Rad54: The Swiss Army knife of homologous recombination?

Nucleic Acids Research

Volumn 34, Issue 15, 2006, Pages 4115-4125

  Heyer, Wolf Dietrich ^a   Li, Xuan ^a   Rolfsmeier, Michael ^a   Zhang, Xiao Ping ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RAD51 PROTEIN; RAD54 PROTEIN; DNA BINDING PROTEIN; RAD52 PROTEIN; RAD54 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SNF2 PROTEIN, S CEREVISIAE; TRANSCRIPTION FACTOR;

CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME SEGREGATION; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA SEQUENCE; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; MEIOSIS; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SACCHAROMYCES CEREVISIAE; SULFOLOBUS SOLFATARICUS; BIOLOGICAL MODEL; CHEMISTRY; GENETIC RECOMBINATION; GENETICS; PHYSIOLOGY;

DNA REPAIR; DNA-BINDING PROTEINS; MODELS, BIOLOGICAL; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 33748713412     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl481     Document Type: Review

References (109)

1. Paques,F. and Haber,J.E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 63, 349-404.
2. Michel,B., Grompone,G., Flores,M.J. and Bidnenko,V. (2004) Multiple pathways process stalled replication forks. Proc. Natl Acad. Sci. USA, 101, 12783-12788.
3. Gorbalenya,A.E. and Koonin,E.V. (1993) Helicases - amino acid sequence comparisons and structure function relationships. Curr. Opin. Struct. Biol., 3, 419-429.
4. Pazin,M.J. and Kadonaga,J.T. (1997) SWI2/SNF2 and related proteins: ATP-driven motors that disrupt protein-DNA interactions? Cell, 88, 737-740.
5. Sung,P., Trujillo,K.M. and Van Komen,S. (2000) Recombination factors of Saccharomyces cerevisiae. Mutat. Res., 451, 257-275.
6. Symington,L.S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev., 66, 630-670.
7. Krogh,B.O. and Symington,L.S. (2004) Recombination proteins in yeast. Annu. Rev. Genet., 38, 233-271.
8. West,S.C. (2003) Molecular views of recombination proteins and their control. Nature Rev. Mol. Cell. Biol., 4, 435-445.
9. Vignali,M., Hassan,A.H., Neely,K.E. and Workman,J.L. (2000) ATP-dependent chromatin-remodeling complexes. Mol. Cell. Biol., 20, 1899-1910.
10. Becker,P.B. and Hörz,W. (2002) ATP-dependent nucleosome remodeling. Annu. Rev. Biochem., 71, 247-273.
11. Martens,J.A. and Winston,F. (2003) Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr. Opin. Genet. Dev., 13, 136-142.
12. Tan,T.L.R., Kanaar,R. and Wyman,C. (2003) Rad54, a Jack of all trades in homologous recombination. DNA Repair, 2, 787-794.
13. Szostak,J.W., Orr-Weaver,T.L., Rothstein,R.J. and Stahl,F.W. (1983) The double-strand-break repair model for recombination. Cell, 33, 25-35.
14. Malkova,A.,Ivanov,E.L. and Haber,J.E. (1996) Double-strand break repair in the absence of RAD51 in yeast: A possible role for break-induced DNA replication. Proc. Natl Acad. Sci. USA, 93, 7131-7136.
15. Yang,H.J., Li,Q.B., Fan,J., Holloman,W.K. and Pavletich,N.P. (2005) The BRCA2 homologue Brh2 nucleates RAD51 filament formation at a dsDNA-ssDNA junction. Nature, 433, 653-657.
16. Lisby,M., Barlow,J.H., Burgess,R.C. and Rothstein,R. (2004) Choreography of the DNA damage response: Spatiotemporal relationships among checkpoint and repair proteins. Cell, 118, 699-713.
17. Game,J.C. and Mortimer,R.K. (1974) A genetic study of X-ray sensitive mutants in yeast. Mutat. Res., 24, 281-292.
18. Suslova,N.G. and Zakharov,I.A. (1970) Genetic control of radiosensitivity in yeast, VII. Identification of the genes determining the sensitivity to X-rays. Genetika, 6, 158.
