The role of Holliday junction resolvases in the repair of spontaneous and induced DNA damage

Nucleic Acids Research

Volumn 39, Issue 16, 2011, Pages 7009-7019

  Agmon, Neta ^a   Yovel, Moran ^a   Harari, Yaniv ^a   Liefshitz, Batia ^a   Kupiec, Martin ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CROSSOVER JUNCTION ENDODEOXYRIBONUCLEASE;

ARTICLE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; FUNGAL GENE; GENE DELETION; GENE INTERACTION; GROWTH RATE; GROWTH RETARDATION; HOLLIDAY JUNCTION; HOMOLOGOUS RECOMBINATION; MEIOSIS; MMS4 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAD1 GENE; RAD51 GENE; RAD52 GENE; VEGETATIVE GROWTH; YEAST; YEN1 GENE;

DNA DAMAGE; FLAP ENDONUCLEASES; GENE DELETION; HOLLIDAY JUNCTION RESOLVASES; MEIOSIS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 80052426793     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr277     Document Type: Article

References (59)

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. (Pubitemid 29264976)
2. Holliday, R. (1964) A mechanism for gene conversion in fungi. Genet. Res., 5, 283-304.
3. Liu, Y. and West, S.C. (2004) Happy Hollidays: 40th anniversary of the Holliday junction. Nat. Rev. Mol. Cell Biol., 5, 937-944. (Pubitemid 39486545)
4. Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.C., Nicolas, A. and Forterre, P. (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature, 386, 414-417. (Pubitemid 27154484)
5. Keeney, S., Giroux, C.N. and Kleckner, N. (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell, 88, 375-384. (Pubitemid 27131379)
6. 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. (Pubitemid 13096431)
7. Mizuuchi, K., Kemper, B., Hays, J. and Weisberg, R.A. (1982) T4 endonuclease VII cleaves holliday structures. Cell, 29, 357-365.
8. Symington, L.S. and Kolodner, R. (1985) Partial purification of an enzyme from Saccharomyces cerevisiae that cleaves Holliday junctions. Proc. Natl Acad. Sci. USA, 82, 7247-7251. (Pubitemid 16193718)
9. West, S.C. and Korner, A. (1985) Cleavage of cruciform DNA structures by an activity from Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 82, 6445-6449. (Pubitemid 16230530)
10. Kleff, S., Kemper, B. and Sternglanz, R. (1992) Identification and characterization of yeast mutants and the gene for a cruciform cutting endonuclease. EMBO J., 11, 699-704.
11. Boddy, M.N., Gaillard, P.H., McDonald, W.H., Shanahan, P., Yates, J.R. 3rd and Russell, P. (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell, 107, 537-548. (Pubitemid 33152788)
12. Chen, X.B., Melchionna, R., Denis, C.M., Gaillard, P.H., Blasina, A., Van de Weyer, I., Boddy, M.N., Russell, P., Vialard, J. and McGowan, C.H. (2001) Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell, 8, 1117-1127. (Pubitemid 34031813)
13. Ciccia, A., Constantinou, A. and West, S.C. (2003) Identification and characterization of the human mus81-eme1 endonuclease. J. Biol. Chem., 278, 25172-25178. (Pubitemid 37548682)
14. Kaliraman, V., Mullen, J.R., Fricke, W.M., Bastin-Shanower, S.A. and Brill, S.J. (2001) Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev., 15, 2730-2740. (Pubitemid 32988882)
15. de los Santos, T., Hunter, N., Lee, C., Larkin, B., Loidl, J. and Hollingsworth, N.M. (2003) The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics, 164, 81-94. (Pubitemid 36617695)
16. Osman, F., Dixon, J., Doe, C.L. and Whitby, M.C. (2003) Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol. Cell, 12, 761-774. (Pubitemid 37222495)
