The RAD52 epistasis group in mammalian double strand break repair

Seminars in Immunology

Volumn 9, Issue 3, 1997, Pages 181-188

  Petrini, John H J ^a   Bressan, Debra A ^a   Yao, Michelle S ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Double strand break repair; Homologous recombination; Illegitimate recombination; Ionizing radiation; Recombinational DNA repair

Indexed keywords

DOUBLE STRANDED DNA; PROTEIN;

ARTICLE; DNA DAMAGE; DNA REPAIR; EPISTASIS; MAMMAL CELL; RADIATION; SACCHAROMYCES CEREVISIAE; T LYMPHOCYTE;

EID: 0031171269     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1006/smim.1997.0067     Document Type: Article

References (95)

1. 1. Game JC (1993) DNA double strand breaks and the RAD50-RAD57 genes in Saccharomyces. Cancer Biol 4:73-83
2. 2. Weaver DT (1995) What to do at an end: DNA double-strand break repair. Trends Genet 11:388-392
3. 3. Haber JE (1992) Exploring the pathways of homologous recombination. Curr Opin Cell Biol 4:401-412
4. 4. Bollag RJ, Waldman AS, Liskay RM (1989) Homologous recombination in mammalian cells. Annu Rev Genet 23:199-225
5. 5. Meyn MS (1995) Ataxia-telangiectasia and cellular responses to DNA damage. Cancer Res 55:5991-6001
6. 6. Hartwell L (1992) Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 71:543-546
7. 7. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand break repair model for recombination. Cell 33:25-35
8. 8. Kadyk LC, Hartwell LH (1992) Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132:387-402
9. 9. Bai Y, Symington L (1996) A Rad52 homolog is required for RAD51-independent mitotic recombination in Saccharomyces cerevisiae. Genes Dev 10:2025-2037
10. 10. Ajimura M, Leem S-H, Ogawa H (1993) Identification of new genes required for meiotic recombination in Saccharomyces cerevisiae. Genetics 133:51-66
11. 11. Ivanov EL, Korolev VG, Fabre F (1992) XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics 132:651-664
12. 12. Shinohara A, Ogawa H, Matsuda Y, Ushio N, Ikeo K, Ogawa T (1993) Cloning of the human, mouse, and fission yeast recombination genes homologous to RAD51 and recA. Nat Genet 4:239-243
13. 13. Kanaar R, Troelstra C, Swagemakers SMA, Essers J, Smit B, Franssen J-H, Pastink A, Bezzubova OY, Buerstedde J-M, Clever B, Heyer W-D, Hoeijmakers JHJ (1996) Human and mouse homologs of the Saccharomyces cerevisiae RAD54 DNA repair gene: evidence for functional conservation. Curr Biol 6:828-838
14. 14. Petrini JHJ, Walsh ME, Di Mare C, Korenberg JR, Chen X-N, Weaver DT (1995) Isolation and characterization of the human MRE11 homologue. Genomics 29:80-86
15. 15. Dolganov GM, Maser RS, Novikov A, Tosto L, Chong S, Bressan DA, Petrini JHJ (1996) Human Rad50 is physically associated with h Mre11: identification of a conserved multiprotein complex implicated in recombinational DNA repair. Mol Cell Biol 16:4832-4841
16. 16. Shen Z, Denison K, Lobb R, Gatewood JM, Chen DJ (1995) The human and mouse homologs of the yeast RAD52 gene: cDNA cloning, sequence analysis, assignment to human chromosome 12p12.2-p13, and mRNA expression in mouse testis. Genomics 25:199-206
17. 17. Bendixen C, Sunjevaric I, Bauchwitz R, Rothstein R (1994) Identification of a mouse homologue of the Saccharomyces cerevisiae recombination and repair gene, RAD52. Genomics 23:300-303
18. 18. Johzhuka K, Ogawa H (1995) Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics 139:1521-1532
19. 19. Shinohara A, Ogawa H, Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69:457-470
20. 20. Milne GT, Weaver DT (1993) Dominant negative alleles of RAD52 reveal a DNA repair/ recombination complex including Rad51 and Rad52. Genes Dev 7:1755-1765
21. 21. Donovan JW, Milne GT, Weaver DT (1994) Homotypic and heterotypic protein association control RAD51 function in double strand break repair. Genes Dev 8:2552-2562
22. 22. Hays SL, Firmenich AA, Berg P (1995) Complex formation in yeast double-strand break repair: Participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc Natl Acad Sci USA 92:6925-6929
23. 23. Johnson RD, Symington LS (1995) Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol Cell Biol 15:4843-4850
