A postsynaptic role for Rhp55/57 that is responsible for cell death in Δrqh1 mutants following replication arrest in Schizosaccharomyces pombe

Genetics

Volumn 170, Issue 2, 2005, Pages 519-531

  Hope, Justin C ^a   Maftahi, Mohamed ^b   Freyer, Greg A ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYUREA; NUCLEOPROTEIN; RAD51 PROTEIN; RAD55 PROTEIN; RAD57 PROTEIN; RECQ HELICASE; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; CHEMOLUMINESCENCE; CHROMOSOME ABERRATION; DNA DAMAGE; EPISTASIS; FUNGAL GENE; FUNGUS MUTANT; GENE OVEREXPRESSION; HOMOLOGOUS RECOMBINATION; MITOSIS INHIBITION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; SCHIZOSACCHAROMYCES POMBE;

ADENOSINE TRIPHOSPHATASES; CELL DEATH; DNA DAMAGE; DNA HELICASES; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTROPHORESIS, GEL, PULSED-FIELD; GENETIC COMPLEMENTATION TEST; GENOTYPE; HYDROXYUREA; MITOSIS; MODELS, GENETIC; MUTATION; NUCLEOPROTEINS; PLASMIDS; RECOMBINATION, GENETIC; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SENSITIVITY AND SPECIFICITY; SYNAPSES; TIME FACTORS;

SACCHAROMYCETALES; SCHIZOSACCHAROMYCES POMBE;

EID: 22144478694     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.037598     Document Type: Article

References (67)