19. Snow,R. (1967) Mutants of yeast sensitive to ultraviolet light. J. Bact., 94, 571-575.
20. Schmuckli-Maurer,J. and Heyer,W.-D. (1999) The Saccharomyces cerevisiae RAD54 gene is important but not essential for natural homothallic mating-type switching. Mol. Gen. Genet., 260, 551-558.
21. Shinohara,M., Shita-Yamaguchi,E., Buerstedde,J.M., Shinagawa,H., Ogawa,H. and Shinohara,A. (1997) Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/ TID1, in mitosis and meiosis. Genetics, 147, 1545-1556.
22. Schmuckli-Maurer,J., Rolfsmeier,N., Nguyen,H. and Heyer,W.-D. (2003) Genome instability in RAD54 mutants of Saccharomyces cerevisiae. Nucleic Acids Res., 31, 1013-1023.
23. Saeki,T., Machida,I. and Nakai,S. (1980) Genetic control of diploid recovery after g-irradiation in the yeast Saccharomyces cerevisiae. Mutat. Res., 73, 3314-3322.
24. Schmuckli-Maurer,J. and Heyer,W.D. (2000) Meiotic recombination in RAD54 mutants of Saccharomyces cerevisiae. Chromosoma, 109, 86-93.
25. Klein,H.L. (1997) RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis. Genetics, 147, 1533-1543.
26. Arbel,A., Zenvirth,D. and Simchen,G. (1999) Sister chromatid-based DNA repair is mediated by RAD54, not by DMC1 or 7ID1. EMBO J., 18, 2648-2658.
27. Seitz,E.M., Haseltine,C.A. and Kowalczykowski,S.C. (2001) DNA recombination and repair in Archaea. Adv. Appl. Microbiol., 50, 101-169
28. Essers,J., Hendriks,R.W., Swagemakers,S.M.A., Troelstra,C., deWit,J., Bootsma,D., Hoeijmakers,J.H.J. and Kanaar,R. (1997) Disruption of mouse RAD54 reduces ionizing radiation resistance. Cell, 89, 195-204.
29. (-1-) mutant of the chicken DT40 cell line. Cell. 89. 185-193.
30. Lim,D.S. and 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.
31. Tsuzuki,T., Fujii,Y., Sakumi,K., Tominaga,Y., Nakao,K., Sekiguchi, M., Matsushiro, A., Yoshimura, Y. and Morita, T. (1996) Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl Acad. Sci. USA, 93, 6236-6240.
32. Rijkers,T., VandenOuweland,J., Morolli,B., Rolink,A.G., Baarends,W.M., VanSloun,P.P.H., Lohman,P.H.M. and Pastink,A. (1998) Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol., 18, 6423-6429.
33. Essers,J., Hendriks,R.W., Wesoly,J., Beerens,C., Smit,B., Hoeijmakers,J.H.J., Wyman,C., Dronkert,M.L.G. and Kanaar,R. (2002) Analysis of mouse Rad54 expression and its implications for homologous recombination. DNA Repair, 1, 779-793.
34. Essers,J., van Steeg,H., de Wit,J., Swagemakers,S.M.A., Vermeij,M., Hoeijmakers,J.H.J. and Kanaar,R. (2000) Homologous and non-homologous recombination differentially affect DNA damage repair in mice. EMBO J., 19, 1703-1710.
35. Mills,K.D., Ferguson,D.O., Essers,J., Eckersdorff,M., Kanaar,R. and Alt,F.W. (2004) Rad54 and DNA Ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev., 18, 1283-1292.
36. Dronkert,M.L.G., Beverloo,H.B., Johnson,R.D., Hoeijmakers,J.H.J., Jasin,M. and Kanaar,R. (2000) Mouse RAD54 affects DNA double-strand break repair and sister chromatid exchange. Mol. Cell. Biol., 20, 3147-3156.
37. Kiianitsa,K Solinger,J.A. and Heyer,W.D. (2002) Rad54 protein exerts diverse modes of ATPase activity on duplex DNA partially and fully covered with Rad51 protein. J. Biol. Chem., 277, 46205-46215.
