand P. One-sided invasion events in homologous recombination at double-strand breaks. Mutat. Res. 314:1994;199-208.
62. Tuteja N., Tuteja R., Ochem A., Taneja P., Huang N.W., Simoncsits A., Susic S., Rahman K., Marusic L., Chen J.et al. Human DNA helicase II: a novel DNA unwinding enzyme identified as the Ku autoantigen. EMBO J. 13:1994;4991-5001.
63. Ochem A.E., Skopac D., Costa M., Rabilloud T., Vuillard L., Simoncsits A., Giacca M., Falaschi A. Functional properties of the separate subunits of human DNA helicase II/Ku autoantigen. J. Biol. Chem. 272:1997;29919-29926.
64. de Vries E., van Driel W., Bergsma W.G., Arnberg A.C., van der Vliet P.C. HeLa nuclear protein recognizing DNA termini and translocating on DNA forming a regular DNA-multimeric protein complex. J. Mol. Biol. 208:1989;65-78.
65. Paillard S., Strauss F. Analysis of the mechanism of interaction of simian Ku protein with DNA. Nucleic Acids Res. 19:1991;5619-5624.
66. Mortensen U.H., Bendixen C., Sunjevaric I., Rothstein R. DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl. Acad. Sci. U.S.A. 93:1996;10729-10734.
67. Reddy G., Golub E.I., Radding C.M. Human Rad52 protein promotes single-strand DNA annealing followed by branch migration. Mutat. Res. 377:1997;53-59.
68. 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.
69. Tauchi H., Kobayashi J., Morishima K., van Gent D.C., Shiraishi T., Verkaik N.S., vanHeems D., Ito E., Nakamura A., Sonoda E., Takata M., Takeda S., Matsuura S., Komatsu K. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature. 420:2002;93-98.
70. 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.
71. Bressan D.A., Baxter B.K., Petrini J.H. The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell Biol. 19:1999;7681-7687.
72. Arrington E.D., Caldwell M.C., Kumaravel T.S., Lohani A., Joshi A., Evans M.K., Chen H.T., Nussenzweig A., Holbrook N.J., Gorospe M. Enhanced sensitivity and long-term G2 arrest in hydrogen peroxide-treated Ku80-null cells are unrelated to DNA repair defects. Free Radic. Biol. Med. 29:2000;1166-1176.
73. Chan J.Y., Chen L.K., Chang J.F., Ting H.M., Goy C., Chen J.L., Hwang J.J., Chen F.D., Chen D.J., Ngo F.Q. Differential gene expression in a DNA double-strand-break repair mutant XRS-5 defective in Ku80: analysis by cDNA microarray. J. Radiat. Res. (Tokyo). 42:2001;371-385.
74. 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.
75. 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.
76. 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.
77. 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.
78. Lim D.S., Vogel H., Willerford D.M., Sands A.T., Platt K.A., Hasty P. Analysis of ku80-mutant mice and cells with deficient levels of p53. Mol. Cell. Biol. 20:2000;3772-3780.
79. Li G., Nelsen C., Hendrickson E.A. Ku86 is essential in human somatic cells. Proc. Natl. Acad. Sci. U.S.A. 99:2002;832-837.
80. Aladjem M.I., Spike B.T., Rodewald L.W., Hope T.J., Klemm M., Jaenisch R., Wahl G.M. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr. Biol. 8:1998;145-155.
81. Schmidt-Kastner P.K., Jardine K., Cormier M., McBurney M.W. Absence of p53-dependent cell cycle regulation in pluripotent mouse cell lines. Oncogene. 16:1998;3003-3011.
82. Gottlieb E., Haffner R., King A., Asher G., Gruss P., Lonai P., Oren M. Transgenic mouse model for studying the transcriptional activity of the p53 protein: age- and tissue-dependent changes in radiation-induced activation during embryogenesis. EMBO J. 16:1997;1381-1390.
83. Ruiz M.T., Matheos D., Price G.B., Zannis-Hadjopoulos M. OBA/Ku86: DNA binding specificity and involvement in mammalian DNA replication. Mol. Biol. Cell. 10:1999;567-580.
84. Novac O., Matheos D., Araujo F.D., Price G.B., Zannis-Hadjopoulos M. In vivo association of Ku with mammalian origins of DNA replication. Mol. Biol. Cell. 12:2001;3386-3401.
85. 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. U.S.A. 98:2001;8181-8188.
86. Kuzminov A. DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc. Natl. Acad. Sci. U.S.A. 98:2001;8461-8468.