Requirement of Rrm3 Helicase for Repair of Spontaneous DNA Lesions in Cells Lacking Srs2 or Sgs1 Helicase

Molecular and Cellular Biology

Volumn 24, Issue 8, 2004, Pages 3213-3226

  Schmidt, Kristina H ^a   Kolodner, Richard D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; DNA; HELICASE; PROTEIN RRM3; REPETITIVE DNA; RIBOSOME DNA; SGS1 HELICASE; SRS2 HELICASE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G2 PHASE; CELL DEATH; CONTROLLED STUDY; DNA CONTENT; DNA DAMAGE; DNA REPAIR; DNA REPLICATION ORIGIN; FUNGUS MUTANT; GENE DISRUPTION; HOMOLOGOUS RECOMBINATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CELL CYCLE; CELL CYCLE PROTEINS; CELL DEATH; CELL DIVISION; CELL SIZE; CELL SURVIVAL; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA REPLICATION; GENE SILENCING; MOLECULAR SEQUENCE DATA; PHENOTYPE; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

FUNGI; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 1642416422     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.8.3213-3226.2004     Document Type: Article

References (76)

1. Aboussekhra, A., R. Chanet, Z. Zgaga, C. Cassier-Chauvat, M. Heude, and F. Fabre. 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.
2. Adams, M. D., M. McVey, and J. J. Sekelsky. 2003. Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science 299:265-267.
3. Bastin-Shanower, S. A., W. M. Fricke, J. R. Mullen, and S. J. Brill. 2003. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol. Cell. Biol. 23:3487-3496.
4. Bennett. R. J., J. A. Sharp, and J. C. Wang. 1998. Purification and characterization of the Sgs1 DNA helicase activity of Saccharomyces cerevisae. J. Biol. Chem. 273:9644-9650.
5. Boulton, S. J., and S. P. Jackson. 1998. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17:1819-1828.
6. Brosh, R. M., Jr., and V. A. Bohr. 2002. Roles of the Werner syndrome protein in pathways required for maintenance of genome stability. Exp. Gerontol 37:491-506.
7. Chester, N., F. Kuo, C. Kozak, C. D. O'Hara, and P. Leder. 1998. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev. 12:3382-3393.
8. Ciccia, A., A. Constantinou, and S. C. West. 2003. Identification and characterization of the human Mus81/Eme1 endonuclecase. J. Biol. Chem. 278:25172-25178.
9. Cobb, J. A., L. Bjergbaek, and S. M. Gasser. 2002. RecQ helicases: at the heart of genetic stability. FEBS Lett. 529:43-48.
10. Connelly, J. C., and D. R. Leach. 2002. Tethering on the brink: the evolutionarily conserved Mre11-Rad50 complex. Trends Biochem. Sci. 27:410-418.
11. Constantinou, A., M. Tarsounas, J. K. Karow, R. M. Brosh, V. A. Bohr, I. D. Hickson, and S. C. West. 2000. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep. 1:80-84.
12. Cox, M. M. 2002. The nonmutagenic repair of broken replication forks via recombination. Mutal. Res. 510:107-120.
13. D'Amours, D., and S. P. Jackson. 2002. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3:317-327.
14. D'Amours, D., and S. P. Jackson. 2001. The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 15:2238-2249.
15. Dillingham, M. S., M. Spies, and S. C. Kowalczykowski. 2003. RecBCD enzyme is a bipolar DNA helicase. Nature 423:893-897.
16. Epstein, C. J., and A. G. Motulsky. 1996. Werner syndrome: entering the helicase era. Bioessays 18:1025-1027.
17. Fabre, F., A. Chan, W. D. Heyer, and S. Gangloff. 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 99:16887-16891
18. Frei, C., and S. M. Gasser. 2000. RecQ-like helicases: the DNA replication checkpoint connection. J. Cell Sci. 113:2641-2646.
19. Frie, C., and S. M. Gasser. 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., J. P. McDonald, C. Bendixen, L. Arthur, and R. Rothstein. 1994. The yeast type 1 topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14:8391-8398.
21. Gangloff, S., C. Soustelle, and F. Fabre. 2000. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet. 25:192-194.
22. German, J. 1995. Bloom's syndrome. Dermatol. Clin. 13:7-18.
23. Grenon, M., C. Gilbert, and N. F. Lowndes. 2001. Checkpoint activation in response to double-strand breaks requires the Mre11/Rad50/Xrs2 complex. Nat. Cell Biol. 3:844-847.
24. Haber, J. E. 1999. DNA recombination: the replication connection. Trends Biochem. Sci. 24:271-275.