38. Petukhova,G., Stratton,S. and Sung,P. (1999) Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature, 393, 91-94.
39. Swagemakers,S.M.A., Essers,J., de Wit,J., Hoeijmakers,J.H.J. and Kanaar,R. (1998) The human Rad54 recombinational DNA repair protein is a double-stranded DNA-dependent ATPase. J. Biol. Chem., 273, 28292-28297.
40. Singleton,M.R. and Wigley,D.B. (2002) Modularity and specialization in Superfamiy 1 and 2 helicases. J. Bact., 184, 1819-1826.
41. Tan,T.L.R., Essers,J., Citterio,E., Swagemakers,S.M.A., de Wit,J., Benson,F.E., Hoeijmakers,J.H.J. and Kanaar,R. (1999) Mouse Rad54 affects DNA conformation and DNA-damage-induced Rad51 foci formation. Curr. Biol., 9, 325-328.
42. Mazin,A.V., Bornarth,C.J., Solinger,J.A., Heyer,W.-D. and Kowalczykowski,S.C. (2000) Rad54 protein is targeted to pairing loci by the Rad51 nucleoprotein filament. Mol. Cell, 6, 583-592.
43. Van Komen,S., Petukhova,G., Sigurdsson,S., Stratton,S. and Sung,P. (2000) Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol. Cell, 6, 563-572.
44. Jaskelioff,M., Van Komen,S., Krebs,J.E., Sung,P. and Peterson,C.L. (2003) Rad54p is a chromatin remodeling enzyme required for heteroduplex joint formation with chromatin. J. Biol. Chem., 278, 9212-9218.
45. Ristic,D., Wyman,C., Paulusma,C. and Kanaar,R. (2001) The architecture of the human Rad54 - DNA complex provides evidence for protein translocation along DNA. Proc. Natl Acad. Sci. USA, 98, 8454-8460.
46. Amitani,I., Baskin,R.J. and Kowaiczykowski,S. (2006) Direct visualization of a chromatin-remodeling protein, Rad54, translocating along single-molecules of double-stranded DNA. Mol. Cell, 23, 143-148.
47. Thoma,N.H., Czyzewski,B.K., Alexeev,A.A., Mazin,A.V., Kowalczykowski,S.C. and Pavletich,N.P. (2005) Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nature Struct. Mol. Biol., 12, 350-356.
48. Dürr H Kömer C Müller M. Hickmann V and Hopfner K P (2005) X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell, 121, 363-373.
49. Singleton,M.R., Scaife,S. and Wigley,D.B. (2001) Structural analysis of DNA replication fork reversal by RecG. Cell, 107, 79-89.
50. Clever,B., Interthal,H., Schmuckli-Maurer,J., King,J., Sigrist,M. and Heyer,W.D. (1997) Recombinational repair in yeast: Functional interactions between. Rad51 and Rad54 proteins. EMBO J., 16, 2535-2544.
51. Jiang,H., Xie,Y.Q., Houston,P., Stemke-Hate,K., Mortensen,U.H., Rothstein,R. and Kodadek,T. (1996) Direct association between the yeast Rad51 and Rad54 recombination proteins. J. Biol. Chem., 271, 33181-33186.
52. Golub,E.I., Kovalenko,O.V., Gupta,K.C., Ward,D.C. and Radding,C.M. (1997) Interaction of human recombination proteins Rad51 and Rad54. Nucleic Acids Res., 25, 4106-4110.
53. Wolner,B., van Komen,S., Sung,P. and Peterson,C.L. (2003) Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell, 12, 221-232.
54. Sung,P., Krejci,L., Van Komen,S. and Sehorn,M.G. (2003) Rad51 recombinase and recombination mediators. J. Biol. Chem., 278, 42729-42732.
55. Mazin,A.V., Alexeev,A.A. and Kowalczykowski,S.C. (2003) A novel function of Rad54 protein - Stabilization of the Rad51 nucleoprotein filament. J. Biol. Chem., 278, 14029-14036.
56. Solinger,J.A., Kiianitsa,K. and Heyer,W.-D. (2002) Rad54, a Swi2/ Snf2-like recombinational repair protein, disassembles Rad51:dSDNA filaments. Mol. Cell, 10, 1175-1188.
57. Wolner,B. and Peterson,C.L. (2005) ATP-dependent and ATP-independent roles for the Rad54 chromatin remodeling enzyme during recombinational repair of a DNA double strand break. J. Biol. Chem., 280, 10855-10860.
58. Petukhova.G., Van Komen,S., Vergano,S., Klein,H. and Sung,P. (1999) Yeast Rad54 promotes Rad51-dependent homologous DNA pairing via ATP hydrolysis-driven change in DNA double helix conformation. J. Biol. Chem., 274, 29453-29462.
59. Clever,B., Schmuckli-Maurer,J., Sigrist,M., Glassner,B. and Heyer,W.-D. (1999) Specific negative effects resulting from elevated levels of the recombinational repair protein Rad54p in Saccharomyces cerevisiae. Yeast, 15, 721-740.
60. Shinohara,M., Gasior,S.L., Bishop,D.K. and Shinohara,A. (2000) Tid1/ Rdh54 promotes colocalization of Rad51 and Dmc1 during meiotic recombination. Proc. Natl Acad. Sci. USA, 97, 10914-10819.
61. Miyazaki,T., Bressan,D.A., Shinohara,M., Haber,J.E. and Shinohara,A. (2004) In vivo assembly and disassembly of Rad51 and Rad52 complexes during double-strand break repair. EMBO J., 23, 939-949.
62. Takata,M., Sasaki,M.S., Sonoda,E., Fukushima,T., Morrison,C., Albala,J.S., Swagemakers,S.M.A., Kanaar,R., Thompson,L.H. and Takeda,S. (2000) The Rad51 paralog Rad51B promotes homologous recombinational repair. Mol. Cell. Biol., 20, 6476-6482.
63. van Veelen,L.R., Essers,J., van de Rakt,M., Odijk,H., Pastink,A., Zdzienicka,M.Z., Paulusma,C.C. and Kanaar,R. (2005) Ionizing radiation-induced foci formation of mammalian Rad51 and Rad54 depends on the Rad51 paralogs, but not on Rad52. 574, 34-49.
64. Sigurdsson,S., Van Komen,S., Petukhova,G. and Sung,P. (2002) Homologous DNA pairing by human recombination factors Rad51 and Rad54. J. Biol. Chem., 277, 42790-42794.
65. Solinger,J.A., Lutz,G., Sugiyama,T., Kowalczykowski,S.C. and Heyer,W.-D. (2001) Rad54 protein stimulates heteroduplex DNA formation in the synaptic phase of DNA strand exchange via specific interactions with the presynaptic Rad51 nucleoprotein filament. J. Mol. Biol., 307, 1207-1221.
66. Van Komen,S., Petukhova,G., Sigurdsson,S. and Sung,P. (2002) Functional cross-talk among Rad51, Rad54, and replication protein A in heteroduplex DNA joint formation. J. Biol. Chem., 277, 43578-43587.
67. Mazin,O.M. and Mazin,A.W. (2004) Human Rad54 protein stimulates DNA strand exchange activity of bRad51 protein in the presence of Ca2+. J. Biol. Chem., 279, 52041-52051.
68. Rattray,A.J. and Symington,L.S. (1995) Multiple pathways for homologous recombination in Saccharomyces cerevisiae. Genetics, 139, 45-56.
69. Palladino,F. and Klein,H.L. (1992) Analysis of mitotic and meiotic defect in Saccharomyces cerevisiae SRS2 DNA helicase mntants. Genetics, 132, 23-37.
70. Krejci,L., Van Komen,S., Li,Y., Villemain,J., Reddy,M.S., Klein,H., Ellenberger,T. and Sung,P. (2003) DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature, 423, 305-309.
71. Veaute,X., Jeusset,J., Soustelle,C., Kowalczykowski,S.C., Le Cam,E. and Fabre,F. (2003) The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature, 423, 309-312.
72. Aboussekhra,A., Chanet,R., Zgaga,Z., Cassier Chauvat,C., Heude,M. and Fabre,F. (1989) RADH, a gene of Saccharomyces cerevisiae encoding a putative DNA helicase involved in DNA repair. Characteristics of radH mutants and sequence of the gene. Nucleic Acids Res., 17, 7211-7219.
73. Aboussekhra,A., Chanet,R., Adjiri,A. and Fabre,F. (1992) Semi-dominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA protein. Mol. Cell. Biol., 12, 3224-3234.
74. Heude,M., Chanet,J.L. and Fabre,F. (1995) Regulation of the Saccharomyces cerevisiae Srs2 helicase during the mitotic cell cycle, meiosis and after irradiation. Mol. Gen. Genet, 248, 59-68.
75. Schild,D. (1995) Suppression of a new allele of the yeast RAD52 gene by overexpression of RAD51, mutations in srs2 and ccr4, or mating-type heterozygosity. Genetics, 140, 115-127.
76. Solinger,J.A. and Heyer,W.-D. (2001) Rad54 protein stimulates the postsynaptic phase of Rad51 protein-mediated DNA strand exchange. Proc. Natl Acad. Sci. USA, 98, 8447-8453.
77. Sung,P. (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science, 265, 1241-1243.
78. Zaitseva,E.M., Zaitsev,E.N. and Kowalezykowski,S.C. (1999) The DNA binding properties of Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem., 274, 2907-2915.
79. Bianco,P.R., Tracy,R.B. and Kowalczykowski,S.C. (1998) DNA strand exchange proteins: A biochemical and physical comparison. Front. Biosci., 3, 570-603.
80. Xu,L. and Marians,K.J. (2002) A dynamic RecA filament permits DNA polymemse-catalyzed extension of the invading strand in recombination intermediates. J. Biol. Chem., 277, 14321-14328.
81. Kiianitsa,K., Solinger,J.A. and Heyer,W.D. (2006) Terminal association of the Rad54 protein with the Rad51-dsDNA filament. Proc. Natl Acad. Sci. USA, 103, 9767-9772.
82. Wesoly,J., Agarwal,S., Sigurdsson,S., Bussen,W., Van Komen,S., Qin,J.A., van Steeg,H., van Benthem,J., Wassenaar,E., Baarends,W.M. et al. (2006) Differential contributions of mammalian Rad54 paralogs to recombination, DNA damage repair, and meiosis. Mol. Cell. Biol., 26, 976-989.
83. Sugawara,N., Wang,X. and Haber,J.E. (2003) In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell, 12, 209-219.
84. Alexeev,A., Mazin,A. and Kowalczykowski,S.C. (2003) Rad54 protein possesses chromatin-remodeling activity stimulated by a Rad51-ssDNA nucleoprotein filament. Nature Struct. Biol., 10, 182-186.
85. Alexiadis,V. and Kadonaga,J.T. (2003) Strand pairing by Rad54 and Rad51 is enhanced by chromatin. Genes Dev., 16, 2767-2771.
86. Sugawara,N., Ivanov,E.L., Fishman Lobell,J., Ray,B.L., Wu,X. and Haber,J.E. (1995) DNA structure-dependent requirements for yeast RAD genes in gene conversion. Nature, 373, 94-86.
87. Bätsch,S., Kang,J.E. and Symington,L.S. (2000) RAD51 is required for the repair of plasmid double-stranded DNA gaps from either plasmid or chromosomal templates. Mol. Cell. Biol., 20, 1194-1205.
88. Hiramoto,T., Nakanishi,J., Sumiyoshi,T., Fukuda,T., Matsuura,S., Tauchi,H., Komatsu,K., Shibasaki,Y., Inui,X., Watatani,M. et al. (1999) Mutations of a novel human RAD54 homologue, RAD54B, in primary cancer. Oncogene, 18, 3422-3426.
89. Petukhova,G., Sung,P. and Klein,H. (2000) Promotion of Rad51-dependent D-loop formation by yeast recombination factor Rdh54/Tid1. Genes Dev., 14, 2206-2215.
90. Dresser,M.E., Ewing,D.J., Conrad,M.N., Dominguez,A.M., Barstead,R., Jiang,H. and Kodadek,T. (1997) DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics, 147, 533-544.
91. Lee,S F., Pellicioli,A., Malkova,A., Foiani,M. and Haber,I.E. (2001) The Saccharomyces recombination protein Tid1p is required for adaptation from G2/M arrest induced by a double-strand break. Curr. Biol., 11, 1053-1057.
92. Broomfield,S., Hryciw,T. and Xiao,W. (2001) DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. Mutat. Res. DNA Repair, 486, 167-184.
93. Prakasb,S. and Prakash,L. (2000) Nucleotide excision repair in yeast. Mutat. Res., 451, 13-24.
94. Troelstra,C., Van Gool,A., Dewi,U., Vermeulen,W., Bootsma,D. and Hoeijmakers,J.H.J. (1992) ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne's syndrome and preferential repair of active genes. Cell, 71, 939-953.
95. Selby,C.P. and Sancar,A. (1993) Molecular mechanism of transcription-repair coupling. Science, 260, 53-58.
96. Citterio,E., Van Den Boom,V., Schnitzler,G., Kanaar,R., Bonte,E., Kingston,R.E., Hoeijmakers,J.H.J. and Vermeulen,W. (2000) ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol. Cell. Biol., 20, 7643-7653.
97. Morrison,A.J., Highland,J., Krogan,N.J., Arbel-Eden,A., Greenblatt,J.F., Haber,J.E. and Shen,X. (2004) INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell, 119, 767-775.
98. van Attikum,H., Fritsch,O., Hohn,B. and Gasser,S.M. (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell, 119, 777-788.
99. Downs,J.A., Allard,S., Jobin-Bobitaille,O., Javaheri,A., Auger,A., Bouchard,N., Kron,S.J, Jackson,S.P. and Cote,J. (2004) Binding of chromatin-modifying activities to phopshorylated histone HZA at DNA damage sites. Mol. Cell. Biol., 16, 979-990.
100. Shen,X., Mizuguchi,G., Harmiche,A. and Wu,C. (2000) A chromatin remodelling complex involved in transciption and DNA processing. Nature, 406, 541-544.
101. Shen,X., Ranallo,R., Choi,E. and Wu,C. (2003) Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell, 12, 147-155.
102. Mizuguchi,G., Shen,X.T., Landry,J., Wu,W.H., Sen,S. and Wu,C. (2004) ATP-Driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science, 303, 343-348.
103. Schwacha,A. and Kleckner,N. (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids durine yeast meiosis. Cell. 76, 51-63
104. Hunter,N. and Kleckner,N. (2001) The single-end invasion: An asymmetric intermediate at the double strand break to double Holliday junction transition of meiotic recombination. Cell, 106, 59-70.
105. Interdial,H. and Heyer,W.D. (2000) MUS81 encodes a novel Helix-hairpin-Helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol. Gen. Genet., 263, 812-827.
106. Calderon,I.L., Conotopoulou.C.R. and Mortimer,R.K. (1983) Isolation and characterization of yeast DNA repair genes. H. Isolation of plasmids that complement the mutations rad50-1, rad51-1, rad54-3 and rad55-3. Curr. Genet., 7, 93-100.
107. Emery,H.S., Schild,D., Kellogg,D.E. and Mortimer,R.K. (1991) Sequence of RAD54, a Saccharomyces cerevisiae gene involved in recombination and repair. Gene, 104, 103-106.
108. Kanaar,R., Troelstra,C., Swagemakers,S.M.A., Essers,J., Smit,B., Franssen,J.H., Pastink,A., Bezzubova,O.Y., Buerstedde,J.M., Clever,B. et al. (1996) Human and mouse homologs of the Saccharomyces cerevisiae RAD54 DNA repair gene: Evidence for functional conservation. Curr. Biol., 6, 828-838.
109. Zhang,X.P., Lee,K.I., Solinger,J.A., Kiianitsa,K. and Heyer,W.D. (2005) Gly-103 in the N-terminal domain of Saccharomyces cerevisiae Rad51 protein is critical for DNA binding. J. Biol. Chem., 280, 26303-26311.