Molecular characterization of the role of the Schizosaccharomyces pombe nip1+/ctp1+ gene in DNA double-strand break repair in association with the Mre11-Rad50-Nbs1 complex

Molecular and Cellular Biology

Volumn 28, Issue 11, 2008, Pages 3639-3651

  Akamatsu, Yufuko ^a,d   Murayama, Yasuto ^a   Yamada, Takatomi ^b   Nakazaki, Tomofumi ^a   Tsutsui, Yasuhiro ^c   Ohta, Kunihiro ^b   Iwasaki, Hiroshi ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDRO 7 HYDROXY 6,6 DIMETHYL 8 (2 OXO 1 PIPERIDYL) 6H PYRANO[2,3 F][2,1,3]BENZOXADIAZOLE; BLEOMYCIN; BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; CHECKPOINT KINASE 1; COMPLEMENTARY DNA; CYCLIN DEPENDENT KINASE ACTIVATING KINASE; CYTIDINE TRIPHOSPHATE; FUNGAL DNA; MRE11 PROTEIN; NIBRIN; RAD50 PROTEIN;

ARABIDOPSIS; ARTICLE; ASPERGILLUS; CARBOXY TERMINAL SEQUENCE; CELL CLONE; CELL CYCLE; CELL CYCLE REGULATION; CELL STRAIN; DNA DAMAGE; DNA REPAIR; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FUNGAL CELL CULTURE; FUNGAL GENE; GENE EXPRESSION; GENE INTERACTION; GENE MUTATION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC CONSERVATION; GENETIC EPISTASIS; GENETIC RECOMBINATION; IMMUNOPRECIPITATION; MUTAGENESIS; NONHUMAN; NUCLEIC ACID METABOLISM; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY; TERMINAL OLIGOPYRIMIDINE TRACT; TRANSCRIPTION TERMINATION; WESTERN BLOTTING;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CHROMOSOMAL PROTEINS, NON-HISTONE; CONSERVED SEQUENCE; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; EPISTASIS, GENETIC; MEIOSIS; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RAD51 RECOMBINASE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

ASPERGILLUS; FUNGI; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE; VERTEBRATA;

EID: 44349086462     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01828-07     Document Type: Article

References (81)

