Brc1-dependent recovery from replication stress

Journal of Cell Science

Volumn 125, Issue 11, 2012, Pages 2753-2764

  Bass, Kirstin L ^a   Murray, Johanne M ^b   O'Connell, Matthew J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Brc1; DNA replication; Fission yeast; Recombination

Indexed keywords

BINDING PROTEIN; BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; CHECKPOINT KINASE 1; DOUBLE STRANDED DNA; HISTONE H2A; ORIGIN RECOGNITION COMPLEX; PRIMER DNA; RAD51 PROTEIN; RAD52 PROTEIN; RECOMBINANT PROTEIN; SINGLE STRANDED DNA;

ARTICLE; BIOACCUMULATION; CELL CYCLE S PHASE; CELL DIVISION; CELL STRESS; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENE SEQUENCE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN STRUCTURE; REPLICATION STRESS; SCHIZOSACCHAROMYCES POMBE;

DNA REPLICATION; DNA, RIBOSOMAL; HYDROXYUREA; MUTAGENESIS; MUTATION; ORIGIN RECOGNITION COMPLEX; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC; REPLICATION PROTEIN A; S PHASE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84864968016     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.103119     Document Type: Article

References (64)

1. Ahn, J. S., Osman, F. and Whitby, M. C. (2005). Replication fork blockage by RTS1 at an ectopic site promotes recombination in fission yeast. EMBO J. 24, 2011-2023.
2. Ampatzidou, E., Irmisch, A., O'Connell, M. J. and Murray, J. M. (2006). Smc5/6 is required for repair at collapsed replication forks. Mol. Cell. Biol. 26, 9387-9401.
3. Andrews, E. A., Palecek, J., Sergeant, J., Taylor, E., Lehmann, A. R. and Watts, F. Z. (2005). Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell. Biol. 25, 185-196.
4. Bailis, J. M., Luche, D. D., Hunter, T. and Forsburg, S. L. (2008). Minichromosome maintenance proteins interact with checkpoint and recombination proteins to promote S-phase genome stability. Mol. Cell. Biol. 28, 1724-1738.
5. Branzei, D. and Foiani, M. (2008). Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 9, 297-308.
6. Branzei, D. and Foiani, M. (2009). The checkpoint response to replication stress. DNA Repair (Amst.) 8, 1038-1046.
7. Byun, T. S., Pacek, M., Yee, M. C., Walter, J. C. and Cimprich, K. A. (2005). Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 19, 1040-1052.
8. Calonge, T. M. and O'Connell, M. J. (2006). Antagonism of Chk1 signaling in the G2 DNA damage checkpoint by dominant alleles of Cdr1. Genetics 174, 113-123.
9. Calonge, T. M., Eshaghi, M., Liu, J., Ronai, Z. and O'Connell, M. J. (2010). Transformation/transcription domain-associated protein (TRRAP)-mediated regulation of Wee1. Genetics 185, 81-93.
10. Coulon, S., Gaillard, P. H., Chahwan, C., McDonald, W. H., Yates, J. R., 3rd and Russell, P. (2004). Slx1-Slx4 are subunits of a structure-specific endonuclease that maintains ribosomal DNA in fission yeast. Mol. Biol. Cell 15, 71-80.
11. Doe, C. L. and Whitby, M. C. (2004). The involvement of Srs2 in post-replication repair and homologous recombination in fission yeast. Nucleic Acids Res. 32, 1480-1491.
12. Doe, C. L., Osman, F., Dixon, J. and Whitby, M. C. (2004). DNA repair by a Rad22-Mus81-dependent pathway that is independent of Rhp51. Nucleic Acids Res. 32, 5570-5581.
13. Forsburg, S. L. and Nurse, P. (1991). Cell cycle regulation in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Annu. Rev. Cell Biol. 7, 227-256.
14. Frampton, J., Irmisch, A., Green, C. M., Neiss, A., Trickey, M., Ulrich, H. D., Furuya, K., Watts, F. Z., Carr, A. M. and Lehmann, A. R. (2006). Postreplication repair and PCNA modification in Schizosaccharomyces pombe. Mol. Biol. Cell 17, 2976-2985.
15. Grallert, B. and Nurse, P. (1996). The ORC1 homolog orp1 in fission yeast plays a key role in regulating onset of S phase. Genes Dev. 10, 2644-2654.
16. Gulli, M. P., Girard, J. P., Zabetakis, D., Lapeyre, B., Melese, T. and Caizergues-Ferrer, M. (1995). gar2 is a nucleolar protein from Schizosaccharomyces pombe required for 18S rRNA and 40S ribosomal subunit accumulation. Nucleic Acids Res. 23, 1912-1918.
