Pif1 helicase and Polδ promote recombination-coupled DNA synthesis via bubble migration

Nature

Volumn 502, Issue 7471, 2013, Pages 393-396

  Wilson, Marenda A ^a   Kwon, Youngho ^b   Xu, Yuanyuan ^b   Chung, Woo Hyun ^a,c   Chi, Peter ^d,e   Niu, Hengyao ^b   Mayle, Ryan ^a   Chen, Xuefeng ^a   Malkova, Anna ^f,g   Sung, Patrick ^b   Ira, Grzegorz ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Duksung Women's University   (South Korea)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^f Biology SL332   (United States)

^g E11 SSH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIR PROTEIN; DNA; DNA DIRECTED DNA POLYMERASE DELTA; HELICASE; PIF1 HELICASE; RAD51 PROTEIN; UNCLASSIFIED DRUG; UNCLASSIFIED ENZYME;

CANCER; ENZYME ACTIVITY; MITOCHONDRIAL DNA; POLYMERASE CHAIN REACTION; PROTEIN; RECOMBINATION; TOPOLOGY; YEAST;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA REPAIR; DNA STRUCTURE; DNA SYNTHESIS; FUNGAL STRAIN; HOMOLOGOUS RECOMBINATION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE;

CROSSING OVER, GENETIC; DNA HELICASES; DNA POLYMERASE III; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; NUCLEIC ACID CONFORMATION; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 84885866032     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12585     Document Type: Article

References (38)