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. Alani, E., R. Padmore, and N. Kleckner. 1990. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61:419-436.
3. Amador, V., S. Ge, P. G. Santamaria, D. Guardavaccaro, and M. Pagano. 2007. APC/C(Cdc20) controls the ubiquitin-mediated degradation of p21 in prometaphase. Mol. Cell 27:462-473.
4. Arora, C., K. Kee, S. Maleki, and S. Keeney. 2004. Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol. Cell 13:549-559.
5. Baroni, E., V. Viscardi, H. Cartagena-Lirola, G. Lucchini, and M. P. Longhese. 2004. The functions of budding yeast Sae2 in the DNA damage response require Mec1- and Tel1-dependent phosphorylation. Mol. Cell. Biol. 24:4151-4165.
6. Bhaskara, V., A. Dupre, B. Lengsfeld, B. B. Hopkins, A. Chan, J. H. Lee, X. Zhang, J. Gautier, V. Zakian, and T. T. Paull. 2007. Rad50 adenylate kinase activity regulates DNA tethering by Mre11/Rad50 complexes. Mol. Cell 25:647-661.
7. Borde, V., W. Lin, E. Novikov, J. H. Petrini, M. Lichten, and A. Nicolas. 2004. Association of Mre11p with double-strand break sites during yeast meiosis. Mol. Cell 13:389-401.
8. Carney, J. P., R. S. Maser, H. Olivares, E. M. Davis, M. Le Beau, J. R. Yates III, L. Hays, W. F. Morgan, and J. H. Petrini. 1998. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93:477-486.
9. Cervantes, M. D., J. A. Farah, and G. R. Smith. 2000. Meiotic DNA breaks associated with recombination in S. pombe. Mol. Cell 5:883-888.
10. Chahwan, C., T. M. Nakamura, S. Sivakumar, P. Russell, and N. Rhind. 2003. The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol. Cell. Biol. 23:6564-6573.
11. Chinnadurai, G. 2006. CtIP, a candidate tumor susceptibility gene is a team player with luminaries. Biochim. Biophys. Acta 1765:67-73.
12. Clerici, M., D. Mantiero, G. Lucchini, and M. P. Longhese. 2006. The Saccharomyces cerevisiae Sae2 protein negatively regulates DNA damage checkpoint signalling. EMBO Rep. 7:212-218.
13. Clerici, M., D. Mantiero, G. Lucchini, and M. P. Longhese. 2005. The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J. Biol. Chem. 280:38631-38638.
14. 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.
15. D'Amours, D., and S. P. Jackson. 2001. The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 15:2238-2249.
16. Debrauwère, H., S. Loeillet, W. Lin, J. Lopes, and A. Nicolas. 2001. Links between replication and recombination in Saccharomyces cerevisiae: a hypersensitive requirement for homologous recombination in the absence of Rad27 activity. Proc. Natl. Acad. Sci. USA 98:8263-8269.
17. de Jager, M., J. van Noort, D. C. van Gent, C. Dekker, R. Kanaar, and C. Wyman. 2001. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell 8:1129-1135.
18. Deveaux, Y., B. Alonso, O. Pierrugues, C. Godon, and M. Kazmaier. 2000. Molecular cloning and developmental expression of AtGR1, a new growth-related Arabidopsis gene strongly induced by ionizing radiation. Radiat. Res. 154:355-364.
19. Difilippantonio, S., A. Celeste, O. Fernandez-Capetillo, H. T. Chen, B. Reina San Martin, F. Van Laethem, Y. P. Yang, G. V. Petukhova, M. Eckhaus, L. Feigenbaum, K. Manova, M. Kruhlak, R. D. Camerini-Otero, S. Sharan, M. Nussenzweig, and A. Nussenzweig. 2005. Role of Nbs1 in the activation of the Atm kinase revealed in humanized mouse models. Nat. Cell Biol. 7:675-685.
20. Dubin, M. J., P. H. Stokes, E. Y. Sum, R. S. Williams, V. A. Valova, P. J. Robinson, G. J. Lindeman, J. N. Glover, J. E. Visvader, and J. M. Matthews. 2004. Dimerization of CtIP, a BRCA1- and CtBP-interacting protein, is mediated by an N-terminal coiled-coil motif. J. Biol. Chem. 279:26932-26938.
21. Dupré, A., L. Boyer-Chatenet, and J. Gautier. 2006. Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex. Nat. Struct. Mol. Biol. 13:451-457.
22. Durocher, D., J. Henckel, A. R. Fersht, and S. P. Jackson. 1999. The FHA domain is a modular phosphopeptide recognition motif. Mol. Cell 4:387-394.
23. Furuse, M., Y. Nagase, H. Tsubouchi, K. Murakami-Murofushi, T. Shibata, and K. Ohta. 1998. Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J. 17:6412-6425.
24. Fusco, C., A. Reymond, and A. S. Zervos. 1998. Molecular cloning and characterization of a novel retinoblastoma-binding protein. Genomics 51:351-358.
25. Glotzer, M., A. W. Murray, and M. W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature 349:132-138.
26. Greenberg, R. A., B. Sobhian, S. Pathania, S. B. Cantor, Y. Nakatani, and D. M. Livingston. 2006. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev. 20:34-46.