1. AKAMATSU, Y., D. DZIADKOWIEC, M. IKEGUCHI, H. SHINAGAWA and H. IWASAKI, 2003 Two different Swi5-containing protein complexes are involved in mating-type switching and recombination repair in fission yeast. Proc. Natl. Acad. Sci. USA 100: 15770-15775.
2. 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.
3. BODDY, M. N., P. H. GAILLARD, W. H. MCDONALD, P. SHANAHAN, J. R. YATES, III et al., 2001 Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107: 537-548.
4. BRENNEMAN, M. A., B. M. WAGENER, C. A. MILLER, C. ALLEN and J. A. NICKOLOFF, 2002 XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination. Mol. Cell 10: 387-395.
5. BRESSAN, D. A., B. K. BAXTER and J. H. PETRINI, 1999 The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 7681-7687.
6. CARR, A. M., 2002 DNA structure dependent checkpoints as regulators of DNA repair. DNA Repair 1: 983-994.
7. CASPARI, T., J. M. MURRAY and A. M. CARR, 2002 Cdc2-cyclin B kinase activity links Crb2 and Rqh1-topoisomerase III. Genes Dev. 16: 1195-1208.
8. CHA, R. S., and N. KLECKNER, 2002 ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297: 602-606.
9. COX, M. M., M. F. GOODMAN, K. N. KREUZER, D. J. SHERRATT, S. J. SANDLER et al., 2000 The importance of repairing stalled replication forks. Nature 404: 37-41.
10. 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.
11. DAVEY, S., C. S. HAN, S. A. RAMER, J. C. KLASSEN, A. JACOBSON et al., 1998 Fission yeast rad12+ regulates cell cycle checkpoint control and is homologous to the Bloom's syndrome disease gene. Mol. Cell. Biol. 18: 2721-2728.
12. DIFFLEY, J. F., K. BOUSSET, K. LABIB, E. A. NOTON, C. SANTOCANALE et al., 2000 Coping with and recovering from hydroxyurea-induced replication fork arrest in budding yeast. Cold Spring Harbor Symp. Quant. Biol. 65: 333-342.
13. DOE, C. L., and M. C. WHITBY, 2004 The involvement of Srs2 in post-replication repair and homologous recombination in fission yeast. Nucleic Acids Res. 32: 1480-1491.
14. DOE, C. L., J. DIXON, F. OSMAN and M. C. WHITBY, 2000 Partial suppression of the fission yeast rqh1(-) phenotype by expression of a bacterial Holliday junction resolvase. EMBO J. 19: 2751-2762.
15. DOE, C. L., J. S. AHN, J. DIXON and M. C. WHITBY, 2002 Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J. Biol. Chem. 277: 32753-32759.
16. EGEL, R., D. H. BEACH and A. J. KLAR, 1984 Genes required for initiation and resolution steps of mating-type switching in fission yeast. Proc. Natl. Acad. Sci. USA 81: 3481-3485.
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: 16887-16892.
18. FORTIN, G. S., and L. S. SYMINGTON, 2002 Mutations in yeast Rad51 that partially bypass the requirement for Rad55 and Rad57 in DNA repair by increasing the stability of Rad51-DNA complexes. EMBO J. 21: 3160-3170.
19. FUKUSHIMA, K., Y. TANAKA, K. NABESHIMA, T. YONEKI, T. TOUGAN et al., 2000 Dmc1 of Schizosaccharomyces pombe plays a role in meiotic recombination. Nucleic Acids Res. 28: 2709-2716.
20. 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.
21. HABER, J. E., and W. D. HEYER, 2001 The fuss about Mus81. Cell 107: 551-554.
22. HAYS, S. L., A. A. FIRMENICH and P. BERG, 1995 Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc. Natl. Acad. Sci. USA 92: 6925-6929.
23. HELLEDAY, T., 2003 Pathways for mitotic homologous recombination in mammalian cells. Mutat. Res. 532: 103-115.
24. HEYER, W. D., K. T. EHMSEN and J. A. SOLINGER, 2003 Holliday junctions in the eukaryotic nucleus: resolution in sight? Trends Biochem. Sci. 28: 548-557.
25. IRA, G., A. MALKOVA, G. LIBERI, M. FOIANI and J. E. HABER, 2003 Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115: 401-411.
26. JANG, Y. K., Y. H. JIN, Y. S. SHIM, M. J. KIM, E. J. YOO et al., 1995 Evidences for possible involvement of Rhp51 protein in mitotic events including chromosome segregation. Biochem. Mol. Biol. Int. 37: 329-337.
27. JOHNSON, R. D., and L. S. SYMINGTON, 1995 Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol. Cell. Biol. 15: 4843-4850.
28. KHASANOV, F. K, G. V. SAVCHENKO, E. V. BASHKIROVA, V. G. KOROLEV, W. D. HEYER et al., 1999 A new recombinational DNA repair gene from Schizosaccharomyces pombe with homology to Escherichia coli RecA. Genetics 152: 1557-1572.
29. KIM, W. J., H. LEE, E. J. PARK, J. K. PARK and S. D. PARK, 2001 Gain- and loss-of-function of Rhp51, a Rad51 homolog in fission yeast, reveals dissimilarities in chromosome integrity. Nucleic Acids Res. 29: 1724-1732.
30. KUZMINOV, A., 1993 RuvA, RuvB and RuvC proteins: cleaning-up after recombinational repairs in E. coli. BioEssays 15: 355-358.
31. LAURSEN, L. V., E. AMPATZIDOU, A. H. ANDERSEN and J. M. MURRAY, 2003 Role for the fission yeast RecQ helicase in DNA repair in G2. Mol. Cell. Biol. 23: 3692-3705.
32. LIBERI, G., I. CHIOLO, A. PELLICIOLI, M. LOPES, P. PLEVANI et al., 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.
33. LIU, Y., J. Y. MASSON, R. SHAH, P. O'REGAN and S. C. WEST, 2004 RAD51C is required for Holliday junction processing in mammalian cells. Science 303: 243-246.
34. LOVETT, S. T., and R. K. MORTIMER, 1987 Characterization of null mutants of the RAD55 gene of Saccharomyces cerevisiae: effects of temperature, osmotic strength and mating type. Genetics 116: 547-553.
35. LUNDIN, C., K. ERIXON, C. ARNAUDEAU, N. SCHULTZ, D. JENSSEN et al., 2002 Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell. Biol. 22: 5869-5878.
36. MAFTAHI, M., J. C. HOPE, L. DELGADO-CRUZATA, C. S. HAN and G. A. FREYER, 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.
