Migrating bubble during break-induced replication drives conservative DNA synthesis

Nature

Volumn 502, Issue 7471, 2013, Pages 389-392

  Saini, Natalie ^a   Ramakrishnan, Sreejith ^b   Elango, Rajula ^b   Ayyar, Sandeep ^b   Zhang, Yu ^a   Deem, Angela ^b,c   Ira, Grzegorz ^c   Haber, James E ^d   Lobachev, Kirill S ^a   Malkova, Anna ^b,e  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b Biology SL332   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HELICASE; PIF1 PROTEIN; UNCLASSIFIED DRUG;

CARCINOGEN; CHROMOSOME; ENZYME ACTIVITY; EUKARYOTE; GENOME; HETEROZYGOSITY; MITOCHONDRIAL DNA; MUTATION;

ARTICLE; BREAK INDUCED REPLICATION; BUDDING; CELL CYCLE S PHASE; DNA REPLICATION; DNA STRAND BREAKAGE; DNA SYNTHESIS; FRAMESHIFT MUTATION; HUMAN; INHERITANCE; NONHUMAN; PRIORITY JOURNAL;

CHROMOSOME BREAKAGE; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; GENOMIC INSTABILITY; MUTAGENESIS; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCETALES;

EID: 84885843906     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12584     Document Type: Article

References (38)

1. Smith, C. E., Llorente, B. & Symington, L. S. Template switching during breakinduced replication. Nature 447, 102-105 (2007).
2. Deem, A. et al. Defective break-induced replication leads to half-crossovers in Saccharomyces cerevisiae. Genetics 179, 1845-1860 (2008).
3. Malkova, A. & Haber, J. E. Mutations arising during repair of chromosome breaks. Annu. Rev. Genet. 46, 455-473 (2012).
4. Malkova, A., Naylor, M. L., Yamaguchi, M., Ira, G. & Haber, J. E. RAD51- dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol. Cell. Biol. 25, 933-944 (2005).
5. Davis, A. P. & Symington, L. S. RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol. 24, 2344-2351 (2004).
6. Bosco, G. & Haber, J. E. Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 150, 1037-1047 (1998).
7. Hastings, P. J., Ira, G. & Lupski, J. R. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet. 5, e1000327 (2009).
8. Payen, C., Koszul, R., Dujon, B. & Fischer, G. Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms. PLoS Genet. 4, e1000175 (2008).
9. Deem, A. et al. Break-induced replication is highly inaccurate. PLoS Biol. 9, e1000594 (2011).
10. 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).
11. Lydeard, J. R. et al. Break-induced replication requires all essentialDNA replication factors except those specific for pre-RC assembly. Genes Dev. 24, 1133-1144 (2010).
12. Llorente, B., Smith, C. E. & Symington, L. S. Break-induced replication: what is it and what is it for? Cell Cycle 7, 859-864 (2008).
13. Malkova, A. & Ira, G. Break-induced replication: functions and molecular mechanism. Curr. Opin. Genet. Dev., (2013).
14. Viggiani, C. J. & Aparicio, O. M. New vectors for simplified construction of BrdUIncorporating strains of Saccharomyces cerevisiae. Yeast 23, 1045-1051 (2006).
15. 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).
16. VanHulle, K. et al. Inverted DNA repeats channel repair of distant double-strand breaks into chromatid fusions and chromosomal rearrangements. Mol. Cell. Biol. 27, 2601-2614 (2007).
17. Fangman, W. L. & Brewer, B. J. Activation of replication origins within yeast chromosomes. Annu. Rev. Cell Biol. 7, 375-402 (1991).
18. Formosa, T. & Alberts, B. M. DNA synthesis dependent on genetic recombination: characterizationof a reaction catalyzed bypurified bacteriophage T4proteins. Cell 47, 793-806 (1986).
19. 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).
20. Yang, Y., Sterling, J., Storici, F., Resnick, M. A. & Gordenin, D. A. Hypermutability of damaged single-strand DNA formed at double-strand breaks and uncapped telomeres in yeast Saccharomyces cerevisiae. PLoS Genet. 4, e1000264 (2008).
21. Yang, Y., Gordenin, D. A. & Resnick, M. A. A single-strand specific lesion drives MMS-induced hyper-mutability at a double-strand break in yeast. DNA Repair 9, 914-921 (2010).
22. Roberts, S. A. et al. Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol. Cell 46, 424-435 (2012).
23. Shcherbakova, P. V. & Pavlov, Y. I. 39R59 exonucleases ofDNApolymerases e and d correct base analog induced DNA replication errors on opposite DNA strands in Saccharomyces cerevisiae. Genetics 142, 717-726 (1996).
24. 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).
25. Wilson, M. A. et al. Pif1 helicase and Pold promote recombination-coupled DNA synthesis via bubble migration. Nature http://dx.doi.org/10.1038/ nature12585 (this issue).
26. Hashimoto, Y. & Costanzo, V. Studying DNA replication fork stability in Xenopus egg extract. Methods Mol. Biol. 745, 437-445 (2011).
27. Pohjoismaki, J. L. & Goffart, S. Of circles, forks and humanity: Topological organisation and replication of mammalian mitochondrial DNA. BioEssays 33, 290-299 (2011).
28. Le, S., Moore, J. K., Haber, J. E. & Greider, C. W. RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 152, 143-152 (1999).
29. Kreuzer, K. N., Saunders, M., Weislo, L. J. & Kreuzer, H. W. Recombinationdependent DNA replication stimulated by double-strand breaks in bacteriophage T4. J. Bacteriol. 177, 6844-6853 (1995).
30. Kuzminov, A. Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16, 373-384 (1995).
31. Halazonetis, T. D., Gorgoulis, V. G. & Bartek, J. An oncogene-induced DNA damage model for cancer development. Science 319, 1352-1355 (2008).
32. Wach, A., Brachat, A., Pohlmann, R. & Philippsen, P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808 (1994).
33. Guthrie, C. & Fink, G. Guide to Yeast Genetics and Molecular Biology (Academic Press, 1991).
34. Oh, S. D. et al. Stabilization and electrophoretic analysis of meiotic recombination intermediates in Saccharomyces cerevisiae. Methods Mol. Biol. 557, 209-234 (2009).
35. Friedman, K. L. & Brewer, B. J. Analysis of replication intermediates by twodimensional agarose gel electrophoresis. Methods Enzymol. 262, 613-627 (1995).
36. Goldstein, A. L. & McCusker, J. H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553 (1999).
37. Conti, C., Caburet, S., Schurra, C. & Bensimon, A.Molecular combing. Curr. Protoc. Cytom. Ch. 8, Unit 8 10 http://dx.doi.org/10.1002/0471142956. cy0810s16 (2001).
38. Mann, H. & Whitney, D. On a test of whether one of 2 random variables is stochastically larger than the other. Ann. Math. Stat. 18, 50-60 (1947).