27. Harrison, J. C., and J. E. Haber. 2006. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 40:209-235.
28. Hartsuiker, E., E. Vaessen, A. M. Carr, and J. Kohli. 2001. Fission yeast Rad50 stimulates sister chromatid recombination and links cohesion with repair. EMBO J. 20:6660-6671.
29. Hopfner, K. P., L. Craig, G. Moncalian, R. A. Zinkel, T. Usui, B. A. Owen, A. Karcher, B. Henderson, J. L. Bodmer, C. T. McMurray, J. P. Carney, J. H. Petrini, and J. A. Tainer. 2002. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418:562-566.
30. Hopfner, K. P., A. Karcher, L. Craig, T. T. Woo, J. P. Carney, and J. A. Tainer. 2001. Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105:473-485.
31. Keeney, S. 2001. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52:1-53.
32. Keeney, S., C. N. Giroux, and N. Kleckner. 1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375-384.
33. Keeney, S., and N. Kleckner. 1995. Covalent protein-DNA complexes at the 5′ strand termini of meiosis-specific double-strand breaks in yeast. Proc. Natl. Acad. Sci. USA 92:11274-11278.
34. King, R. W., M. Glotzer, and M. W. Kirschner. 1996. Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol. Biol. Cell 7:1343-1357.
35. Krogh, B. O., and L. S. Symington. 2004. Recombination proteins in yeast. Annu. Rev. Genet. 38:233-271.
36. Lee, J. H., and T. T. Paull. 2004. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304:93-96.
37. Li, J., G. W. Hooker, and G. S. Roeder. 2006. Saccharomyces cerevisiae Mer2, Mei4 and Rec114 form a complex required for meiotic double-strand break formation. Genetics 173:1969-1981.
38. Li, S., N. S. Ting, L. Zheng, P. L. Chen, Y. Ziv, Y. Shiloh, E. Y. Lee, and W. H. Lee. 2000. Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature 406:210-215.
39. Limbo, O., C. Chahwan, Y. Yamada, R. A. de Bruin, C. Wittenberg, and P. Russell. 2007. Ctp1 is a cell cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 28:134-146.
40. Lupas, A., M. Van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science 252:1162-1164.
41. Matsuura, S., H. Tauchi, A. Nakamura, N. Kondo, S. Sakamoto, S. Endo, D. Smeets, B. Solder, B. H. Belohradsky, V. M. Der Kaloustian, M. Oshimura, M. Isomura, Y. Nakamura, and K. Komatsu. 1998. Positional cloning of the gene for Nijmegen breakage syndrome. Nat. Genet. 19:179-181.
42. McKee, A. H. Z., and N. Kleckner. 1997. A general method for identifying recessive diploid-specific mutations in Saccharomyces cerevisiae, its application to the isolation of mutants blocked at intermediate stages of meiotic prophase and characterization of a new gene SAE2. Genetics 146:797-816.
43. Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795-823.
44. Morikawa, H., T. Morishita, S. Kawane, H. Iwasaki, A. M. Carr, and H. Shinagawa. 2004. Rad62 protein functionally and physically associates with the smc5/smc6 protein complex and is required for chromosome integrity and recombination repair in fission yeast. Mol. Cell. Biol. 24:9401-9413.
45. Morishita, T., F. Furukawa, C. Sakaguchi, T. Toda, A. M. Carr, H. Iwasaki, and H. Shinagawa. 2005. Role of the Schizosaccharomyces pombe F-box DNA helicase in processing recombination intermediates. Mol. Cell. Biol. 25:8074-8083.
46. Morishita, T., Y. Tsutsui, H. Iwasaki, and H. Shinagawa. 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.
47. Murray, J. M., M. Tavassoli, R. al-Harithy, K. S. Sheldrick, A. R. Lehmann, A. M. Carr, and F. Z. Watts. 1994. Structural and functional conservation of the human homolog of the Schizosaccharomyces pombe rad2 gene, which is required for chromosome segregation and recovery from DNA damage. Mol. Cell. Biol. 14:4878-4888.
48. Nairz, K., and F. Klein. 1997. mre11S - a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev. 11:2272-2290.
49. Nakada, D., K. Matsumoto, and K. Sugimoto. 2003. ATM-related Te11 associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev. 17:1957-1962.
50. Neale, M. J., J. Pan, and S. Keeney. 2005. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053-1057.
51. Pâques, 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.
52. Paull, T. T., and M. Gellert. 1998. The 3′ to 5′ exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol. Cell 1:969-979.
53. Pringle, J. R., A. E. Adams, D. G. Drubin, and B. K. Haarer. 1991. Immunofluorescence methods for yeast. Methods Enzymol. 194:565-602.
54. Prinz, S., A. Amon, and F. Klein. 1997. Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. Genetics 146:781-795.
