Esc2 and Sgsl act in functionally distinct branches of the homologous recombination repair pathway in Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 20, Issue 6, 2009, Pages 1683-1694

  Mankouri, Hocine W ^a   Ngo, Hien Ping ^a   Hickson, Ian D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOM SYNDROME HELICASE; FANCONI ANEMIA GROUP M PROTEIN; FANCONI ANEMIA PROTEIN; PROTEIN ESC2; PROTEIN MPH1; PROTEIN SGS1; RAD51 PROTEIN; SUMO PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; ESC2 PROTEIN, S CEREVISIAE; FUNGAL DNA; MHP1 PROTEIN, S CEREVISIAE; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR PROTEIN; PROTEIN SERINE THREONINE KINASE; RAD53 PROTEIN, S CEREVISIAE; RECQ HELICASE; SACCHAROMYCES CEREVISIAE PROTEIN; SGS1 PROTEIN, S CEREVISIAE;

ARTICLE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENETIC STABILITY; HOMOLOGOUS RECOMBINATION; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; CYTOLOGY; GENETIC RECOMBINATION; GENETICS; GENOMIC INSTABILITY; METABOLISM; MUTATION;

SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPAIR; DNA, FUNGAL; GENOMIC INSTABILITY; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MUTATION; NUCLEAR PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC; RECQ HELICASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 65249090885     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-08-0877     Document Type: Article

References (64)

