Failed gene conversion leads to extensive end processing and chromosomal rearrangements in fission yeast

EMBO Journal

Volumn 28, Issue 21, 2009, Pages 3400-3412

  Tinline Purvis, Helen ^a   Savory, Andrew P ^a   Cullen, Jason K ^a   Davé, Anoushka ^a   Moss, Jennifer ^a   Bridge, Wendy L ^a   Marguerat, Samuel ^b   Bähler, Jürg ^b   Ragoussis, Jiannis ^c   Mott, Richard ^c   A Walker, Carol ^a   Humphrey, Timothy C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Break induced replication; Copy number variation; DSB; Homologous recombination; Isochromosome

Indexed keywords

ARTICLE; CENTROMERE; CHROMOSOME ARM; CHROMOSOME LOSS; CHROMOSOME REARRANGEMENT; DNA STRAND BREAKAGE; GENE CONVERSION; GENE LOCUS; GENETIC SCREENING; HETEROZYGOSITY LOSS; HOMOLOGOUS RECOMBINATION; ISOCHROMOSOME; MINICHROMOSOME; NONHUMAN; PRIORITY JOURNAL; YEAST;

ADENOSINE TRIPHOSPHATASES; CENTROMERE; CHROMOSOMES, FUNGAL; DNA BREAKS, DOUBLE-STRANDED; DNA-BINDING PROTEINS; GENE CONVERSION; LOSS OF HETEROZYGOSITY; RAD51 RECOMBINASE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SCHIZOSACCHAROMYCETACEAE;

EID: 70350780181     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.265     Document Type: Article

References (66)