17. Heichinger, C., Penkett, C. J., Bähler, J. and Nurse, P. (2006). Genome-wide characterization of fission yeast DNA replication origins. EMBO J. 25, 5171-5179.
18. Hirano, T. (2006). At the heart of the chromosome: SMC proteins in action. Nat. Rev. Mol. Cell Biol. 7, 311-322.
19. Huang, J., Huen, M. S., Kim, H., Leung, C. C., Glover, J. N., Yu, X. and Chen, J. (2009). RAD18 transmits DNA damage signalling to elicit homologous recombina-tion repair. Nat. Cell Biol. 11, 592-603.
20. 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.
21. Irmisch, A., Ampatzidou, E., Mizuno, K., O'Connell, M. J. and Murray, J. M. (2009). Smc5/6 maintains stalled replication forks in a recombination-competent conformation. EMBO J. 28, 144-155.
22. Jensen, R. B., Carreira, A. and Kowalczykowski, S. C. (2010). Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 467, 678-683.
23. Kai, M. and Wang, T. S. (2003). Checkpoint responses to replication stalling: inducing tolerance and preventing mutagenesis. Mutat. Res. 532, 59-73.
24. 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.
25. Kim, S. M. and Huberman, J. A. (2001). Regulation of replication timing in fission yeast. EMBO J. 20, 6115-6126.
26. Kojic, M., Mao, N., Zhou, Q., Lisby, M. and Holloman, W. K. (2008). Compensatory role for Rad52 during recombinational repair in Ustilago maydis. Mol. Microbiol. 67, 1156-1168.
27. Krejci, L., Van Komen, S., Li, Y., Villemain, J., Reddy, M. S., Klein, H., Ellenberger, T. and Sung, P. (2003). DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423, 305-309.
28. Krogh, B. O. and Symington, L. S. (2004). Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271.
29. Lambert, S., Watson, A., Sheedy, D. M., Martin, B. and Carr, A. M. (2005). Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell 121, 689-702.
30. Latif, C., den Elzen, N. R. and O'Connell, M. J. (2004). DNA damage checkpoint maintenance through sustained Chk1 activity. J. Cell Sci. 117, 3489-3498.
31. Lee, K. M., Nizza, S., Hayes, T., Bass, K. L., Irmisch, A., Murray, J. M. and O'Connell, M. J. (2007). Brc1-mediated rescue of Smc5/6 deficiency: requirement for multiple nucleases and a novel Rad18 function. Genetics 175, 1585-1595.
32. Lee, K. Y. and Myung, K. (2008). PCNA modifications for regulation of post-replication repair pathways. Mol. Cells 26, 5-11.
33. Lindsay, H. D., Griffiths, D. J. F., Edwards, R. J., Christensen, P. U., Murray, J. M., Osman, F., Walworth, N. and Carr, A. M. (1998). S-phase-specific activation of Cds1 kinase defines a subpathway of the checkpoint response in Schizosaccharomyces pombe. Genes Dev. 12, 382-395.
34. Lisby, M., Mortensen, U. H. and Rothstein, R. (2003). Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 5, 572-577.
35. Lupardus, P. J., Byun, T., Yee, M. C., Hekmat-Nejad, M. and Cimprich, K. A. (2002). A requirement for replication in activation of the ATR-dependent DNA damage checkpoint. Genes Dev. 16, 2327-2332.
36. MacDougall, C. A., Byun, T. S., Van, C., Yee, M. C. and Cimprich, K. A. (2007). The structural determinants of checkpoint activation. Genes Dev. 21, 898-903.
37. Meister, P., Taddei, A., Vernis, L., Poidevin, M., Gasser, S. M. and Baldacci, G. (2005). Temporal separation of replication and recombination requires the intra-S checkpoint. J. Cell Biol. 168, 537-544.
38. Moreno, S., Klar, A. and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
39. Morikawa, H., Morishita, T., Kawane, S., Iwasaki, H., Carr, A. M. and Shinagawa, H. (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.
40. Mortensen, U. H., Bendixen, C., Sunjevaric, I. and Rothstein, R. (1996). DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl. Acad. Sci. USA 93, 10729-10734.
41. Mortensen, U. H., Lisby, M. and Rothstein, R. (2009). Rad52. Curr. Biol. 19, R676-R677.
42. Noguchi, E., Noguchi, C., Du, L. L. and Russell, P. (2003). Swi1 prevents replication fork collapse and controls checkpoint kinase Cds1. Mol. Cell. Biol. 23, 7861-7874.
43. O'Connell, M. J. and Cimprich, K. A. (2005). G2 damage checkpoints: what is the turn-on? J. Cell Sci. 118, 1-6.