25. Haber, J. E. 1998. The many interfaces of Mre11. Cell 95:583-586.
26. Haber, J. E., and W. D. Heyer. 2001. The fuss about Mus81. Cell 107:551-554.
27. Heyer, W. D., M. R. Rao, L. F. Erdile, T. J. Kelly, and R. D. Kolodner. 1990. An essential Saccharomyces cerevisiae single-stranded DNA binding protein is homologous to the large subunit of human RP-A. EMBO J. 9:2321-2329.
28. Hickson, I. D., S. L. Davies, J. L. Li, N. C. Levitt, P. Mohaghegh, P. S. North, and L. Wu. 2001. Role of the Bloom's syndrome helicase in maintenance of genome stability. Biochem. Soc. Trans. 29:201-204.
29. Huang, M. E., A. de Calignon, A. Nicolas, and F. Galibert. 2000. POL32, a subunit of the Saccharomyces cerevisiae DNA polymerase δ, defines a link between DNA replication and the mutagenic bypass repair pathway. Curr. Genet. 38:178-187.
30. Interthal, H., and W. D. Heyer. 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.
31. Ivessa, A. S., B. A. Lenzmeier, J. B. Bessler, L. K. Goudsouzian, S. L. Schnakenberg, and V. A. Zakian. 2003. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication fork progression past non-histone protein-DNA complexes. Mol. Cell 12:1525-1536.
32. Ivessa, A. S., J. Q. Zhou, V. P. Schulz, E. K. Monson, and V. A. Zakian. 2002. Saccharomyces Rrm3p, a 5′ to 3′ DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 16:1383-1396.
33. Ivessa, A. S., J. Q. Zhou, and V. A. Zakian. 2000. The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell 100:479-489.
34. Kaliraman, V., J. R. Mullen, W. M. Fricke, S. A. Bastin-Shanower, and S. J. Brill. 2001. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15:2730-2740.
35. Karow, J. K., A. Constantinou, J. L. Li, S. C. West, and I. D. Hickson. 2000. The Bloom's syndrome gene product promotes branch migration of Holiday junctions. Proc. Natl. Acad. Sci. USA 97:6504-6508.
36. Keil, R. L., and A. D. McWilliams. 1993. A gene with specific and global effects on recombination of sequences from tandemly repeated genes in Saccharomyces cerevisiae. Genetics 135:711-718.
37. Klein, H. L. 2001. Mutations in recombinational repair and in checkpoint control genes suppress the lethal combination of sra2Δ with other DNA repair genes in Saccharomyces cerevisiae. Genetics 157:557-565.
38. Klein, H. L., and K. N. Kreuzer. 2002. Replication, recombination, and repair: going for the gold. Mol. Cell 9:471-180.
39. Krejci, L., S. Van Komen, Y. Li, J. Villemain, M. S. Reddy, H. Klein, T. Ellenberger, and P. Sung. 2003. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305-309.
40. Kusano, K., M. E. Berres, and W. R. Engels. 1999. Evolution of the RECQ family of helicases: a Drosophila homolog, Dmblm, is similar to the human bloom syndrome gene. Genetics 151:1027-1039.
41. Lee, S. K., R. E. Johnson, S. L. Yu, L. Prakash, and S. Prakash. 1999. Requirement of yeast SGS1 and SRS2 genes for replication and transcription. Science 286:2339-2342.
42. Liberi, G., I. Chiolo, A. Pellicioli, M. Lopes, P. Plevani, M. Muzi-Falconi, and M. Foiani. 2000. Srs2 DNA helicase is involved in checkpoint response and its regulation requires a functional Mec1-dependent pathway and Cdk1 activity. EMBO J. 19:5027-5038.
43. Lopes, M., C. Cotta-Ramusino, G. Liberi, and M. Foiani. 2003. Branch migrating sister chromatid junctions form at replication origins through Rad51/Rad52-independent mechanisms. Mol. Cell 12:1499-1510.
44. Lou, G., I. M. Santoro, L. D. McDaniel, I. Nishijima, M. Mills, H. Youssoufian, H. Vogel, R. A. Schultz, and A. Bradley. 2000. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat. Genet. 26:424-429.
45. Mirzoeva, O. K., and J. H. Petrini. 2001. DNA damage-dependent nuclear dynamics of the Mre11 complex. Mol. Cell. Biol. 21:281-288.
46. Miyagawa, K. 1998. Genetic instability and cancer. Int. J. Hematol. 67:3-14.
47. Modesti, M., and R. Kanaar. 2001. Homologous recombination: from model organisms to human disease. Genome Biol. 2:1014.1-1014.5.
48. Mullen, J. R., V. Kaliraman, S. S. Ibrahim, and S. J. Brill. 2001. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157:103-118.
49. Myung, K., A. Datta, C. Chen, and R. D. Kolodner. 2001. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homologous recombination. Nat. Genet. 27:113-116.