55. Rattray, A. J., C. B. McGill, B. K. Shafer, and J. N. Strathern. 2001. Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics 158:109-122.
56. Roeder, G. S. 1997. Meiotic chromosomes: it takes two to tango. Genes Dev. 11:2600-2621.
57. Schaeper, U., T. Subramanian, L. Lim, J. M. Boyd, and G. Chinnadurai. 1998. Interaction between a cellular protein that binds to the C-terminal region of adenovirus E1A (CtBP) and a novel cellular protein is disrupted by E1A through a conserved PLDLS motif. J. Biol. Chem. 273:8549-8552.
58. Sung, P., and H. Klein. 2006. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 7:739-750.
59. Symington, L. S. 1998. Homologous recombination is required for the viability of rad27 mutants. Nucleic Acids Res. 26:5589-5595.
60. 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.
61. Tavassoli, M., M. Shayeghi, A. Nasim, and F. Z. Watts. 1995. Cloning and characterisation of the Schizosaccharomyces pombe rad32 gene: a gene required for repair of double strand breaks and recombination. Nucleic Acids Res. 23:383-388.
62. Trujillo, K. M., S. S. Yuan, E. Y. Lee, and P. Sung. 1998. Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem. 273:21447-21450.
63. Tsukamoto, Y., C. Mitsuoka, M. Terasawa, H. Ogawa, and T. Ogawa. 2005. Xrs2p regulates Mre11p translocation to the nucleus and plays a role in telomere elongation and meiotic recombination. Mol. Biol. Cell 16:597-608.
64. 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 RAD57 gene and is phylogenetically related to the human XRCC3 gene. Genetics 154:1451-1461.
65. Tsutsui, Y., T. Morishita, T. Natsume, K. Yamashita, H. Iwasaki, F. Yamao, and H. Shinagawa. 2005. Genetic and physical interactions between Schizosaccharomyces pombe Mcl1 and Rad2, Dna2 and DNA polymerase α: evidence for a multifunctional role of Mcl1 in DNA replication and repair. Curr. Genet. 48:34-43.
66. Uanschou, C., T. Siwiec, A. Pedrosa-Harand, C. Kerzendorfer, E. Sanchez-Moran, M. Novatchkova, S. Akimcheva, A. Woglar, F. Klein, and P. Schlogelhofer. 2007. A novel plant gene essential for meiosis is related to the human CtIP and the yeast COM1/SAE2 gene. EMBO J. 26:5061-5070.
67. + gene involved in DNA repair and telomere maintenance. Mol. Cell. Biol. 23:6553-6563.
68. 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.
69. Usui, T., T. Ohta, H. Oshiumi, J. Tomizawa, H. Ogawa, and T. Ogawa. 1998. Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95:705-716.
70. Varon, R., C. Vissinga, M. Platzer, K. M. Cerosaletti, K. H. Chrzanowska, K. Saar, G. Beckmann, E. Seemanova, P. R. Cooper, N. J. Nowak, M. Stumm, C. M. Weemaes, R. A. Gatti, R. K. Wilson, M. Digweed, A. Rosenthal, K. Sperling, P. Concannon, and A. Reis. 1998. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 93:467-476.
71. Watson, A., J. Mata, J. Bahler, A. Carr, and T. Humphrey. 2004. Global gene expression responses of fission yeast to ionizing radiation. Mol. Biol. Cell 15:851-860.
72. Wilson, S., M. Tavassoli, and F. Z. Watts. 1998. Schizosaccharomyces pombe rad32 protein: a phosphoprotein with an essential phosphoesterase motif required for repair of DNA double strand breaks. Nucleic Acids Res. 26:5261-5269.
73. 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.
74. Wong, A. K., P. A. Ormonde, R. Pero, Y. Chen, L. Lian, G. Salada, S. Berry, Q. Lawrence, P. Dayananth, P. Ha, S. V. Tavtigian, D. H. Teng, and P. L. Bartel. 1998. Characterization of a carboxy-terminal BRCA1 interacting protein. Oncogene 17:2279-2285.
75. Wu, G., and W. H. Lee. 2006. CtIP, a multivalent adaptor connecting transcriptional regulation, checkpoint control and tumor suppression. Cell Cycle 5:1592-1596.
76. You, Z., C. Chahwan, J. Bailis, T. Hunter, and P. Russell. 2005. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol. 25:5363-5379.
77. Young, J. A., R. W. Hyppa, and G. R. Smith. 2004. Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167:593-605.
78. Young, J. A., R. W. Schreckhise, W. W. Steiner, and G. R. Smith. 2002. Meiotic recombination remote from prominent DNA break sites in S. pombe. Mol. Cell 9:253-263.
79. Yu, X., and J. Chen. 2004. DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol. Cell. Biol. 24:9478-9486.
80. Yu, X., S. Fu, M. Lai, R. Baer, and J. Chen. 2006. BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. Genes Dev. 20:1721-1726.
81. Yu, X., L. C. Wu, A. M. Bowcock, A. Aronheim, and R. Baer. 1998. The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J. Biol. Chem. 273:25388-25392.