44. O'Connell, M. J., Raleigh, J. M., Verkade, H. M. and Nurse, P. (1997). Chk1 is a wee1 kinase in the G2 DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J. 16, 545-554.
45. O'Connell, M. J., Walworth, N. C. and Carr, A. M. (2000). The G2-phase DNA-damage checkpoint. Trends Cell Biol. 10, 296-303.
46. Ohouo, P. Y., Bastos de Oliveira, F. M., Almeida, B. S. and Smolka, M. B. (2010). DNA damage signaling recruits the Rtt107-Slx4 scaffolds via Dpb11 to mediate replication stress response. Mol. Cell 39, 300-306.
47. Osman, F., Fortunato, E. A. and Subramani, S. (1996). Double-strand break-induced mitotic intrachromosomal recombination in the fission yeast Schizosaccharomyces pombe. Genetics 142, 341-357.
48. Osman, F., Adriance, M. and McCready, S. (2000). The genetic control of spontaneous and UV-induced mitotic intrachromosomal recombination in the fission yeast Schizosaccharomyces pombe. Curr. Genet. 38, 113-125.
49. Outwin, E. A., Irmisch, A., Murray, J. M. and O'Connell, M. J. (2009). Smc5-Smc6-dependent removal of cohesin from mitotic chromosomes. Mol. Cell. Biol. 29, 4363-4375.
50. Pebernard, S., McDonald, W. H., Pavlova, Y., Yates, J. R., 3rd and Boddy, M. N. (2004). Nse1, Nse2, and a novel subunit of the Smc5-Smc6 complex, Nse3, play a crucial role in meiosis. Mol. Biol. Cell 15, 4866-4876.
51. Roberts, T. M., Kobor, M. S., Bastin-Shanower, S. A., Ii, M., Horte, S. A., Gin, J. W., Emili, A., Rine, J., Brill, S. J. and Brown, G. W. (2006). Slx4 regulates DNA damage checkpoint-dependent phosphorylation of the BRCT domain protein Rtt107/ Esc4. Mol. Biol. Cell 17, 539-548.
52. Sheedy, D. M., Dimitrova, D., Rankin, J. K., Bass, K. L., Lee, K. M., Tapia-Alveal, C., Harvey, S. H., Murray, J. M. and O'Connell, M. J. (2005). Brc1-mediated DNA repair and damage tolerance. Genetics 171, 457-468.
53. Szüts, D., Simpson, L. J., Kabani, S., Yamazoe, M. and Sale, J. E. (2006). Role for RAD18 in homologous recombination in DT40 cells. Mol. Cell. Biol. 26, 8032-8041.
54. Tapia-Alveal, C. and O'Connell, M. J. (2011). Nse1-dependent recruitment of Smc5/6 to lesion-containing loci contributes to the repair defects of mutant complexes. Mol. Biol. Cell 22, 4669-4682.
55. Thorslund, T. and West, S. C. (2007). BRCA2: a universal recombinase regulator. Oncogene 26, 7720-7730.
56. Uemura, T., Ohkura, H., Adachi, Y., Morino, K., Shiozaki, K. and Yanagida, M. (1987). DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50, 917-925.
57. van Veelen, L. R., Essers, J., van de Rakt, M. W., Odijk, H., Pastink, A., Zdzienicka, M. Z., Paulusma, C. C. and Kanaar, R. (2005). Ionizing radiation-induced foci formation of mammalian Rad51 and Rad54 depends on the Rad51 paralogs, but not on Rad52. Mutat. Res. 574, 34-49.
58. Vanoli, F., Fumasoni, M., Szakal, B., Maloisel, L. and Branzei, D. (2010). Replication and recombination factors contributing to recombination-dependent bypass of DNA lesions by template switch. PLoS Genet. 6, e1001205.
59. Veaute, X., Jeusset, J., Soustelle, C., Kowalczykowski, S. C., Le Cam, E. and Fabre, F. (2003). The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423, 309-312.
60. Verkade, H. M., Bugg, S. J., Lindsay, H. D., Carr, A. M. and O'Connell, M. J. (1999). Rad18 is required for DNA repair and checkpoint responses in fission yeast. Mol. Biol. Cell 10, 2905-2918.
61. Verkade, H. M., Teli, T., Laursen, L. V., Murray, J. M. and O'Connell, M. J. (2001). A homologue of the Rad18 postreplication repair gene is required for DNA damage responses throughout the fission yeast cell cycle. Mol. Genet. Genomics 265, 993-1003.
62. Walworth, N. C. and Bernards, R. (1996). rad-dependent response of the chk1-encoded protein kinase at the DNA damage checkpoint. Science 271, 353-356.
63. Williams, J. S., Williams, R. S., Dovey, C. L., Guenther, G., Tainer, J. A. and Russell, P. (2010). gammaH2A binds Brc1 to maintain genome integrity during S-phase. EMBO J. 29, 1136-1148.
64. Xu, Y. J., Davenport, M. and Kelly, T. J. (2006). Two-stage mechanism for activation of the DNA replication checkpoint kinase Cds1 in fission yeast. Genes Dev. 20,990-1003.