24. 24. Shen Z, Cloud KG, Chen DJ, Park MS (1996) Specific interactions between the human Rad52 and Rad52 proteins. J Biol Chem 271:148-152
25. 25. Alani E, Padmore R, Kleckner N (1990) Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61:419-436
26. 26. Resnick MA (1987) Investigating the genetic control of biochemical events in meiotic recombination, in Meiosis (Moens PB, ed.) pp 157-210. Academic Press, New York
27. 27. Friedberg EC (1988) Deoxyribonucleic acid repair in the yeast Saccharomyces cerevisiae. Microbiol Rev 52:70-102
28. 28. Ivanov EL, Sugawara N, White CI, Fabre F, Haber JE (1994) Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol Cell Biol 14:3414-3425
29. 29. Malone RE, Ward T, Lin S, Waring J (1990) The RAD50 gene, a member of the double strand break repair epistasis group, is not required for spontaneous mitotic recombination in yeast. Curr Genet 18:111-116
30. 30. Schiestl RH, Zhu J, Petes TD (1994) Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisae. Mol Cell Biol 14:4495-4500
31. 31. Moore JK, Haber JE (1996) Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol Cell Biol 16:2164-2173
32. 32. Tsukamoto Y, Kato J, Ikeda H (1996) Effects of mutations of RAD50, RAD51, RAD52 and related genes on illegitimate recombination in Saccharomyces cerevisiae. Genetics 142:383-391
33. 33. Thomas KR, Capecchi MR (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51:503-512
34. 34. Weinert TA, Kiser GL, Hartwell LH (1994) Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev 8:652-665
35. 35. Allen JB, Zhou Z, Siede W, Friedberg EC, Elledge SJ (1994) The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev 8:2401-2415
36. 36. Sanchez Y, Desany BA, Jones WJ, Liu Q, Wang B, Elledge SJ (1996) Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271:357-360
37. 37. Morrow DM, Tagle DA, Shiloh Y, Collins FS, Hieter P (1995) TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell 82:831-840
38. 38. Greenwell PW, Kronmal SL, Porter SE, Gassenhuber J, Obermaier B, Petes TD (1995) TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell 82:823-829
39. 39. Savitsky K, Sfez S, Tagle DA, Ziv Y, Sartiel A, Collins FS, Shiloh Y, Rotman G (1995) The complete sequence of the coding region of the ATM gene reveals similarity to cell cycle regulators in different species. Hum Mol Genet 4:2025-2032
40. 40. Valancius V, Smithies O (1991) Double-strand gap repair in a mammalian gene targeting reaction. Mol Cell Biol 11:4389-4397
41. 41. Roth DB, Wilson JH (1988) Illegitimate recombination in mammalian cells, in Genetic Recombination (Kucherlapati R, Smith GR, eds) pp 621-654. American Society for Microbiology, Washington DC
42. 42. Roth DB, Wilson JH (1985) Relative rates of homologous and nonhomologous recombination in transfected DNA. Proc Natl Acad Sci USA 82:3355-3359
43. 43. Godwin AR, Bollag RJ, Christie DM, Liskay RM (1994) Spontaneous and restriction enzyme-induced chromosomal recombination in mammalian cells. Proc Natl Acad Sci USA 91:12554-12558
44. 44. Thompson LH (1988) Mammalian cell mutations affecting recombination, in Genetic Recombination (Kucherlapati R, Smith GR, eds) pp 597-620. American Society for Microbiology, Washington DC
45. 45. Benjamin MB, Little JB (1992) X rays induce interallelic homologous recombination at the thymidine kinase gene. Mol Cell Biol 12:2730-2738
46. 46. Wang Y, Maher V, Liskay RM, McCormick JJ (1988) Carcinogens can induce homologous recombination between duplicated chromosomal sequences in mouse L cells. Mol Cell Biol 8:196-202
47. 47. Rouet P, Smih F, Jasin M (1994) Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc Natl Acad Sci USA 91:6064-6068
48. 48. Choulika A, Perrin A, Dujon B, Nicolas JF (1995) Induction of homologous recombination in mammalian chromosomes by using the I-Scel system of Saccharomyces cerevisiae. Mol Cell Biol 15:1968-1973
49. 49. Smih F, Rouet P, Romanienko PJ, Jasin M (1995) Double-strand breaks at the target locus stimulate gene targeting in embryonic stem cells. Nucleic Acids Res 23:5012-5019
50. 50. Morrow B, Kucherlapati R (1993) Gene targeting in mammalian cells by homologous recombination. Curr Opin Biotech 4:577-582
