Mammalian Rad51 protein: A RecA homologue with pleiotropic functions

Biochimie

Volumn 79, Issue 9-10, 1997, Pages 587-592

  Vispe S ^a   Defais, M ^a  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

Author keywords

DNA repair; Homologous recombination; Rad51

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; DNA; DNA BINDING PROTEIN; PROTEIN P53; RAD51 PROTEIN; RECA PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; BACTERIUM; CELL GROWTH; CONFERENCE PAPER; DNA RECOMBINATION; DNA REPAIR; MEIOSIS; NONHUMAN; ONCOGENE; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; YEAST;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 0031449639     PISSN: 03009084     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0300-9084(97)82007-X     Document Type: Conference Paper

References (87)

1. Edelmann W, Kucherlapati R (1996) Role of recombination enzymes in mammalian cell survival. Proc Natl, Acad Sci USA 93, 6225-6227
2. Thompson LH (1996) Evidence that mammalian cells possess homologous recombinational repair pathways. Mutat Res 363, 77-88
3. Roca AI, Cox MM (1997) RecA protein: structure, function, and role in recombinational DNA repair. Progr Nucleic Acid Res Mol Biol 56, 129-223
4. West SC (1992) Enzymes and molecular mechanisms of genetic recombination. Annu Rev Biochem 61, 603-640
5. Kowalczykowski SC, Dixon DA, Eggleston AK, Lauder SD, Rehrauer WM (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev 58, 401-465
6. 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
7. Aboussekhra A, Chanet R, Adjiri A, Fabre F (1992) Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Mol Cell Biol 12, 3224-3234
8. 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
9. Jang YK, Jin YH, Kim EM, Fabre F, Hong SH, Park SD (1994) Cloning and sequence analysis of rhp51+, a Schizosaccharomyces pombe homolog of the Saccharomyces cerevisiae RAD51 gene. Gene 142, 207-211
10. Shinohara A, Ogawa H, Matsuda Y, Ushio N, Ikeo K, Ogawa T (1993) Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nat Genet 4, 239-243
11. Muris DF, Vreeken K, Carr AM, Broughton BC, Lehmann AR, Lohman PH, Pastink A (1993) Cloning the RAD51 homologue of Schizosaccharomyces pombe. Nucleic Acids Res 21, 4586-4591
12. Ogawa T, Shinohara A, Nabetani A, Ikeya T, Yu X, Egelman EH, Ogawa H (1993) RecA-like recombination proteins in eukaryotes: functions and structures of RAD51 genes. Cold Spring Harb Symp Quant Biol 58, 567-576
13. Yoshimura Y, Morita T, Yamamoto A, Matsushiro A (1993) Cloning and sequence of the human RecA-like gene cDNA. Nucleic Acids Res 21, 1665
14. Jachymczyk WJ, von Borstel RC, Mowat MR, Hastings PJ (1981) Repair of interstrand cross-links in DNA of Saccharomyces cerevisiae requires two systems for DNA repair: the RAD3 system and the RAD51 system. Mol Gen Genet 182, 196-205
15. Resnick MA (1987) Investigating the genetic control of biochemical events in meiotic recombination. In: The Meiosis (Moens PB, ed) Academic Press, New-York, 157-210
16. Petes TD, Malone RE, Symington LS (1991). In: The molecular biology and cellular biology of the yeast Saccharomyces: genome dynamics, protein synthesis and energetics (Broach JR, Pringle J, Jones E, eds) Cold Spring Harbor Lab, NY, 407-521
17. Sung P (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265, 1241-1243
18. Sung P, Robberson DL (1995) DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 82, 453-461
19. Sung P, Stratton SA (1996) Yeast Rad51 recombinase mediates polar DNA strand exchange in the absence of ATP hydrolysis. J Biol Chem 271, 27983-27986
20. Clever B, Interthal H, Schmuckli-Maurer J, King J, Sigrist M, Heyer WD (1997) Recombinational repair in yeast: functional interactions between Rad51 and Rad54 proteins. EMBO J 6, 2535-2544