1. Maloisel, L., Fabre, F. & Gangloff, S. DNA polymerase d is preferentially recruited during homologous recombination to promote heteroduplex DNA extension. Mol. Cell. Biol. 28, 1373-1382 (2008).
2. Wang, X. et al. Role of DNA replication proteins in double-strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 24, 6891-6899 (2004).
3. Li, X., Stith, C. M., Burgers, P. M. & Heyer, W. D. PCNA is required for initiation of recombination-associated DNA synthesis by DNA polymerase d. Mol. Cell 36, 704-713 (2009).
4. Chung, W. H., Zhu, Z., Papusha, A., Malkova, A. & Ira, G. Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet. 6, e1000948 (2010).
5. Dewar, J. M. & Lydall, D. Pif1- and Exo1-dependent nucleases coordinate checkpoint activation following telomere uncapping. EMBO J. 29, 4020-4034 (2010).
6. Cesare, A. J. & Reddel, R. R. Alternative lengthening of telomeres: models, mechanisms and implications. Nature Rev. Genet. 11, 319-330 (2010).
7. Paeschke, K., Capra, J. A. & Zakian, V. A. DNA replication through G-Quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell 145, 678-691 (2011).
8. Sabouri, N.,McDonald, K. R.,Webb, C. J., Cristea, I. M. & Zakian, V. A.DNAreplication through hard-to-replicate sites, including both highly transcribed RNA Pol II and Pol III genes, requires the S. pombe Pfh1 helicase. Genes Dev. 26, 581-593 (2012).
9. Budd, M. E., Reis, C. C., Smith, S., Myung, K. & Campbell, J. L. Evidence suggesting that Pif1 helicase functions in DNA replication with the Dna2 helicase/nuclease and DNA polymerase d. Mol. Cell. Biol. 26, 2490-2500 (2006).
10. Pike, J. E., Burgers, P. M., Campbell, J. L. & Bambara, R. A. Pif1 helicase lengthens some Okazaki fragment flaps necessitating Dna2 nuclease/helicase action in the two-nuclease processing pathway. J. Biol. Chem. 284, 25170-25180 (2009).
11. Rossi, M. L. et al. Pif1 helicase directs eukaryotic Okazaki fragments toward the two-nuclease cleavage pathway for primer removal. J. Biol. Chem. 283, 27483-27493 (2008).
12. Deem, A. et al. Defective break-induced replication leads to half-crossovers in Saccharomyces cerevisiae. Genetics 179, 1845-1860 (2008).
13. Schulz, V. P. & Zakian, V. A. The saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 76, 145-155 (1994).
14. Lydeard, J. R., Jain, S., Yamaguchi, M. & Haber, J. E. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448, 820-823 (2007).
15. Ho, C. K., Mazon, G., Lam, A. F. & Symington, L. S. Mus81 and Yen1 promote reciprocal exchangeduringmitotic recombination tomaintaingenome integrity in budding yeast. Mol. Cell 40, 988-1000 (2010).
16. Ira, G., Malkova, A., Liberi, G., Foiani, M. & Haber, J. E. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115, 401-411 (2003).
17. Prakash, R. et al. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev. 23, 67-79 (2009).
18. Petukhova, G., Stratton, S. & Sung, P. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393, 91-94 (1998).
19. Van Komen, S., Petukhova, G., Sigurdsson, S. & Sung, P. Functional cross-talk among Rad51, Rad54, and replication protein A in heteroduplex DNA joint formation. J. Biol. Chem. 277, 43578-43587 (2002).
20. Bochman, M. L., Sabouri, N. & Zakian, V. A. Unwinding the functions of the Pif1 family helicases. DNA Repair 9, 237-249 (2010).
21. Sugiyama, T., Zaitseva, E. M. & Kowalczykowski, S. C. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 272, 7940-7945 (1997).
22. Boule, J. B. & Zakian, V. A. The yeast Pif1p DNA helicase preferentially unwinds RNA DNA substrates. Nucleic Acids Res. 35, 5809-5818 (2007).
23. Sebesta, M., Burkovics, P., Haracska, L. & Krejci, L. Reconstitution of DNA repair synthesis in vitro and the role of polymerase and helicase activities. DNA Repair 10, 567-576 (2011).
24. Smith, C. E., Lam, A. F. & Symington, L. S. Aberrant double-strand break repair resulting in half crossovers inmutants defective for Rad51 or theDNApolymerase d complex. Mol. Cell. Biol. 29, 1432-1441 (2009).
25. Burgers, P. M. & Gerik, K. J. Structure and processivity of two forms of Saccharomyces cerevisiae DNA polymerase d. J. Biol. Chem. 273, 19756-19762 (1998).
26. Formosa, T. & Alberts, B. M. DNA synthesis dependent on genetic recombination: characterizationof a reaction catalyzed bypurified bacteriophage T4proteins. Cell 47, 793-806 (1986).
27. Griffith, J. D. & Christiansen, G. Electron microscope visualization of chromatin and other DNA-protein complexes. Annu. Rev. Biophys. Bioeng. 7, 19-35 (1978).
28. Ferguson, D. O. & Holloman, W. K. Recombinational repair of gaps in DNA is asymmetric in Ustilago maydis and can be explained by a migrating D-loopmodel. Proc. Natl Acad. Sci. USA 93, 5419-5424 (1996).
29. Hastings, P. J., Lupski, J. R., Rosenberg, S. M. & Ira, G. Mechanisms of change in gene copy number. Nature Rev. Genet. 10, 551-564 (2009).
30. Malkova, A. & Ira, G. Break-induced replication: functions and molecular mechanism. Curr. Opin. Genet. Dev. 23, 271-279 (2013).
31. Sugawara, N., Wang, X. & Haber, J. E. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12, 209-219 (2003).
32. Janke, R. et al. A truncated DNA-damage-signaling response is activated after DSB formation in the G1 phase of Saccharomyces cerevisiae. Nucleic Acids Res. 38, 2302-2313 (2010).
33. Busygina, V. et al. Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev. 22, 786-795 (2008).
34. 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).
35. Malkova, A., Klein, F., Leung, W. Y. & Haber, J. E. HO endonuclease-induced recombination in yeast meiosis resembles Spo11-induced events. Proc. Natl Acad. Sci. USA 97, 14500-14505 (2000).
36. Acharya, N., Klassen, R., Johnson, R. E., Prakash, L. & Prakash, S. PCNA binding domains in all three subunits of yeast DNA polymerase delta modulate its function in DNA replication. Proc. Natl Acad. Sci. USA 108, 17927-17932 (2011).
37. Van Komen, S., Macris, M., Sehorn, M. G. & Sung, P. Purification and assays of Saccharomyces cerevisiae homologous recombination proteins. Methods Enzymol. 408, 445-463 (2006).
38. Raschle, M., VanKomen,S.,Chi, P., Ellenberger, T. & Sung, P. Multiple interactions with the Rad51 recombinase govern the homologous recombination function of Rad54. J. Biol. Chem. 279, 51973-51980 (2004).