DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2

Nature

Volumn 467, Issue 7311, 2010, Pages 112-116

  Cejka, Petr ^a   Cannavo, Elda ^a   Polaczek, Piotr ^b   Masuda Sasa, Taro ^b   Pokharel, Subhash ^b   Campbell, Judith L ^b   Kowalczykowski, Stephen C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA TOPOISOMERASE; DNA TOPOISOMERASE 3; DNA2; DOUBLE STRANDED DNA; HELICASE; MRE11 PROTEIN; RAD50 PROTEIN; REPLICATION FACTOR A; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG; DEOXYRIBONUCLEASE; DNA BINDING PROTEIN; DNA HELICASE; DNA2 PROTEIN, S CEREVISIAE; EXODEOXYRIBONUCLEASE; MRE11 PROTEIN, S CEREVISIAE; RAD50 PROTEIN, S CEREVISIAE; RECQ HELICASE; RFA1 PROTEIN, S CEREVISIAE; RMI1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SGS1 PROTEIN, S CEREVISIAE; TOP3 PROTEIN, S CEREVISIAE; XRS2 PROTEIN, S CEREVISIAE;

DNA; ENZYME ACTIVITY; EUKARYOTE; EXPERIMENTAL STUDY; GENETIC ANALYSIS; PROTEIN; RECOMBINATION; RNA;

ARTICLE; DNA DEGRADATION; DNA DENATURATION; DNA END RESECTION; DNA REPAIR; HUMAN; IN VITRO STUDY; PRIORITY JOURNAL; PROTECTION; STIMULATION; METABOLISM; SACCHAROMYCES CEREVISIAE;

DEOXYRIBONUCLEASES; DNA HELICASES; DNA REPAIR; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; RECQ HELICASES; REPLICATION PROTEIN A; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 77956325620     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09355     Document Type: Article

References (32)

1. Krogh, B. O. & Symington, L. S. Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271 (2004).
2. Mimitou, E. P. & Symington, L. S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770-774 (2008).
3. Gravel, S., Chapman, J. R., Magill, C. & Jackson, S. P. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22, 2767-2772 (2008).
4. Zhu, Z., Chung, W. H., Shim, E. Y., Lee, S. E. & Ira, G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134, 981-994 (2008).
5. Gangloff, S., McDonald, J. P., Bendixen, C., Arthur, L. & Rothstein, R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: A potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14, 8391-8398 (1994).
6. Chiolo, I. et al. Srs2 and Sgs1 DNA helicases associate with Mre11 in different subcomplexes following checkpoint activation and CDK1-mediated Srs2 phosphorylation. Mol. Cell. Biol. 25, 5738-5751 (2005).
7. Szankasi, P. & Smith, G. R. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267, 1166-1169 (1995).
8. Budd, M. E., Choe, W. C. & Campbell, J. L. DNA2 encodes a DNA helicase essential for replication of eukaryotic chromosomes. J. Biol. Chem. 270, 26766-26769 (1995).
9. Budd, M. E., Choe, W. & Campbell, J. L. The nuclease activity of the yeast DNA2 protein, which is related to the RecB-like nucleases, is essential in vivo. J. Biol. Chem. 275, 16518-16529 (2000).
10. Llorente, B. & Symington, L. S. The Mre11 nuclease is not required for 59 to 39 resection at multiple HO-induced double-strand breaks. Mol. Cell. Biol. 24, 9682-9694 (2004).
11. Budd, M. E. & Campbell, J. L. Interplay of Mre11 nuclease with Dna2 plus Sgs1 in Rad51-dependent recombinational repair. PLoS ONE 4, e4267 (2009).
12. Cejka, P. & Kowalczykowski, S. C. The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds Holliday junctions. J. Biol. Chem. 285, 8290-8301 (2010).
13. Cobb, J. A., Bjergbaek, L., Shimada, K., Frei, C. & Gasser, S. M. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22, 4325-4336 (2003).
14. Bae, S. H. & Seo, Y. S. Characterization of the enzymatic properties of the yeast Dna2 helicase/endonuclease suggests a new model for Okazaki fragment processing. J. Biol. Chem. 275, 38022-38031 (2000).
15. Masuda-Sasa, T., Polaczek, P., Peng, X. P., Chen, L. & Campbell, J. L. Processing of G4 DNA by Dna2 helicase/nuclease and replication protein A (RPA) provides insights into the mechanism of Dna2/RPA substrate recognition. J. Biol. Chem. 283, 24359-24373 (2008).
16. Zierhut, C. & Diffley, J. F. Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J. 27, 1875-1885 (2008).
17. Li, X., Stith, C. M., Burgers, P. M. & Heyer, W. D. PCNA is required for initiation of recombination-associated DNA synthesis by DNA polymerase delta. Mol. Cell 36, 704-713 (2009).
18. Kao, H. I., Veeraraghavan, J., Polaczek, P., Campbell, J. L. & Bambara, R. A. On the roles of Saccharomyces cerevisiae Dna2p and Flap endonuclease 1 in Okazaki fragment processing. J. Biol. Chem. 279, 15014-15024 (2004).
19. Bae, S. H., Bae, K. H., Kim, J. A. & Seo, Y. S. RPA governs endonuclease switching during processing of Okazaki fragments in eukaryotes. Nature 412, 456-461 (2001).
20. Bae, K. H. et al. Bimodal interaction between replication-protein A and Dna2 is critical for Dna2 function both in vivo and in vitro. Nucleic Acids Res. 31, 3006-3015 (2003).
21. Mullen, J. R., Nallaseth, F. S., Lan, Y. Q., Slagle, C. E. & Brill, S. J. Yeast Rmi1/Nce4 controls genome stability as a subunit of the Sgs1-Top3 complex. Mol. Cell. Biol. 25, 4476-4487 (2005).
22. Chang, M. et al. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO J. 24, 2024-2033 (2005).
23. Stracker, T. H., Theunissen, J. W., Morales, M. & Petrini, J. H. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair 3, 845-854 (2004).
24. Neale, M. J., Pan, J. & Keeney, S. Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436, 1053-1057 (2005).
25. Hartsuiker, E., Neale, M. J. & Carr, A. M. Distinct requirements for the Rad32(Mre11) nuclease and Ctp1(CtIP) in the removal of covalently bound topoisomerase I and II from DNA. Mol. Cell 33, 117-123 (2009).
26. Niu, H. et al. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature doi:10.1038/nature09318 (this issue).
27. Dillingham, M. S. & Kowalczykowski, S. C. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 72, 642-671 (2008).
28. Anderson, D. G. & Kowalczykowski, S. C. The translocating RecBCD enzyme stimulates recombination by directing RecA protein onto ssDNA in a x-regulated manner. Cell 90, 77-86 (1997).
29. Wu, L., Davies, S. L., Levitt, N. C. & Hickson, I. D. Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J. Biol. Chem. 276, 19375-19381 (2001).
30. Nimonkar, A. V., Ozsoy, A. Z., Genschel, J., Modrich, P. & Kowalczykowski, S. C. Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc. Natl Acad. Sci. USA 105, 16906-16911 (2008).
31. Handa, N., Morimatsu, K., Lovett, S. T. & Kowalczykowski, S. C. Reconstitution of initial steps of ds DNA break repair by the RecF pathway of E. coli. Genes Dev. 23, 1234-1245 (2009).
32. Cejka, P., Plank, J. L., Bachrati, C. Z., Hickson, I. D. & Kowalczykowski, S. C. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat. Struct. Mol. Biol. (in the press).