21. 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
22. Jiang H, Xie Y, Houston P. Stemke-Hale K, Mortensen UH, Rothstein R, Kodadek T (1996) Direct association between the yeast Rad51 and Rad54 recombination proteins. J Biol Chem 271, 33181-33186
23. Morita T, Yoshimura Y, Yamamoto A, Murata K, Mori M, Yamamoto H, Matsushiro A (1993) A mouse homolog of the Escherichia coli recA and Saccharomyces cerevisiae RAD51 genes. Proc Natl Acad Sci USA 90, 6577-6580
24. Bezzubova O, Shinohara A, Mueller RG, Ogawa H, Buerstedde JM (1993) A chicken RAD51 homologue is expressed at high levels in lymphoid and reproductive organs. Nucleic Acids Res 21, 1577-1580
25. Maeshima K, Morimatsu K, Shinohara A, Horii T (1995) RAD51 homologues in Xenopus laevis: two distinct genes are highly expressed in ovary and testis. Gene 160, 195-200
26. McKee BD, Ren X, Hong C (1996) A recA-like gene in Drosophila melanogaster that is expressed at high levels in female but not male meiotic tissues. Chromosoma 104, 479-488
27. Akaboshi E, Inoue Y, Ryo H (1994) Cloning of the cDNA and genomic DNA that correspond to the recA-like gene of Drosophila melanogaster. Jpn J Genet 69, 663-670
28. Cerutti H, Osman M, Grandoni P, Jagendorf AT (1992) A homolog of Escherichia coli RecA protein in plastids of higher plants. Proc Natl Acad Sci USA 89, 8068-8072
29. Benson FE, Stasiak A, West SC (1994) Purification and characterization of the human Rad51 protein, an analogue of E coli RecA. EMBO J 13, 5764-5771
30. Baumann P, Benson FE, West SC (1996) Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87, 757-766
31. Baumann P, West SC (1997) The human Rad51 protein: polarity of strand transfer and stimulation by hRPA. EMBO J 16, 5198-5206
32. Gupta RC, Bazemore LR, Golub EI, Radding CM (1997) Activities of human recombination protein Rad51. Proc Natl Acad Sci USA 94, 463-468
33. Shen Z, Cloud KG, Chen DJ, Park MS (1996) Specific interactions between the human RAD51 and RAD52 proteins. J Biol Chem 271, 148-152
34. Li MJ, Peakman MC, Golub EI, Reddy G, 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
35. 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
36. Barlow AL, Benson F, West SC, Hultén MA (1997) Distribution of the Rad51 recombinase in human and mouse spermatocytes. EMBO J 16, 5207-5215
37. Kovalenko OV, Plug AW, Haaf T, Gonda DK, Ashley T, Ward DC, Radding CM, Golub EI (1996) Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc Natl Acad Sci USA 93, 2958-2963
38. Shen Z, Pardington-Purtymun PE, Comeaux JC, Moyzis RK, Chen DJ (1996) Associations of UBE21 with RAD52, UBL1, p53, and RAD51 proteins in a yeast two-hybrid system. Genomics 37, 183-186
39. Shen Z, Pardington-Purtymun PE, Comeaux JC, Moyzis RK, Chen DJ (1996) UBL1, a human ubiquitin-like protein associating with human RAD51/RAD52 proteins. Genomics 36, 271-279
40. Hershko A, Ciechanover A (1992) The ubiquitin system for protein degradation. Annu Rev Biochem 61, 761-807
41. Lim DS, Hasty P (1996) A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol Cell Biol 16, 7133-7143
42. Tsuzuki T, Fujii Y, Sakumi K, Tominaga Y, Nakao K, Sekiguchi M, Matsushiro A, Yoshimura Y, MoritaT (1996) Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc Natl Acad Sci USA 93, 6236-6240
43. Taki T, Ohnishi T, Yamamoto A, Hiraga S, Arita N, Izumoto S, Hayakawa T, Morita T (1996) Antisense inhibition of the RAD51 enhances radiosensitivity. Biochem Biophys Res Commun 223, 434-438
44. 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
45. 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
46. Flygare J, Benson F, Hellgren D (1996) Expression of the human RAD51 gene during the cell cycle in primary human peripheral blood lymphocytes. Biochim Biophys Acta 1312, 231-236