37. MAISNIER-PATIN, S., K. NORDSTROM and S. DASGUPTA, 2001 Replication arrests during a single round of replication of the Escherichia coli chromosome in the absence of DnaC activity. Mol. Microbiol. 42: 1371-1382.
38. MARCHETTI, M. A., S. KUMAR, E. HARTSUIKER, M. MAFTAHI, A. M. CARR et al., 2002 A single unbranched S-phase DNA damage and replication fork blockage checkpoint pathway. Proc. Natl. Acad. Sci. USA 99: 7472-7477.
39. MCGLYNN, P., and R. G. LLOYD, 2002 Recombinational repair and restart of damaged replication forks. Nat. Rev. Mol. Cell. Biol. 3: 859-870.
40. MICHEL, B., 2000 Replication fork arrest and DNA recombination. Trends Biochem. Sci. 25: 173-178.
41. MICHEL, B., S. D. EHRLICH and M. UZEST, 1997 DNA double-strand breaks caused by replication arrest. EMBO J. 16: 430-438.
42. MICHEL, B., M. J. FLORES, E. VIGUERA, G. GROMPONE, M. SEIGNEUR et al., 2001 Rescue of arrested replication forks by homologous recombination. Proc. Natl. Acad. Sci. USA 98: 8181-8188.
43. MURIS, D. F., K. VREEKEN, A. M. CARR, B. C. BROUGHTON, A. R. LEHMANN et al., 1993 Cloning the RAD51 homologue of Schizosaccharomyces pombe. Nucleic Acids Res. 21: 4586-4591.
44. MURIS, D. F., K. VREEKEN, A. M. CARR, J. M. MURRAY, C. SMIT et al., 1996 Isolation of the Schizosaccharomyces pombe RAD54 homologue, rhp54+, a gene involved in the repair of radiation damage and replication fidelity. J. Cell Sci. 109 (Pt. 1): 73-81.
45. MURIS, D. F., K. VREEKEN, H. SCHMIDT, K. OSTERMANN, B. CLEVER et al., 1997 Homologous recombination in the fission yeast Schizosaccharomyces pombe: different requirements for the rhp51+, rhp54+ and rad22+ genes. Curr. Genet. 31: 248-254.
46. MURRAY, J. M., H. D. LINDSAY, C. A. MUNDAY and A. M. CARR, 1997 Role of Schizosaccharomyces pombe RecQ homolog, recombination, and checkpoint genes in UV damage tolerance. Mol. Cell. Biol. 17: 6868-6875.
47. NELMS, B. E., R. S. MASER, J. F. MACKAY, M. G. LAGALLY and J. H. PETRINI, 1998 In situ visualization of DNA double-strand break repair in human fibroblasts. Science 280: 590-592.
48. NYBERG, K. A., R. J. MICHELSON, C. W. PUTNAM and T. A. WEINERT, 2002 Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36: 617-656.
49. OSTERMANN, K., A. LORENTZ and H. SCHMIDT, 1993 The fission yeast rad22 gene, having a function in mating-type switching and repair of DNA damages, encodes a protein homolog to Rad52 of Saccharomyces cerevisiae. Nucleic Acids Res. 21: 5940-5944.
50. PAQUES, F., and J. E. HABER, 1999 Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63: 349-404.
51. ROGAKOU, E. P., C. BOON, C. REDON and W. M. BONNER, 1999 Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146: 905-916.
52. SAINTIGNY, Y., F. DELACOTE, G. VARES, F. PETITOT, S. LAMBERT et al., 2001 Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 20: 3861-3870.
53. SHARPLES, G. J., S. M. INGLESTON and R. G. LLOYD, 1999 Holliday junction processing in bacteria: insights from the evolutionary conservation of RuvABC, RecG, and RusA. J. Bacteriol. 181: 5543-5550.
54. SOLINGER, J. A., G. LUTZ, T. SUGIYAMA, S. C. KOWALCZYKOWSKI and W. D. HEYER, 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.
55. STEWART, E., C. R. CHAPMAN, F. AL-KHODAIRY, A. M. CARR and T. ENOCH, 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.
56. SUNG, P., 1997 Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev. 11: 1111-1121.
57. SUTO, K., A. NAGATA, H. MURAKAMI and H. OKAYAMA, 1999 A double-strand break repair component is essential for S phase completion in fission yeast cell cycling. Mol. Biol. Cell 10: 3331-3343.
58. 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.
59. TRUJILLO, K. M., D. H. ROH, L. CHEN, S. VAN KOMEN, A. TOMKINSON et al., 2003 Yeast xrs2 binds DNA and helps target rad50 and mre11 to DNA ends. J. Biol. Chem. 278: 48957-48964.
60. TSUTSUI, Y., T. MORISHITA, H. IWASAKI, H. TOH and H. SHINAGAWA, 2000 A recombination repair gene of Schizosaccharomyces pombe, rhp57, is a functional homolog of the Saccharomyces cerevisiae RAD57gene and is phylogenetically related to the human XRCC3 gene. Genetics 154: 1451-1461.
61. UENO, M., T. NAKAZAKI, Y. AKAMATSU, K. WATANABE, K. TOMITA et al., 2003 Molecular characterization of the Schizosaccharomyces pombe nbs1+ gene involved in DNA repair and telomere maintenance. Mol. Cell. Biol. 23: 6553-6563.
62. VAN DEN BOSCH, M., K. VREEKEN, J. B. ZONNEVELD, J. A. BHANDSMA, M. LOMBAERTS et al., 2001 Characterization of RAD52 homologs in the fission yeast Schizosaccharomyces pombe. Mutat. Res. 461: 311-323.
63. VAN KOMEN, S., G. PETUKHOVA, S. SIGURDSSON, S. STRATTON and P. SUNG, 2000 Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol. Cell 6: 563-572.
64. VAN KOMEN, S., G. PETUKHOVA, S. SIGURDSSON and P. SUNG, 2002 Functional cross-talk among Rad51, Rad54, and replication protein A in heteroduplex DNA joint formation. J. Biol. Chem. 277: 43578-43587.
65. WILSON, S., N. WARR, D. L. TAYLOR and F. Z. WATTS, 1999 The role of Schizosaccharomyces pombe Rad32, the Mre11 homologue, and other DNA damage response proteins in non-homologous end joining and telomere length maintenance. Nucleic Acids Res. 27: 2655-2661.
66. WU, L., and I. D. HICKSON, 2003 The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874.
67. YOKOYAMA, H., H. KURUMIZAKA, S. IKAWA, S. YOKOYAMA and T. SHIBATA, 2003 Holliday junction binding activity of the human Rad51B protein. J. Biol. Chem. 278: 2767-2772.