51. 51. Tsujimura T, Maher VM, Godwin AR, Liskay RM, McCormick JJ (1990) Frequency of intrachromosomal homologous recombination induced by UV irradiation of normally repairing and excision repair-deficient human cells. Proc Natl Acad Sci USA 87:1566-1570
52. 52. Bollag RJ, Elwood DR, Tobin ED, Godwin AR, Liskay RM (1992) Formation of heteroduplex DNA during mammalian intrachromosomal gene conversion. Mol Cell Biol 12:1546-1552
53. 53. Bollag RJ, Liskay RM (1988) Conservative intrachromosomal recombination between inverted repeats in mouse cells: association between reciprocal exchange and gene conversion. Genetics 119:161-169
54. 54. Maizels N (1989) Might gene conversion be the mechanism of somatic mutation of mammalian immunoglobulin genes? Trends Genet 5:4-8
55. 55. Becker RS, Knight KL (1990) Somatic diversification of immunoglobulin heavy chain VDJ genes: evidence for somatic gene conversion in rabbits. Cell 63:987-997
56. 56. Giaccia A, Weinstein R, Hu J, Stamato TD (1985) Cell cycle-dependent repair of double-strand DNA breaks in a gamma-ray-sensitive Chinese hamster cell. Somat Cell Mol Genet 11:485491
57. 57. Whitemore GF, Varghese AJ, Gulyas S (1989) Cell cycle responses of two X-ray sensitive mutants defective in DNA repair. Int J Radiat Biol 56:657-665
58. 58. Jeggo PA, Kemp LM (1983) X-ray sensitive mutants of Chinese hamster ovary cell line: isolation and cross-sensitivity to other DNA damaging agents. Mutat Res 112:313-327
59. 59. Blunt T, Finnie NJ, Taccioli GE, Smith GC, Demengeot J, Gottlieb TM, Mizuta R, Varghese AJ, Alt FW, Jeggo PA, Jackson SP (1995) Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80:813-823
60. 60. Porges AJ, Ng T, Reeves WH (1990) Antigenic determinants of the Ku (p70/p80) autoantigen are poorly conserved between species. J Immunol 145:4222-4228
61. 61. Reeves WH, Sthoeger ZM (1989) Molecular cloning of cDNA encoding the p70 (Ku) lupus autoantigen. J Biol Chem 264:5047-5052
62. 62. Li Z, Otevrel T, Gao Y, Cheng H-L, Seed B, Stamato TD, Taccioli GE, Alt FW (1995) The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination. Cell 83:1079-1089
63. 63. Biedermann KA, Sun J, Giaccia AJ, Tosto LM, Brown JM (1991) scid mutation in mice confers hypersensitivity to ionizing radiation and a deficiency in DNA double-strand break repair. Proc Natl Acad Sci USA 88:1394-1397
64. 64. Hendrickson EA, Qin X-Q, Bump EA, Schatz DG, Oettinger M, Weaver DT (1991) A link between double-strand break-related repair and V(D)J recombination: the scid mutation. Proc Natl Acad Sci USA 88:4061-4065
65. 65. Taccioli GE, Rathbun G, Oltz E, Stamato T, Jeggo PA, Alt FW (1993) Impairment of V(D)J recombination in double-strand break repair mutants. Science 260:207-210
66. 66. Taccioli GE, Gottlieb TM, Blunt T, Priestley A, Demengeot J, Mizuta R, Lehmann AR, Alt FW, Jackson SP, Jeggo PA (1994) Ku80: Product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 265:1442-1445
67. 67. Boubnov NV, Hall KT, Wills Z, Lee SE, He DM, Benjamin DM, Pulaski CR, Band H, Reeves W, Hendrickson EA, Weaver DT (1995) Complementation of the ionizing radiation sensitivity, DNA end binding, and V(D) J recombination defects of double-strand break repair mutants by the p86 Ku autoantigen. Proc Natl Acad Sci USA 92:890-894
68. 68. Jackson SP, Jeggo PA (1995) DNA double-strand break repair and V(D)J recombination: involvement of DNA-PK Trends Biochem Sci 20:412-415
69. 69. Jeggo PA, Taccioli GE, Jackson SP (1995) Menage a trois: double strand break repair, V(D)J recombination and DNA-PK. Bioessays 17:949-957
70. 70. Jones NJ, Cox R, Thacker J (1988) Six complementation groups for ionising radiation sensitivity in Chinese hamster cells. Mutat Res 193:139-144
71. 71. Jeggo PA, Tesmer J, Chen DJ (1991) Genetic analysis of ionizing radiation sensitive mutants of cultured mammalian cell lines. Mutat Res 254:125-133
72. 72. Verhaegh GW, Jongmans W, Morolli B, Jaspers NG, van der Schans GP, Lohman PH, Zdzienicka MZ (1995) A novel type of X-ray-sensitive Chinese hamster cell mutant with radioresistant DNA synthesis and hampered DNA double-strand break repair. Mutat Res 337:119-129