47. Chen F, Nastasi A, Shen Z, Brenneman M, Crissman H, Chen DJ (1997) Cell cycle-dependent protein expression of mammalian homologs of yeast DNA double-strand break repair genes Rad51 and Rad52 [In Process Citation]. Mutat Res 384, 205-211
48. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res 51, 6304-6311
49. Lane DP (1993) Cancer. A death in the life of p53 [news; comment]. Nature 362, 786-787
50. Hansen R, Oren M (1997) p53; from inductive signal to cellular effect. Curr Opin Genet Dev 7, 46-51
51. Sturzbecher HW, Donzelmann B, Henning W, Knippschild U, Buchhop S (1996) p53 is linked directly to homologous recombination processes via Rad51/RecA protein interaction. EMBO J 15, 1992-2002
52. Buchhop S, Gibson MK, Wang XW, Wagner P, Sturzbecher HW, Harris CC (1997) Interaction of p53 with the human rad51 protein [In Process Citation]. Nucleic Acids Res 25, 3868-3874
53. Bertrand P, Rouillard D, Boulet A, Levalois C, Soussi T, Lopez BS (1997) Increase of spontaneous intrachromosomal homologous recombination in mammalian cells expressing a mutant p53 protein. Oncogene 14, 1117-1122
54. Mekeel KL, Tang W, Kachnic LA, Luo CM, DeFrank JS, Powell SN (1997) Inactivation of p53 results in high rates of homologous recombination. Oncogens 14, 1847-1857
55. Scully R, Chen J, Plug A, Xiao Y, Weaver D, Feunteun J, Ashley T, Livingston DM (1997) Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 88, 265-275
56. Sharan SK, Morimatsu M, Albrecht U, Lim DS, Regel E, Dinh C, Sands A, Eichele G, Hasty P, Bradley A (1997) Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386, 804-810
57. Feunteun J, Lenoir GM (1996) BRCA1, a gene involved in inherited predisposition to breast and ovarian cancer. Biochim Biophys Acta 1242, 177-180
58. Gayther SA, Mangion J, Russell P, Seal S, Barfoot R, Ponder BA, Stratton MR, Easton D (1997) Variation of risks of breast and ovarian cancer associated with different germline mutations of the BRCA2 gene. Nat Genet 15, 103-105
59. Suzuki A, de la Pompa JL, Hakem R, Elia A, Yoshida R, Mo R, Nishina H, Chuang T, Wakeham A, Itie A, Koo W, Billia P, Ho A, Fukumoto M, Hui CC, Mak TW (1997) Brca2 is required for embryonic cellular proliferation in the mouse. Genes Dev II, 1242-1252
60. Hakem R, de la Pompa JL, Sirard C, Mo R, Woo M, Hakem A, Wakeham A, Potter J, Reitmair A, Billia F, Firpo E, Hui CC, Roberts J, Rossant J, Mak TW (1996) The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85, 1009-1023
61. Rajan JV, Wang M, Marquis ST, Chodosh LA (1996) Brca2 is coordinately regulated with Brca1 during proliferation and differentiation in mammary epithelial cells. Proc Natl Acad Sci USA 93, 13078-13083
62. Rajan JV, Marquis ST, Gardner HP, Chodosh LA (1997) Developmental expression of Brca2 colocalizes with Brca1 and is associated with proliferation and differentiation in multiple tissues. Dev Biol 184, 385-401
63. Thomas JE, Smith M, Tonkinson JL, Rubinfeld B, Polakis P (1997) Induction of phosphorylation on BRCA1 during the cell cycle and after DNA damage. Cell Growth Differ 8, 801-809
64. Scully R, Chen J, Ochs RL, Keegan K, Hoekstra M, Feunteun J, Livingston DM (1997) Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90, 425-135
65. Hakem R, de la Pompa JL, Elia A, Potter J, Mak TW (1997) Partial rescue of Brca1 (5-6) early embryonic lethality by p53 or p21 null mutation. Nat Genet 16, 298-302
66. Ludwig T, Chapman DL, Papaioannou VE, Efstratiadis A (1997) Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev 11, 1226-1241
67. Brugarolas J, Jacks T (1997) Double indemnity: p53, BRCA and cancer. p53 mutation partially rescues developmental arrest in Brca1 and Brca2 null mice, suggesting a role for familial breast cancer genes in DNA damage repair. Nat Med 3, 721-722