1. Allshire R (2004) Centromere and kinetochore structure and function. In The molecular biology of Schizosaccharomyces pombe, Egel R (ed), Vol.10, pp 150-169. Heidelberg: Springer-Verlag
2. Andersen MK, Pedersen-Bjergaard J (2000) Increased frequency of dicentric chromosomes in therapy-related MDS and AML compared to de novo disease is significantly related to previous treatment with alkylating agents and suggests a specific susceptibility to chromosome breakage at the centromere. Leukemia 14: 105-111
3. Atkin NB, Baker MC (1982) Specific chromosome change, i(12p), in testicular tumours? Lancet 2: 1349
4. Bartsch S, Kang LE, Symington LS (2000) RAD51 is required for the repair of plasmid double-stranded DNA gaps from either plasmid or chromosomal templates. Mol Cell Biol 20: 1194-1205
5. Bosco G, Haber JE (1998) Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 150: 1037-1047
6. Christ N, Moynahan M, Jasin M (2007) BRCA2: safeguarding the genome through homologous recombination. In Molecular genetics of recombination, Aguilera A, Rothstein R (eds), pp 363-380. Berlin-Heidelberg: Springer-Verlag
7. Clerici M, Mantiero D, Lucchini G, Longhese MP (2005) The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J Biol Chem 280: 38631-38638
8. Cullen JK, Hussey SP, Walker C, Prudden J, Wee BY, Dave A, Findlay JS, Savory AP, Humphrey TC (2007) Break-induced loss of heterozygosity in fission yeast: dual roles for homologous recombination in promoting translocations and preventing de novo telomere addition. Mol Cell Biol 27: 7745-7757
9. Darlington C (1939) Misdivision and the genetics of the centromere. J Genet 37: 341-364
10. Davis AP, Symington LS (2004) RAD51-dependent break-induced replication in yeast. Mol Cell Biol 24: 2344-2351
11. Deem AK, Barker K, Vanhulle K, Downing BD, Vayl A, Malkova A (2008) Defective break-induced replication leads to half-crossovers in Saccharomyces cerevisiae. Genetics 179: 1845-1860
12. Gravel S, Chapman JR, Magill C, Jackson SP (2008) DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev 22: 2767-2772
13. Haber JE (2006) Transpositions and translocations induced by site-specific double-strand breaks in budding yeast. DNA Repair (Amst) 5: 998-1009
14. Heichinger C, Penkett CJ, Bahler J, Nurse P (2006) Genome-wide characterization of fission yeast DNA replication origins. EMBO J 25: 5171-5179
15. Hope JC, Mense SM, Jalakas M, Mitsumoto J, Freyer GA (2006) Rqh1 blocks recombination between sister chromatids during double strand break repair, independent of its helicase activity. Proc Natl Acad Sci USA 103: 5875-5880
16. Huertas P, Cortes-Ledesma F, Sartori AA, Aguilera A, Jackson SP (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455: 689-692
17. Jasin M (2000) LOH and mitotic recombination. In DNA alterations in Cancer, Ehrlich M (ed), pp 191-209.
18. Natick, MA, USA: Eaton Publishing Knudson AG (1993) Antioncogenes and human cancer. Proc Natl Acad Sci USA 90: 10914-10921
19. Krogh BO, Symington LS (2004) Recombination proteins in yeast. Annu Rev Genet 38: 233-271
20. Lasko D, Cavenee W, Nordenskjold M (1991) Loss of constitutional heterozygosity in human cancer. Annu Rev Genet 25: 281-314
21. Li H, Ruan J, Durbin R (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18: 1851-1858
22. Limbo O, Chahwan C, Yamada Y, de Bruin RA, Wittenberg C, Russell P (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
23. Llorente B, Smith CE, Symington LS (2008) Break-induced replication: what is it and what is it for? Cell Cycle 7: 859-864
24. Llorente B, Symington LS (2004) The Mre11 nuclease is not required for 50-30 resection at multiple HO-induced double-strand breaks. Mol Cell Biol 24: 9682-9694
25. Lobachev KS, Gordenin DA, Resnick MA (2002) The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108: 183-193
26. Lorda-Sanchez I, Binkert F, Maechler M, Schinzel A (1991) A molecular study of X isochromosomes: parental origin, centro-meric structure, and mechanisms of formation. Am J Hum Genet 49: 1034-1040
27. Lydeard JR, Jain S, Yamaguchi M, Haber JE (2007) Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448: 820-823
28. Lyne R, Burns G, Mata J, Penkett CJ, Rustici G, Chen D, Langford C, Vetrie D, Bahler J (2003) Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 4: 27
29. Malkova A, Ivanov EL, Haber JE (1996) Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc Natl Acad Sci USA 93: 7131-7136
30. Malkova A, Naylor ML, Yamaguchi M, Ira G, Haber JE (2005) RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol Cell Biol 25: 933-944
31. Manolis KG, Nimmo ER, Hartsuiker E, Carr AM, Jeggo PA, Allshire RC (2001) Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J 20: 210-221
32. Maringele L, Lydall D (2004) Telomerase-and recombination-independent immortalization of budding yeast. Genes Dev 18: 2663-2675
33. Mimitou EP, Symington LS (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455: 770-774
34. Mimitou EP, Symington LS (2009) Nucleases and helicases take center stage in homologous recombination. Trends Biochem Sci 34: 264-272