1. Allers, T., and Lichten, M. (2000). A method for preparing genomic DNA that restrains branch migration of Holliday junctions. Nucleic Acids Res. 28, e6.
2. Alvaro, D., Lisby, M., and Rothstein, R. (2007). Genome-wide analysis of Rad52 foci reveals diverse mechanisms impacting recombination. PLoS Genet. 3, 2439-2449.
3. Bachrati, C. Z., Borts, R. H., and Hickson, I. D. (2006). Mobile D-loops are a preferred substrate for the Bloom's syndrome helicase. Nucleic Acids Res. 34, 2269-2279.
4. Bastin-Shanower, S. A., Fricke, W. M., Mullen, J. R., and Brill, S. J. (2003). The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol. Cell. Biol. 23, 3487-3496.
5. Bjergbaek, L., Cobb, J. A., Tsai-Pflugfelder, M., and Gasser, S. M. (2005). Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J. 24, 405-417.
6. Boddy, M. N., Lopez-Girona, A., Shanahan, P., Interthal, H., Heyer, W. D., and Russell, P. (2000). Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell. Biol. 20, 8758-8766.
7. Boddy, M. N., Shanahan, P., McDonald, W. H., Lopez-Girona, A., Noguchi, E., Yates, I. J., and Russell, P. (2003). Replication checkpoint kinase Cds1 regulates recombinational repair protein Rad60. Mol. Cell. Biol. 23, 5939-5946.
8. Branzei, D., and Foiani, M. (2007). Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Rep. 6, 994-1003.
9. Branzei, D., and Foiani, M. (2008). Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 9, 297-308.
10. Branzei, D., Sollier, J., Liberi, G., Zhao, X., Maeda, D., Seki, M., Enomoto, T., Ohta, K., and Foiani, M. (2006). Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127, 509-522.
11. Brewer, B. J., and Fangman, W. L. (1987). The localization of replication origins on ARS plasmids in. S. cerevisiae. Cell 51, 463-471.
12. Cuperus, G., and Shore, D. (2002). Restoration of silencing in Saccharomyces cerevisiae by tethering of a novel Sir2-interacting protein, Esc8. Genetics 162, 633-645.
13. Dhillon, N., and Kamakaka, R. T. (2000). A histone variant, Htz1p, and a Sir1p-like protein, Esc2p, mediate silencing at HMR. Mol. Cell 6, 769-780.
14. Eladad, S., Ye, T. Z., Hu, P., Leversha, M., Beresten, S., Matunis, M. J., and Ellis, N. A. (2005). Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. Hum. Mol. Genet. 14, 1351-1365.
15. Ellis, N. A., Groden, J., Ye, T. Z., Straughen, J., Lennon, D. J., Ciocci, S., Proytcheva, M., and German, J. (1995). The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83, 655-666.
16. 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. USA 99, 16887-16892.
17. 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.
18. Gangloff, S., McDonald, J. P., Bendixen, C., Arthur, L., and Rothstein, R. (1994). The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14, 8391-8398.
19. 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.
20. German, J. (1993). Bloom syndrome: a mendelian prototype of somatic mutational disease. Medicine 72, 393-406.
21. Hanada, K., and Hickson, I.D. (2007). Molecular genetics of RecQ helicase disorders. Cell. Mol. Life Sci. 64, 2306-2322.
22. Hope, J. C., Cruzata, L. D., Duvshani, A., Mitsumoto, J., Maftahi, M., and Freyer, G. A. (2007). Mus81-Eme1-dependent and -independent crossovers form in mitotic cells during double-strand break repair in Schizosaccharomyces pombe. Mol. Cell. Biol. 27, 3828-3838.
23. Hope, J. C., Maftahi, M., and Freyer, G. A. (2005). A postsynaptic role for Rhp55/57 that is responsible for cell death in Deltarqh1 mutants following replication arrest in Schizosaccharomyces pombe. Genetics 170, 519-531.
24. Johnson, F. B., Lombard, D. B., Neff, N. F., Mastrangelo, M. A., Dewolf, W., Ellis, N. A., Marciniak, R. A., Yin, Y., Jaenisch, R., and Guarente, L. (2000). Association of the Bloom syndrome protein with topoisomerase IIIalpha in somatic and meiotic cells. Cancer Res. 60, 1162-1167.
25. Kanellis, P., Gagliardi, M., Banath, J. P., Szilard, R. K., Nakada, S., Galicia, S., Sweeney, F. D., Cabelof, D. C., Olive, P. L., and Durocher, D. (2007). A screen for suppressors of gross chromosomal rearrangements identifies a conserved role for PLP in preventing DNA lesions. PLoS Genet. 3, e134.
26. 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. USA 97, 6504-6508.
27. Krogh, B. O., and Symington, L. S. (2004). Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271.
28. Laursen, L. V., Ampatzidou, E., Andersen, A. H., and Murray, J. M. (2003). Role for the fission yeast RecQ helicase in DNA repair in G2. Mol. Cell. Biol. 23, 3692-3705.
29. Liberi, G., Maffioletti, G., Lucca, C., Chiolo, I., Baryshnikova, A., Cotta-Ramusino, C., Lopes, M., Pellicioli, A., Haber, J. E., and Foiani, M. (2005). Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19, 339-350.
30. Lopes, M., Cotta-Ramusino, C., Liberi, G., and Foiani, M. (2003). Branch migrating sister chromatid junctions form at replication origins through Rad51/Rad52-independent mechanisms. Mol. Cell 12, 1499-1510.
31. Maftahi, M., Hope, J. C., Delgado-Cruzata, L., Han, C. S., and Freyer, G. A. (2002). The severe slow growth of Deltasrs2 Deltarqh1 in Schizosaccharomyces pombe is suppressed by loss of recombination and checkpoint genes. Nucleic Acids Res. 30, 4781-4792.
