Break-induced loss of heterozygosity in fission yeast: Dual roles for homologous recombination in promoting translocations and preventing de novo telomere addition

Molecular and Cellular Biology

Volumn 27, Issue 21, 2007, Pages 7745-7757

  Cullen, Jason K ^a   Hussey, Sharon P ^a   Walker, Carol ^a   Prudden, John ^a   Wee, Boon Yu ^a   Davé, Anoushka ^a   Findlay, James S ^a   Savory, Andrew P ^a   Humphrey, Timothy C ^a  

^a MRC Radiation   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; ENDONUCLEASE;

ARTICLE; CARCINOGENESIS; CHROMOSOME ARM; CROSSING OVER; DNA STRAND BREAKAGE; ENZYME ACTIVE SITE; GENE LOCUS; GENE OVEREXPRESSION; HETEROZYGOSITY LOSS; HOMOLOGOUS RECOMBINATION; MARKER GENE; MINICHROMOSOME; MUS81 GENE; MUTANT; NBS1 GENE; NONHUMAN; PRIORITY JOURNAL; RAD22 GENE; RAD32 GENE; RAD50 GENE; RHP51 GENE; RHP54 GENE; RHP55 GENE; SCHIZOSACCHAROMYCES POMBE; TELOMERE; YEAST;

ALLELES; BASE SEQUENCE; CHROMOSOMES, FUNGAL; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; GENETIC MARKERS; LOSS OF HETEROZYGOSITY; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MUTATION; PHYLOGENY; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TELOMERE; TRANSLOCATION, GENETIC;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 35748954645     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00462-07     Document Type: Article

References (68)

1. Boddy, M. N., P. H. Gaillard, W. H. McDonald, P. Shanahan, J. R. Yates III, and P. Russell. 2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:537-548.
2. Bosco, G., and J. E. Haber. 1998. Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 150:1037-1047.
3. Bressan, D. A., B. K. Baxter, and J. H. Petrini. 1999. The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:7681-7687.
4. Chahwan, C., T. M. Nakamura, S. Sivakumar, P. Russell, and N. Rhind. 2003. The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol. Cell. Biol. 23:6564-6573.
5. Cromie, G. A., R. W. Hyppa, A. F. Taylor, K. Zakharyevich, N. Hunter, and G. R. Smith. 2006. Single Holliday junctions are intermediates of meiotic recombination. Cell 127:1167-1178.
6. Davis, A. P., and L. S. Symington. 2004. RAD51-depcndent break-induced replication in yeast. Mol. Cell. Biol. 24:2344-2351.
7. Diede, S. J., and D. E. Gottschling. 2001. Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr. Biol. 11:1336-1340.
8. Diede, S. J., and D. E. Gottschling. 1999. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 99:723-733.
9. Doe, C. L., F. Osman, J. Dixon, and M. C. Whitby. 2004. DNA repair by a Rad22-Mus81-dependent pathway that is independent of Rhp51. Nucleic Acids Res. 32:5570-5581.
10. Gaillard, P. H., E. Noguchi, P. Shanahan, and P. Russell. 2003. The endogenous Mus81-Eme1 complex resolves Holliday junctions by a nick and counternick mechanism. Mol. Cell 12:747-759.
11. Hollingsworth, N. M., and S. J. Brill. 2004. The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev. 18:117-125.
12. Ivanov, E. L., N. Sugawara, C. I. White, F. Fabre, and J. E. Haber. 1994. Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14:3414-3425.
13. Jasin, M. 2000. LOH and mitotic recombination, p. 191-209. In M. Ehrlich (ed.), DNA alterations in cancer. Eaton Publishing, Natick, MA.
14. Kadyk, L. C., and L. H. Hartwell. 1992. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132:387-402.
15. Khanna, K. K., and S. P. Jackson. 2001. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27:247-254.
16. Kinzler, K., and B. Vogelstein. 1997. Introduction to cancer genetics. In C. R. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle (ed.), The metabolic and molecular bases of inherited disease, 7th ed. McGraw-Hill, New York.
17. Knudson, A. G. 1993. Antioncogenes and human cancer. Proc. Natl. Acad. Sci. USA 90:10914-10921.
18. Kramer, K. M., and J. E. Haber. 1993. New telomeres in yeast are initiated with a highly selected subset of TG1-3 repeats. Genes Dev. 7:2345-2356.
19. Krogh, B. O., and L. S. Symington. 2004. Recombination proteins in yeast. Annu. Rev. Genet. 38:233-271.
20. Lasko, D., W. Cavenee, and M. Nordenskjold. 1991. Loss of constitutional heterozygosity in human cancer. Annu. Rev. Genet. 25:281-314.
21. Lee, M. S., R. C. Gallagher, J. Bradley, and E. H. Blackburn. 1993. In vivo and in vitro studies of telomeres and telomerase. Cold Spring Harbor Symp. Quant. Biol. 58:707-718.
22. 2/M arrest after DNA damage. Cell 94:399-409.
23. Leupold, U., and H. Gutz. 1964. Genetic fine structure in Schizosaccharomyces pombe. Proc. XIth Intl. Congr. Genet. 2:31-35.
24. Lewis, L. K., and M. A. Resnick. 2000. Tying up loose ends: non-homologous end-joining in Saccharomyces cerevisiae. Mutat. Res. 451:71-89.
25. Llorente, B., and L. S. Symington. 2004. The Mre11 nuclease is not required for 5′ to 3′ resection at multiple HO-induced double-strand breaks. Mol. Cell. Biol. 24:9682-9694.
26. Malkova, A., E. L. Ivanov, and J. E. Haber. 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.
27. Malkova, A., M. L. Naylor, M. Yamaguchi, G. Ira, and J. E. Haber. 2005. RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol. Cell. Biol. 25:933-944.
28. Mangahas, J. L., M. K. Alexander, L. L. Sandell, and V. A. Zakian. 2001. Repair of chromosome ends after telomere loss in Saccharomyces. Mol. Biol. Cell 12:4078-4089.
29. Matsumoto, T., K. Fukui, O. Niwa, N. Sugawara, J. W. Szostak, and M. Yanagida. 1987. Identification of healed terminal DNA fragments in linear minichromosomes of Schizosaccharomyces pombe. Mol. Cell. Biol. 7:4424-4430.
30. Mazin, A. V., A. A. Alexeev, and S. C. Kowalczykowski. 2003. A novel function of Rad54 protein. Stabilization of the Rad51 nucleoprotein filament. J. Biol. Chem. 278:14029-14036.
31. McClintock, B. 1941. The stability of broken ends of chromosomes of Zea mays. Genetics 23:234-282.
32. McEachern, M. J., and J. E. Haber. 2006. Break-induced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem. 75:111-135.
33. Moore, J. K., and J. E. Haber. 1996. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:2164-2173.
34. Moreau, S., J. R. Ferguson, and L. S. Symington. 1999. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19:556-566.
35. Morrow, D. M., C. Connelly, and P. Hieter. 1997. "Break copy" duplication: a model for chromosome fragment formation in Saccharomyces cerevisiae. Genetics 147:371-382.
36. Moynahan, M. E., and M. Jasin. 1997. Loss of heterozygosity induced by a chromosomal double-strand break. Proc. Natl. Acad. Sci. USA 94:8988-8993.
37. Muris, D. F., K. Vreeken, A. M. Carr, B. C. Broughton, A. R. Lehmann, P. H. Lohman, and A. Pastink. 1993. Cloning the RAD51 homologue of Schizosaccharomyces pombe. Nucleic Acids Res. 21:4586-4591.
38. Myung, K., C. Chen, and R. D. