Yeast Mphl helicase dissociates Rad51-made D-loops: Implications for crossover control in mitotic recombination

Genes and Development

Volumn 23, Issue 1, 2009, Pages 67-79

  Prakash, Rohit ^a   Satory, Dominik ^b   Dray, Eloïse ^a   Papusha, Almas ^b   Scheller, Jürgen ^c,g   Kramer, Wilfried ^c   Krejci, Lumir ^d   Klein, Hannah ^e   Haber, James E ^f   Sung, Patrick ^a   Ira, Grzegorz ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d MASARYK UNIVERSITY   (Czech Republic)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f BRANDEIS UNIVERSITY   (United States)

^g UNIVERSITY OF KIEL   (Germany)

Author keywords

Crossing over; Dna helicase; Fanconi anemia; Genome instability; Recombination

Indexed keywords

FANCONI ANEMIA GROUP M PROTEIN; FANCONI ANEMIA PROTEIN; HELICASE; MPH1 HELICASE; RAD51 PROTEIN; SGS1 HELICASE; SRS2 HELICASE; UNCLASSIFIED DRUG; DEAD BOX PROTEIN; FUNGAL DNA; MPH1 PROTEIN, S CEREVISIAE; RAD51 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CROSSING OVER; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; GENOMIC INSTABILITY; MITOTIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; SISTER CHROMATID EXCHANGE; ALLELE; CHEMISTRY; CONFORMATION; ENZYMOLOGY; GENETICS; METABOLISM; MITOSIS; SACCHAROMYCES CEREVISIAE;

EUKARYOTA; SACCHAROMYCETALES;

ALLELES; CROSSING OVER, GENETIC; DEAD-BOX RNA HELICASES; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA, FUNGAL; MITOSIS; NUCLEIC ACID CONFORMATION; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SISTER CHROMATID EXCHANGE;

EID: 58149494717     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1737809     Document Type: Article

References (90)

1. Allers, T., and Lichten, M. 2001. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47-57.
2. Barbera, M.A., and Petes, T.D. 2006. Selection and analysis of spontaneous reciprocal mitotic cross-overs in Saccharo-myces cerevisiae. Proc. Natl. Acad. Sci. 103: 12819-12824.
3. Beumer, K.J., Pimpinelli, S., and Golic, K.G. 1998. Induced chromosomal exchange directs the segregation of recombinant chromatids in mitosis of Drosophila. Genetics 150: 173-188.
4. Bridge, W.L., Vandenberg, C.J., Franklin, R.J., and Hiom, K. 2005. The BRIP1 helicase functions independently of BRCA1 in the Fanconi anemia pathway for DNA crosslink repair. Nat. Genet. 37: 953-957.
5. Brosh, Jr., R.M., Orren, D.K., Nehlin, J.O., Ravn, P.H., Kenny, M.K., Machwe, A., and Bohr, V.A. 1999. Functional and physical interaction between WRN helicase and human replication protein A. J. Biol. Chem. 274: 18341-18350.
6. Brosh, Jr., R.M., Li, J.L., Kenny, M.K., Karow, J.K., Cooper, M.P., Kureekattil, R.P., Hickson, I.D., and Bohr, V.A. 2000. Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J. Biol. Chem. 275: 23500-23508.
7. Bugreev, D.V., Mazina, O.M., and Mazin, A.V. 2006. Rad54 protein promotes branch migration of Holliday junctions. Nature 442: 590-593.
8. Bugreev, D.V., Yu, X., Egelman, E.H., and Mazin, A.V. 2007. Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes & Dev. 21: 3085-3094.
9. Bugreev, D.V., Brosh, Jr., R.M., and Mazin, A.V. 2008. RECQ1 possesses DNA branch migration activity. J. Biol. Chem. 283: 20231-20242.
10. Chaganti, R.S., Schonberg, S., and German, J. 1974. A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc. Natl. Acad. Sci. 71: 4508-4512.
11. Chang, M., Bellaoui, M., Zhang, C., Desai, R., Morozov, P., Delgado-Cruzata, L., Rothstein, R., Freyer, G.A., Boone, C., and Brown, G.W. 2005. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO J. 24: 2024-2033.
12. Chi, P., San Filippo, J., Sehorn, M.G., Petukhova, G.V., and Sung, P. 2007. Bipartite stimulatory action of the Hop2-Mnd1 complex on the Rad51 recombinase. Genes & Dev. 21: 1747-1757.
13. Cui, S., Arosio, D., Doherty, K.M., Brosh, Jr., R.M., Falaschi, A., and Vindigni, A. 2004. Analysis of the unwinding activity of the dimeric RECQ1 helicase in the presence of human replication protein A. Nucleic Acids Res. 32: 2158-2170.
14. Dupaigne, P., Le Breton, C., Fabre, F., Gangloff, S., Le Cam, E., and Veaute, X. 2008. The Srs2 helicase activity is stimulated by Rad51 filaments on dsDNA: Implications for crossover incidence during mitotic recombination. Mol. Cell 29: 243-254.
15. Entian, K.D., Schuster, T., Hegemann, J.H., Becher, D., Feldmann, H., Guldener, U., Gotz, R., Hansen, M., Hollenberg, C.P., and Jansen, G., et al. 1999. Functional analysis of 150 deletion mutants in Saccharomyces cerevisiae by a systematic approach. Mol. Gen. Genet. 262: 683-702.
16. Esposito, M.S., 1978. Evidence that spontaneous mitotic recombination occurs at the two-strand stage. Proc. Natl. Acad. Sci. 75: 4436-4440.
17. Fabre, F., Chan, A., Heyer, W.D., and Gangloff, S. 2002. Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. 99: 16887-16892.
18. Fasullo, M.T., and Davis, R.W. 1987. Recombinational substrates designed to study recombination between unique and repetitive sequences in vivo. Proc. Natl. Acad. Sci. 84: 6215-6219.
19. Frei, C., and Gasser, S.M. 2000. The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes & Dev. 14: 81-96.
20. Gangloff, S., Soustelle, C., and Fabre, F. 2000. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet. 25: 192-194.
21. Gravel, S., Chapman, J.R., Magill, C., and Jackson, S.P. 2008. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes & Dev. 22: 2767-2772.
22. Guillon, H., Baudat, F., Grey, C., Liskay, R.M., and de Massy, B. 2005. Crossover and noncrossover pathways in mouse mei-osis. Mol. Cell 20: 563-573.
23. Hirano, S., Yamamoto, K., Ishiai, M., Yamazoe, M., Seki, M., Matsushita, N., Ohzeki, M., Yamashita, Y.M., Arakawa, H., and Buerstedde, J.M., et al. 2005. Functional relationships of FANCC to homologous recombination, translesion synthesis, and BLM. EMBO J. 24: 418-427.
24. Howlett, N.G., Taniguchi, T., Olson, S., Cox, B., Waisfisz, Q., De Die-Smulders, C., Persky, N., Grompe, M., Joenje, H., and Pals, G. 2002. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 297: 606-609.
25. Hu, Y., Lu, X., Barnes, E., Yan, M., Lou, H., and Luo, G. 2005. Recql5 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers. Mol. Cell. Biol. 25: 3431-3442.
26. Hu, Y., Raynard, S., Sehorn, M.G., Lu, X., Bussen, W., Zheng, L., Stark, J.M., Barnes, E.L., Chi, P., and, Janscak, P., et al. 2007. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes & Dev. 21: 3073-3084.
27. 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.
28. Hussain, S., Wilson, J.B., Blom, E., Thompson, L.H., Sung, P., Gordon, S.M., Kupfer, G.M., Joenje, H., Mathew, C.G., and Jones, N.J. 2006. Tetratricopeptide-motif-mediated interaction of FANCG with recombination proteins XRCC3 and BRCA2. DNA Repair (Amst.) 5: 629-640.
29. Ira, G., Malkova, A., Liberi, G., Foiani, M., and Haber, J.E. 2003. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115: 401-411.
30. Ira, G., Satory, D., and Haber, J.E. 2006. Conservative inheritance of newly synthesized DNA in double-strand break-induced gene conversion. Mol. Cell. Biol. 26: 9424-9429.
31. Jessop, L., and Lichten, M. 2008. Mus81/Mms4 endonuclease and Sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol. Cell 31: 313-323.
32. Jessop, L., Rockmill, B., Roeder, G.S., and Lichten, M. 2006. Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of sgs1. PLoS Genet. 2: e155. doi:10.1371/journal.pgen.0020155.
33. Johnson, R.D., and Jasin, M. 2000. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19: 3398-3407.
34. Karow, J.K., Constantinou, A., Li, J.L., West, S.C., and Hickson, I.D. 2000. The Bloom's syndrome gene product promotes branch migration of Holliday junctions. Proc. Natl. Acad. Sci. 97: 6504-6508.
35. Komori, K., Fujikane, R., Shinagawa, H., and Ishino, Y. 2002. Novel endonuclease in Archaea cleaving DNA with various branched structure. Genes Genet. Syst. 77: 227-241.
36. Komori, K., Hidaka, M., Horiuchi, T., Fujikane, R., Shinagawa, H., and Ishino, Y. 2004. Cooperation of the N-terminal Helicase and C-terminal endonuclease activities of Archaeal Hef protein in processing stalled replication forks. J. Biol. Chem. 279: 53175-53185.
37. 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.
38. Krogh, B.O., and Symington, L.S. 2004. Recombination proteins in yeast. Annu. Rev. Genet. 38: 233-271.
39. Kwon, Y., Seong, C., Chi, P., Greene, E.C., Klein, H., and Sung, P. 2008. ATP-dependent chromatin remodeling by the Saccha-romyces cerevisiae homologous recombination factor Rdh54. J. Biol. Chem. 283: 10445-10452.
40. Litman, R., Peng, M., Jin, Z., Zhang, F., Zhang, J., Powell, S., Andreassen, P.R., and Cantor, S.B. 2005. BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell 8: 255-265.
41. Liu, Y., Masson, J.Y., Shah, R., O'Regan, P., and West, S.C. 2004. RAD51C is required for Holliday junction processing in mammalian cells. Science 303: 243-246.
42. Lo, Y.C., Paffett, K.S., Amit, O., Clikeman, J.A., Sterk, R., Brenneman, M.A., and Nickoloff, J.A. 2006. Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol. Cell. Biol. 26: 4086-4094.
43. Magner, D.B., Blankschien, M.D., Lee, J.A., Pennington, J.M., Lupski, J.R., and Rosenberg, S.M. 2007. RecQ promotes toxic recombination in cells lacking recombination intermediate-removal proteins. Mol. Cell 26: 273-286.
44. McMahill, M.S., Sham, C.W., and Bishop, D.K. 2007. Synthesis-dependent strand annealing in meiosis. PLoS Biol. 5: e299. doi:10.1371/journal.pbio.0050299.
45. Meetei, A.R., Medhurst, A.L., Ling, C., Xue, Y., Singh, T.R., Bier, P., Steltenpool, J., Stone, S., Dokal, I., and Mathew, C.G. 2005. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet. 37: 958-963.
46. Mimitou, E.P., and Symington, L.S. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455: 770-774.
47. Mosedale, G., Niedzwiedz, W., Alpi, A., Perrina, F., Pereira-Leal, J.B., Johnson, M., Langevin, F., Pace, P., and Patel, K.J. 2005. The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway. Nat. Struct. Mol. Biol. 12: 763-771.
48. Mullen, J.R., Nallaseth, F.S., Lan, Y.Q., Slagle, C.E., and Brill, S.J. 2005. Yeast Rmi1/Nce4 controls genome stability as a sub-unit of the Sgs1-Top3 complex. Mol. Cell. Biol. 25: 4476-4487.
49. Myung, K., Datta, A., Chen, C., and Kolodner, R.D. 2001. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN.
50. suppresses genome instability and homeologous recombination. Nat. Genet. 27: 113-116.
51. Nassif, N., Penney, J., Pal, S., Engels, W.R., and Gloor, G.B. 1994. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 14: 1613-1625.
52. Niedzwiedz, W., Mosedale, G., Johnson, M., Ong, C.Y., Pace, P., and Patel, K.J. 2004. The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol. Cell 15: 607-620.
53. Oh, S.D., Lao, J.P., Hwang, P.Y., Taylor, A.F., Smith, G.R., and Hunter, N. 2007. BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130: 259-272.
54. Oh, S.D., Lao, J.P., Taylor, A.F., Smith, G.R., and Hunter, N. 2008. RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during mei-otic recombination. Mol. Cell 31: 324-336.
55. Onoda, F., Seki, M., Wang, W., and Enomoto, T. 2004. The hyper unequal sister chromatid recombination in an sgs1 mutant of budding yeast requires MSH2. DNA Repair (Amst.) 3: 1355-1362.
56. Orren, D.K., Theodore, S., and Machwe, A. 2002. The Werner syndrome helicase/exonuclease (WRN) disrupts and degrades D-loops in vitro. Biochemistry 41: 13483-13488.
57. Palladino, F., and Klein, H.L. 1992. Analysis of mitotic and meiotic defects in Saccharomyces cerevisiae SRS2 DNA helicase mutants. Genetics 132: 23-37.
58. 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.
59. Pichierri, P., Franchitto, A., and Rosselli, F. 2004. BLM and the FANC proteins collaborate in a common pathway in response to stalled replication forks. EMBO J. 23: 3154-3163.
60. Prakash, R., Krejci, L., Van Komen, S., Anke Schürer, K., Kramer, W., and Sung, P. 2005. Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 3' to 5' DNA helicase. J. Biol. Chem. 280: 7854-7860.
61. Raynard, S., Bussen, W., and Sung, P. 2006. A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIα, and BLAP75. J. Biol. Chem. 281: 13861-13864.
62. Richardson, C., Moynahan, M.E., and Jasin, M. 1998. Double-strand break repair by interchromosomal recombination: Suppression of chromosomal translocations. Genes & Dev. 12: 3831-3842.
63. Robert, T., Dervins, D., Fabre, F., and Gangloff, S. 2006. Mrc1 and Srs2 are major actors in the regulation of spontaneous crossover. EMBO J. 25: 2837-2846.
64. Roeder, G.S., 1995. Sex and the single cell: Meiosis in yeast. Proc. Natl. Acad. Sci. 92: 10450-10456.
65. San Filippo, J., Sung, P., and Klein, H. 2008. Mechanism of eukaryotic homologous recombination. Annu. Rev. Bio-chem. 77: 229-257.
66. Scheller, J., Schürer, A., Rudolph, C., Hettwer, S., and Kramer, W. 2000. MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics 155: 1069-1081.
67. Schürer, K.A., Rudolph, C., Ulrich, H.D., and Kramer, W. 2004. Yeast MPH1 gene functions in an error-free DNA damage bypass pathway that requires genes from homologous recombination, but not from postreplicative repair. Genetics 166: 1673-1686.
68. Shaw, C.J., and Lupski, J.R. 2004. Implications of human genome architecture for rearrangement-based disorders: The genomic basis of disease. Hum. Mol. Genet. 13: R57-R6410.1093/hmg/ddh073.
69. Sigurdsson, S., Trujillo, K., Song, B., Stratton, S., and Sung, P. 2001. Basis for avid homologous DNA strand exchange by human Rad51 and RPA. J. Biol. Chem. 276: 8798-8806.
70. 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. 98: 8447-8453.
71. 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.
72. Stark, J.M., and Jasin, M. 2003. Extensive loss of heterozygosity is suppressed during homologous repair of chromosomal breaks. Mol. Cell. Biol. 23: 733-743.
73. +, a fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S phase arrest. EMBO J. 16: 2682-2692.
74. 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.
75. Sung, P., and Klein, H. 2006. Mechanism of homologous recombination: Mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 7: 739-750.
76. Sung, P., and Stratton, S.A. 1996. Yeast Rad51 recombinase mediates polar DNA strand exchange in the absence of ATP hydrolysis. J. Biol. Chem. 271: 27983-27986.
77. 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.
78. Tong, A.H., Lesage, G., Bader, G.D., Ding, H., Xu, H., Xin, X., Young, J., Berriz, G.F., Brost, R.L., and Chang, M., et al. 2004. Global mapping of the yeast genetic interaction network. Science 303: 808-813.
79. van Brabant, A.J., Ye, T., Sanz, M., German, J.L. III, Ellis, N.A., and Holloman, W.K. 2000. Binding and melting of D-loops by the Bloom syndrome helicase. Biochemistry 39: 14617-14625.
80. Van Komen, S., Macris, M., Sehorn, M.G., and Sung, P. 2006. Purification and assays of Saccharomyces cerevisiae homologous recombination proteins. Methods Enzymol. 408: 445-463.
81. 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.
82. Virgin, J.B., Bailey, J.P., Hasteh, F., Neville, J., Cole, A., and Tromp, G. 2001. Crossing over is rarely associated with mitotic intragenic recombination in Schizosaccharomyces pombe. Genetics 157: 63-77.
83. Wang, W., Seki, M., Narita, Y., Nakagawa, T., Yoshimura, A., Otsuki, M., Kawabe, Y., Tada, S., Yagi, H., and Ishii, Y., et al. 2003. Functional relation among RecQ family helicases RecQL1, RecQL5, and BLM in cell growth and sister chro-matid exchange formation. Mol. Cell. Biol. 23: 3527-3535.
84. 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.
85. Wu, L., and Hickson, I.D. 2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874.
86. Wu, L., Bachrati, C.Z., Ou, J., Xu, C., Yin, J., Chang, M., Wang, W., Li, L., Brown, G.W., and Hickson, I.D. 2006. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl. Acad. Sci. 103: 4068-4073.
87. Xue, Y., Li, Y., Guo, R., Ling, C., and Wang, W. 2008. FANCM of the Fanconi anemia core complex is required for both monoubiquitination and DNA repair. Hum. Mol. Genet. 17: 1641-1652.
88. Yamamoto, K., Hirano, S., Ishiai, M., Morishima, K., Kitao, H., Namikoshi, K., Kimura, M., Matsushita, N., Arakawa, H., and Buerstedde, J.M. 2005. Fanconi anemia protein FANCD2 promotes immunoglobulin gene conversion and DNA repair through a mechanism related to homologous recombination. Mol. Cell. Biol. 25: 34-43.
89. Zarr, J.H., 1999. Biostatistical analysis. Prentice Hall, Inc., Englewood Cliffs, NJ.
90. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E., and Ira, G. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134: 981-994.