32. Mankouri, H. W., and Hickson, I. D. (2006). Top3 processes recombination intermediates and modulates checkpoint activity after DNA damage. Mol. Biol. Cell 17, 4473-4483.
33. Mankouri, H. W., and Hickson, I. D. (2007). The RecQ helicase- topoisomerase III-Rmi1 complex: a DNA structure-specific 'dissolvasome'? Trends Biochem. Sci. 32, 538-546.
34. Mankouri, H. W., Ngo, H. P., and Hickson, I. D. (2007). Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1-Rmi1-Top3. Mol. Biol. Cell 18, 4062-4073.
35. Meetei, A. R. et al. (2005). A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet. 37, 958-963.
36. Miyabe, I., Morishita, T., Hishida, T., Yonei, S., and Shinagawa, H. (2006). Rhp51-dependent recombination intermediates that do not generate check-point signal are accumulated in Schizosaccharomyces pombe rad60 and smc5/6 mutants after release from replication arrest. Mol. Cell. Biol. 26, 343-353.
37. Morishita, T., Tsutsui, Y., Iwasaki, H., and Shinagawa, H. (2002). The Schizosaccharomyces pombe rad60 gene is essential for repairing double-strand DNA breaks spontaneously occurring during replication and induced by DNA-damaging agents. Mol. Cell. Biol. 22, 3537-3548.
38. Mullen, J. R., Kaliraman, V., Ibrahim, S. S., and Brill, S. J. (2001). Requirement for three novel protein complexes in the absence of the Sgsl DNA helicase in Saccharomyces cerevisiae. Genetics 157, 103-118.
39. Murray, J. M., Lindsay, H. D., Munday, C. A., and Carr, A. M. (1997). Role of Schizosaccharomyces pombe RecQ homolog, recombination, and checkpoint genes in UV damage tolerance. Mol. Cell. Biol. 17, 6868-6875.
40. Myung, K., and Kolodner, R. D. (2002). Suppression of genome instability by redundant S-phase checkpoint pathways in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99, 4500-4507.
41. Novatchkova, M., Bachmair, A., Eisenhaber, B., and Eisenhaber, F. (2005). Proteins with two SUMO-like domains in chromatin-associated complexes: the RENi (Rad60-Esc2-NIP45) family. BMC Bioinformatics 6, 22.
42. 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.
43. Prakash, R., Krejci, L., Van Komen, S., Schurer, K.A., 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.
44. Raynard, S., Bussen, W., and Sung, P. (2006). A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIalpha, and BLAP75. J. Biol. Chem. 281, 13861-13864.
45. 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.
46. Schurer, 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.
47. Shor, E., Weinstein, J., and Rothstein, R. (2005). A genetic screen for top3 suppressors in Saccharomyces cerevisiae identifies SHU1, SHU2, PSY3 and CSM 2, four genes involved in error-free DNA repair. Genetics 169, 1275-1289.
48. Sollier, J., Driscoll, R., Castellucci, F., Foiani, M., Jackson, S. P., and Branzei, D. (2009). The Saccharomyces cerevisiae Esc2 and Smc5-6 proteins promote sister chromatid junction-mediated intra-S repair. Mol. Biol. Cell 20, 1671-1682.
49. Spell, R. M. and Jinks-Robertson S. (2004) Determination of mitotic recombination rates by fluctuation analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 262, 3-12.
50. 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.
51. Stewart, E., Chapman, C. R., Al-Khodairy, F., Carr, A. M., and Enoch, T. (1997). rqh1+, 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.
52. Sung, P., Krejci, L., Van Komen, S., and Sehorn, M. G. (2003). Rad51 recom- binase and recombination mediators. J. Biol. Chem. 278, 42729-42732.
53. Tong, A. H. et al. (2001). Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368.
54. van Brabant, A. J., Ye, T., Sanz, M., German, I. J., Ellis, N. A., and Holloman, W. K. (2000). Binding and melting of D-loops by the Bloom syndrome helicase. Biochemistry 39, 14617-14625.
55. Wach, A., Brachat, A., Pohlmann, R., and Philippsen, P. (1994). New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.
56. Wang, S. W., Goodwin, A., Hickson, I. D., and Norbury, C. J. (2001). Involvement of Schizosaccharomyces pombe Srs2 in cellular responses to DNA damage. Nucleic Acids Res. 29, 2963-2972.
57. Wang, W. (2007). Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet. 8, 735-748.
58. Watt, P. M., Hickson, I. D., Borts, R. H., and Louis, E. J. (1996). SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics 144, 935-945.
59. West, S. C. (2003). Molecular views of recombination proteins and their control. Nat. Rev. 4, 435-445.
60. 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. USA 103, 4068-4073.
61. Wu, L., Davies, S. L., North, P. S., Goulaouic, H., Riou, J. F., Turley, H., Gatter, K. C., and Hickson, I. D. (2000). The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem. 275, 9636-9644.
62. Wu, L., and Hickson, I. D. (2003). The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870-874.
63. Yamagata, K., Kato, J., Shimamoto, A., Goto, M., Furuichi, Y., and Ikeda, H. (1998). Bloom's and Werner's syndrome genes suppress hyperrecombination in yeast sgs1 mutant: implication for genomic instability in human diseases. Proc. Natl. Acad. Sci. USA 95, 8733-8738.
64. Yin, J., Sobeck, A., Xu, C., Meetei, A. R., Hoatlin, M., Li, L., and Wang, W. (2005). BLAP75, an essential component of Bloom's syndrome protein complexes that maintain genome integrity. EMBO J. 24, 1465-1476.