35. Mitelman F, Johansson B, Mertens F (2008) Mitelman Database of Chromosome Aberrations in Cancer
36. Myung K, Chen C, Kolodner RD (2001) Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cere-visiae. Nature 411: 1073-1076
37. Myung K, Kolodner RD (2003) Induction of genome instability by DNA damage in Saccharomyces cerevisiae. DNA Repair (Amst) 2: 243-258
38. Nakamura K, Okamoto A, Katou Y, Yadani C, Shitanda T, Kaweeteerawat C, Takahashi TS, Itoh T, Shirahige K, Masukata H, Nakagawa T (2008) Rad51 suppresses gross chromosomal rearrangement at centromere in Schizosaccharomyces pombe. EMBO J 27: 3036-3046
39. Niwa O, Matsumoto T, Yanagida M (1986) Construction of a minichromosome by deletion and its mitotic and meiotic behaviour in fission yeast. Mol Gen Genet 203: 397-405
40. Palmer CG, Reichmann A (1976) Chromosomal and clinical findings in 110 females with Turner syndrome. Hum Genet 35: 35-49
41. Paques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349-404
42. Pfeiffer P, Goedecke W, Obe G (2000) Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. Mutagenesis 15: 289-302
43. Phelan MC, Prouty LA, Stevenson RE, Howard-Peebles PN, Page DC, Schwartz CE (1988) The parental origin and mechanism of formation of three dicentric X chromosomes. Hum Genet 80: 81-84
44. Pidoux AL, Allshire RC (2004) Kinetochore and heterochromatin domains of the fission yeast centromere. Chromosome Res 12: 521-534
45. Pohl TJ, Nickoloff JA (2008) Rad51-independent interchromosomal double-strand break repair by gene conversion requires Rad52 but not Rad55, Rad57, or Dmc1. Mol Cell Biol 28: 897-906
46. Prudden J, Evans JS, Hussey SP, Deans B, O'Neill P, Thacker J, Humphrey T (2003) Pathway utilization in response to a site-specific DNA double-strand break in fission yeast. EMBO J 22: 1419-1430
47. Putnam CD, Pennaneach V, Kolodner RD (2005) Saccharomyces cerevisiae as a model system to define the chromosomal instability phenotype. Mol Cell Biol 25: 7226-7238
48. Reynolds JF, Daniel A, Kelly TE, Gollin SM, Stephan MJ, Carey J, Adkins WN, Webb MJ, Char F, Jimenez JF, Opitz JM (1987) Isochromosome 12p mosaicism (Pallister mosaic aneuploidy or Pallister-Killian syndrome): report of 11 cases. Am J Med Genet 27: 257-274
49. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP (2007) Human CtIP promotes DNA end resection. Nature 450: 509-514
50. Selmecki A, Gerami-Nejad M, Paulson C, Forche A, Berman J (2008) An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol Microbiol 68: 624-641
51. Shrivastav M, De Haro LP, Nickoloff JA (2008) Regulation of DNA double-strand break repair pathway choice. Cell Res 18: 134-147
52. Smith CE, Llorente B, Symington LS (2007) Template switching during break-induced replication. Nature 447: 102-105
53. Sugawara N, Wang X, Haber JE (2003) In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol Cell 12: 209-219
54. Sung P (1997a) Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J Biol Chem 272: 28194-28197
55. Sung P (1997b) Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev 11: 1111-1121
56. Suto K, Nagata A, Murakami H, Okayama H (1999) A double-strand break repair component is essential for S phase completion in fission yeast cell cycling. Mol Biol Cell 10: 3331-3343
57. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand-break repair model for recombination. Cell 33: 25-35
58. Tanaka H, Ryu GH, Seo YS, MacNeill SA (2004) Genetics of lagging strand DNA synthesis and maturation in fission yeast: suppression analysis links the Dna2-Cdc24 complex to DNA polymerase delta. Nucleic Acids Res 32: 6367-6377
59. Therman E, Sarto GE, Patau K (1974) Apparently isodicentric but functionally monocentric X chromosome in man. Am J Hum Genet 26: 83-92
60. Tomita K, Matsuura A, Caspari T, Carr AM, Akamatsu Y, Iwasaki H, Mizuno K, Ohta K, Uritani M, Ushimaru T, Yoshinaga K, Ueno M (2003) Competition between the Rad50 complex and the Ku heterodimer reveals a role for Exo1 in processing double-strand breaks but not telomeres. Mol Cell Biol 23: 5186-5197
61. Tsubouchi H, Ogawa H (2000) Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevi-siae. Mol Biol Cell 11: 2221-2233
62. van den Bosch M, Vreeken K, Zonneveld JB, Brandsma JA, Lombaerts M, Murray JM, Lohman PH, Pastink A (2001) Characterization of RAD52 homologs in the fission yeast Schizosaccharomyces pombe. Mutat Res 461: 311-323
63. VanHulle K, Lemoine FJ, Narayanan V, Downing B, Hull K, McCullough C, Bellinger M, Lobachev K, Petes TD, Malkova A (2007) Inverted DNA repeats channel repair of distant double-strand breaks into chromatid fusions and chromosomal rearrangements. Mol Cell Biol 27: 2601-2614
64. Wolner B, van Komen S, Sung P, Peterson CL (2003) Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol Cell 12: 221-232 (Pubitemid 36957837)
65. Yeh E, Haase J, Paliulis LV, Joglekar A, Bond L, Bouck D, Salmon ED, Bloom KS (2008) Pericentric chromatin is organized into an intramolecular loop in mitosis. Curr Biol 18: 81-90
66. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134: 981-994