68. Milner J, Ponder B, Hughes-Davies L, Seltmann M, Kouzarides T (1997) Transcriptional activation functions in BRCA2. Nature 386, 772-773
69. Monteiro AN, August A, Hanafusa H (1996) Evidence for a transcriptional activation function of BRCA1 C-terminal region. Proc Natl Acad Sci USA 93, 13595-13599
70. Maldonado E, Shiekhattar R, Sheldon M, Cho H, Drapkin R, Rickert P, Lees E, Anderson CW, Linn S, Reinberg D (1996) A human RNA polymerase II complex associated with SRB and DNA-repair proteins. Nature 381, 86-89
71. Sengstag C (1994) The role of mitotic recombination in carcinogenesis. Crit Rev Toxicol 24, 323-353
72. Flygare J, Orsan S, Hellgren D (1997) Expression of Rad51 in human cells. Mutat Res Fund Mol Mech Mutagen (suppl 1) 379, S62
73. Kaufmann SH, Desnoyers S, Ottaviano Y, Davidson NE, Poirier GG (1993) Specific proteolytic cleavage of poly (ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res 53, 3976-3985
74. Bezzubova OY, Schmidt H, Ostermann K, Heyer WD, Buerstedde JM (1993) Identification of a chicken RAD52 homologue suggests conservation of the RAD52 recombination pathway throughout the evolution of higher eukaryotes. Nucleic Acids Res 21, 5945-5949
75. Muris DF, Bezzubova O, Buerstedde JM, Vreeken K, Balajee AS, Osgood CJ, Troelstra C, Hoeijmakers JH, Ostermann K, Schmidt H et al (1994) Cloning of human and mouse genes homologous to RAD52, a yeast gene involved in DNA repair and recombination. Mutat Res 315, 295-305
76. Kanaar R, Troelstra C, Swagemakers SM, Essers J, Smit B, Franssen JH, Pastink A, Bezzubova OY, Buerstedde JM, Clever B, Heyer WD, Hoeijmakers JH (1996) Human and mouse homologs of the Saccharomyces cerevisiae RAD54 DNA repair gene: evidence for functional conservation. Curr Biol 6, 828-838
77. Friedberg EC, Siede W, Cooper AJ (1991). In: The molecular biology and cellular biology of the yeast Saccharomyces: genome dynamics, protein synthesis and energetics (Broach JR, Pringle J, Jones E, eds) Cold Spring Harbor Lab, NY, 147-192
78. Park MS (1995) Expression of human RAD52 confers resistance to ionizing radiation in mammalian cells. J Biol Chem 270, 15467-15470
79. Essers J, Hendriks RW, Swagemakers SM, Troelstra C, de Wit J, Bootsma D, Hoeijmakers JH, Kanaar R (1997) Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89, 195-204
80. -/- mutant of the chicken DT40 cell line. Cell 89, 185-193
81. Bishop DK, Park D, Xu L, Kleckner N (1992) DMC1: a meiosis-specific yeast homolog of E coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69, 439-456
82. Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79, 1081-1092
83. Habu T, Taki T, West A, Nishimune Y, Morita T (1996) The mouse and human homologs of DMC1, the yeast meiosis-specific homologous recombination gene, have a common unique form of exonskipped transcript in meiosis. Nucleic Acids Res 24, 470-477
84. Li Z, Golub E, Gupta R, Radding C (1997) Recombination activities of HsDmc1 protein, the meiotic human homolog of RecA protein. Proc Natl Acad Sci USA 94, 11221-11226
85. Tebbs RS, Zhao Y, Tucker JD, Scheerer JB, Siciliano MJ, Hwang M, Liu N, Legerski RJ, Thompson LH (1995) Correction of chromosomal instability and sensitivity to diverse mutagens by a cloned cDNA of the XRCC3 DNA repair gene. Proc Natl Acad Sci USA 92, 6354-6358
86. Liu N, Lamerdin JE, Siciliano MJ, Carrano AV (1995) Molecular cloning of the XRCC2 human DNA repair gene, which is similar to RAD51 of S cerevisiae. Am J Hum Genet (suppl 57), A147
87. Doutriaux MP, Couteau F, Bergougnioux C, White C (1998) Isolation and characterization of the RAD51 and DMC1 homologues from Arabidopsis thaliana. Mol Gen Genet, in press