17. Ip, S.C., Rass, U., Blanco, M.G., Flynn, H.R., Skehel, J.M. and West, S.C. (2008) Identification of Holliday junction resolvases from humans and yeast. Nature, 456, 357-361.
18. Lieber, M.R. (1997) The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair. Bioessays, 19, 233-240. (Pubitemid 27140647)
19. Blanco, M.G., Matos, J., Rass, U., Ip, S.C. and West, S.C. (2010) Functional overlap between the structure-specific nucleases Yen1 and Mus81-Mms4 for DNA-damage repair in S. cerevisiae. DNA Repair, 9, 394-402.
20. Ho, C.K., Mazon, G., Lam, A.F. and Symington, L.S. (2010) Mus81 and Yen1 promote reciprocal exchange during mitotic recombination to maintain genome integrity in budding yeast. Mol. Cell, 40, 988-1000.
21. Tay, Y.D. and Wu, L. (2010) Overlapping roles for Yen1 and Mus81 in cellular Holliday junction processing. J. Biol. Chem., 285, 11427-11432.
22. 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.
23. Orr-Weaver, T.L., Nicolas, A. and Szostak, J.W. (1988) Gene conversion adjacent to regions of double-strand break repair. Mol. Cell. Biol., 8, 5292-5298.
24. 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.
25. 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. (Pubitemid 37456803)
26. Wu, L. and Hickson, I.D. (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature, 426, 870-874. (Pubitemid 38056876)
27. Aylon, Y., Liefshitz, B., Bitan-Banin, G. and Kupiec, M. (2003) Molecular dissection of mitotic recombination in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol., 23, 1403-1417. (Pubitemid 36177048)
28. Smith, S., Hwang, J.Y., Banerjee, S., Majeed, A., Gupta, A. and Myung, K. (2004) Mutator genes for suppression of gross chromosomal rearrangements identified by a genome-wide screening in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 101, 9039-9044. (Pubitemid 38781607)
29. 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.
30. Basile, G., Aker, M. and Mortimer, R.K. (1992) Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51. Mol. Cell. Biol., 12, 3235-3246.
31. Reynolds, P., Prakash, L. and Prakash, S. (1987) Nucleotide sequence and functional analysis of the RAD1 gene of Saccharomyces cerevisiae. Mol. Cell. Biol., 7, 1012-1020. (Pubitemid 17017420)
32. Inbar, O., Liefshitz, B., Bitan, G. and Kupiec, M. (2000) The relationship between homology length and crossing over during the repair of a broken chromosome. J. Biol. Chem., 275, 30833-30838.
33. St Onge, R.P., Mani, R., Oh, J., Proctor, M., Fung, E., Davis, R.W., Nislow, C., Roth, F.P. and Giaever, G. (2007) Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions. Nat. Genet., 39, 199-206. (Pubitemid 46184350)
34. Prakash, L. and Prakash, S. (1977) Isolation and characterization of MMS-sensitive mutants of Saccharomyces cerevisiae. Genetics, 86, 33-55.
35. Interthal, 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.
36. Lee, K.Y. and Myung, K. (2008) PCNA modifications for regulation of post-replication repair pathways. Mol. Cells, 26, 5-11.
37. Hoege, C., Pfander, B., Moldovan, G.L., Pyrowolakis, G. and Jentsch, S. (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature, 419, 135-141. (Pubitemid 35025438)
38. Stelter, P. and Ulrich, H.D. (2003) Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature, 425, 188-191. (Pubitemid 37150898)
39. Sung, P., Reynolds, P., Prakash, L. and Prakash, S. (1993) Purification and characterization of the Saccharomyces cerevisiae RAD1/RAD10 endonuclease. J. Biol. Chem., 268, 26391-26399. (Pubitemid 23361714)