50. Ohhata, T., R. Araki, R. Fukumura, A. Kuroiwa, Y. Matsuda, and M. Abe. 2001. Cloning, genomic structure and chromosomal localization of the gene encoding mouse DNA helicase RECQL5β. Gene 280:59-66.
51. Ooi, S. L., D. D. Shoemaker, and J. D. Boeke. 2003. DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat. Genet. 35:277-286.
52. Rong, L., and H. L. Klein. 1993. Purification and characterization of the SRS2 DNA helicase of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 268:1252-1259.
53. Rong, L., F. Palladino, A. Aguilera, and H. L. Klein. 1991. The hyper-gene conversion hpr5-1 mutation of Saccharomyces cerevisiae is an allele of the SRS2/RADH gene. Genetics 127:75-85.
54. Rothstein, R., B. Michel, and S. Gangloff. 2000. Replication fork pausing and recombination or "gimme a break." Genes Dev. 14:1-10.
55. Schiestl, R. H., S. Prakash, and L. Prakash. 1990. The SRS2 suppressor of rad6 mutations of Saccharomyes cerevisiae acts by channeling DNA lesions into the RAD52 DNA repair pathway. Genetics 124:817-831.
56. 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.
57. Schmidt, K. H., K. L. Derry, and R. D. Kolodner. 2002. Saccharomyces cerevisiae RRM3, a 5′ to 3′ DNA helicase, physically interacts with proliferating cell nuclear antigen. J. Biol. Chem. 277:45331-45337.
58. Scholes, D. T., M. Banerjee, B. Bowen, and M. J. Curcio. 2001. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159:1449-1465.
59. Seigneur, M., V. Bidnenko, S. D. Ehrlich, and B. Michel. 1998. RuvAB acts at arrested replication forks. Cell 95:419-430.
60. Shor, E., S. Gangloff, M. Wagner, J. Weinstein, G. Price, and R. Rothstein. 2002. Mutations in homologous recombination genes rescue top3 slow growth in Saccharomyces cerevisiae. Genetics 162:647-662.
61. Smith, G. R. 2001. Homologous recombination near and far from DNA breaks: alternative roles and contrasting views. Annu. Rev. Genet. 35:243-274.
62. Szostak, J. W., T. L. Orr-Weaver, R. J. Rothstein, and F. W. Stahl. 1983. The double strand-break repair model for recombination. Cell 33:25-35.
63. Taylor, A. F., and G. R. Smith. 2003. RecBCD enzyme is a DNA helicase with fast and slow motors of opposite polarity. Nature 423:889-893.
64. Tong, A. H., M. Evangelista, A. B. Parsons, H. Xu, G. D. Bader, N. Page, M. Robinson, S. Raghibizadeh, C. W. Hogue, H. Bussey, B. Andrews, M. Tyers, and C. Boone. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294:2364-2368.
65. Torres, J. Z., S. L. Schnakenberg, and V. A. Zakian. 2004. The Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol. Cell. Biol. 24:3198-3212.
66. Tsukamoto, Y., A. K. Taggart, and V. A. Zakian. 2001. The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr. Biol. 11:1328-1335.
67. Usui, T., H. Ogawa, and J. H. Petrini. 2001. A DNA damage response pathway controlled by Te11 and the Mre11 complex. Mol. Cell 7:1255-1266.
68. Veaute, X., J. Jeusset, C. Soustelle, S. C. Kowalczykowski, E. Le Cam, and F. Fabre. 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309-312.
69. Vennos, E. M., and W. D. James. 1995. Rothmund-Thomson syndrome Dermatol. Clin. 13:143-150.
70. Watt, P. M., I. D. Hickson, R. H. Borts, and E. J. Louis. 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.
71. Watt, P. M., E. J. Louis, R. H. Borts, and I. D. Hickson. 1995. Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell 81:253-260.
72. West, S. C. 1995. Formation, translocation and resolution of Holliday junctions during homologous genetic recombination. Philos. Trans. R. Soc. London B 347:21-25.
73. Whitby, M. C., F. Osman, and J. Dixon. 2003. Cleavage of model replication forks by fission yeast Mus81-Eme1 and budding yeast Mus81-Mms4. J. Biol. Chem. 278:6928-6935.
74. Wu, L., and I. D. Dickson. 2002. RecQ helicases and cellular responses to DNA damage. Mutat. Res. 509:35-47.
75. Yamagata, K., J. Kato, A. Shimamoto, M. Goto, Y. Furuichi, and H. Ikeda. 1998. Bloom's and Werner's syndrome genes suppress hyperrecombination in yeast sgv1 mutant: implication for genomic instability in human diseases. Proc. Natl. Acad. Sci. USA 95:8733-8738.
76. Zou, H., and R. Rothstein. 1997. Holliday junctions accumulate in replication mutants vía via a RecA homolog-independent mechanism. Cell 90:87-96.