73. 73. Lee SE, Pulaski CR, He DM, Benjamin DM, Voss M, Um J, Hendrickson EA (1995) Isolation of mammalian cell mutants that are X-ray sensitive, impaired in DNA double-strand break repair and defective for V(D)J recombination. Mutat Res 336:279-291
74. 74. Thompson LH, Brookman KW, Jones NJ, Allen SA, Carrano AV (1990) Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange. Mol Cell Biol 10:6160-6171
75. 75. Yamamoto A, Taki T, Yagi H, Habu T, Yoshida K, Yoshimura Y, Yamamoto K, Matsushiro A, Nishimune Y, Morita T (1996) Cell cycle-dependent expression of the mouse Rad51 gene in proliferating cells. Mol Gen Genet 251:1-12
76. 76. Plug AW, Xu J, Reddy G, Golub EI, Ashley T (1996) Presynaptic association of Rad51 protein with selected sites in meiotic chromatin. Proc Natl Acad Sci USA 93:5920-5924
77. 77. Muris DFR, Bezzubova O, Buerstedde JM, Vreeken K, Balajee AS, Osgood CJ, Troelstra C, Hoeijmakers JHJ, Ostermann K, Schmidt H, Natarajan AT, Eeken JCJ, Lohman PHM, Pastink A (1994) Cloning of human and mouse genes homologous to RAD52, a yeast gene involved in DNA repair and recombination. Mutat Res 315:295-305
78. 78. Li M-J, Peakman M, Golub EI, ReddyG, Ward DC, Radding CM, Maizels N (1996) Rad51 expression and localization in B cells carrying out class switch recombination. Proc Natl Acad Sci USA 93:10222-10227
79. 79. Park MS (1995) Expression of human RAD52 confers resistance to ionizing radiation in mammalian cells. J Biol Chem 270:15467-15470
80. 80. Tsuzuki T , Fujii Y, Sakumi K, Tominaga Y, Nakao K, Sekiguchi M, Matsushiro A, Yoshimura Y, Morita T (1996) Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc Natl Acad Sci USA 93:6236-6240
81. 81. Haaf T, Golub EI, Reddy G, Radding CM, Ward DC (1995) Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci USA 92:2298-2302
82. 82. Boulton SJ, Jackson SP (1996) Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J 15:5093-5103
83. 83. Milne GT, Jin S, Shannon KB, Weaver DT (1996) Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol Cell Biol 16:4189-4198
84. 84. Lin WC, Desiderio S (1995) V(D)J recombination and the cell cycle. Immunol Today 16:279-289
85. 85. Basile G, Aker M, Mortimer RK (1992) Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51 Mol Cell Biol 12:3235-3246
86. 86. Johnston LH, Johnson AL (1995) The DNA repair genes RAD54 and UNG1 are cell cycle regulated in budding yeast but MCB promoter elements have no essential role in the DNA damage response. Nucleic Acids Res 23:2147-2152
87. 87. Tashiro S, Kotomura N, Shinohara A, Tanaka K, Ueda K, Kamada N (1996) S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes. Oncogene 12:2165-2170
88. 88. Sugawara N, Ivanov EL, Fishman-Lobell J, Ray BL, Wu X, Haber JE (1995) DNA structure-dependent requirements for yeast RAD genes in gene conversion. Nature 373:84-86
89. 89. Blackwell TK, Alt FW (1989) Mechanism and developmental program of immunoglobulin gene rearrangement in mammals. Annu Rev Genet 23:605-636
90. 90. Stanhope-Baker P, Hudson KM, Shaffer AL, Constantinescu A, Schlissel MS (1996) Cell type-specific chromatin structure determines the targeting Of V(D)J recombinase activity in vitro. Cell 85:887-897
91. 91. Lutzker S, Rothman P, Pollock R, Coffman R, Alt FW (1988) Mitogen- and IL-4-egulated expression of germ-line Ig γ2b transcripts: evidence for directed heavy chain class switching. Cell 53:177-184
92. 92. Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443-453
93. 93. Petes TD, Malone RE, Symington LE (1991) Recombination in yeast, in The Molecular and Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis, and Energetics (Broach JR, Pringle J, Jones E, eds) pp 407-521. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
94. 94. Mezard C, Nicolas A (1994) Homologous, homeologous, and illegitimate repair of double-strand breaks during transformation of a wild-type strain and a rad52 mutant strain of Saccharomyces cerevisiae. Mol Cell Biol 14:1278-1292
95. 95. Kramer KM, Brock JA, Bloom K, Moore JK, Haber JE (1994) Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol Cell Biol 14:1293-1301