40. Agmon, N., Pur, S., Liefshitz, B. and Kupiec, M. (2009) Analysis of repair mechanism choice during homologous recombination. Nucleic Acids Res., 37, 5081-5092.
41. Ivanov, E.L. and Haber, J.E. (1995) RAD1 and RAD10, but not other excision repair genes, are required for double-strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol., 15, 2245-2251.
42. Liefshitz, B., Parket, A., Maya, R. and Kupiec, M. (1995) The role of DNA repair genes in recombination between repeated sequences in yeast. Genetics, 140, 1199-1211.
43. Liefshitz, B., Steinlauf, R., Friedl, A., Eckardt-Schupp, F. and Kupiec, M. (1998) Genetic interactions between mutants of the 'error-prone' repair group of Saccharomyces cerevisiae and their effect on recombination and mutagenesis. Mutat. Res., 407, 135-145. (Pubitemid 28241555)
44. Habraken, Y., Sung, P., Prakash, L. and Prakash, S. (1994) Holliday junction cleavage by yeast Rad1 protein. Nature, 371, 531-534. (Pubitemid 24306613)
45. West, S.C. (1995) Holliday junctions cleaved by Rad1? Nature, 373, 27-28.
46. Fekairi, S., Scaglione, S., Chahwan, C., Taylor, E.R., Tissier, A., Coulon, S., Dong, M.Q., Ruse, C., Yates, J.R. 3rd, Russell, P. et al. (2009) Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell, 138, 78-89.
47. Toh, G.W., Sugawara, N., Dong, J., Toth, R., Lee, S.E., Haber, J.E. and Rouse, J. (2010) Mec1/Tel1-dependent phosphorylation of Slx4 stimulates Rad1-Rad10-dependent cleavage of non-homologous DNA tails. DNA Repair, 9, 718-726.
48. Borts, R.H. and Haber, J.E. (1987) Meiotic recombination in yeast: alteration by multiple heterozygosities. Science, 237, 1459-1465. (Pubitemid 17134611)
49. Lee, P.S., Greenwell, P.W., Dominska, M., Gawel, M., Hamilton, M. and Petes, T.D. (2009) A fine-structure map of spontaneous mitotic crossovers in the yeast Saccharomyces cerevisiae. PLoS Genet., 5, e1000410.
50. Bzymek, M., Thayer, N.H., Oh, S.D., Kleckner, N. and Hunter, N. (2010) Double Holliday junctions are intermediates of DNA break repair. Nature, 464, 937-941.
51. Branzei, D., Vanoli, F. and Foiani, M. (2008) SUMOylation regulates Rad18-mediated template switch. Nature, 456, 915-920.
52. Karras, G.I. and Jentsch, S. (2010) The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell, 141, 255-267.
53. Michel, B., Flores, M.J., Viguera, E., Grompone, G., Seigneur, M. and Bidnenko, V. (2001) Rescue of arrested replication forks by homologous recombination. Proc. Natl Acad. Sci. USA, 98, 8181-8188. (Pubitemid 32678011)
54. Postow, L., Ullsperger, C., Keller, R.W., Bustamante, C., Vologodskii, A.V. and Cozzarelli, N.R. (2001) Positive torsional strain causes the formation of a four-way junction at replication forks. J. Biol. Chem., 276, 2790-2796.
55. Branzei, D. and Foiani, M. (2009) The checkpoint response to replication stress. DNA Repair, 8, 1038-1046.
56. Prakash, L. (1981) Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol. Gen. Genet., 184, 471-478. (Pubitemid 12129873)
57. Mortensen, U.H., Lisby, M. and Rothstein, R. (2009) Rad52. Curr. Biol., 19, R676-677.
58. Seong, C., Sehorn, M.G., Plate, I., Shi, I., Song, B., Chi, P., Mortensen, U., Sung, P. and Krejci, L. (2008) Molecular anatomy of the recombination mediator function of Saccharomyces cerevisiae Rad52. J. Biol. Chem., 283, 12166-12174.
59. Dubrana, K., van Attikum, H., Hediger, F. and Gasser, S.M. (2007) The processing of double-strand breaks and binding of single-strand-binding proteins RPA and Rad51 modulate the formation of ATR-kinase foci in yeast. J. Cell Sci., 120, 4209-4220.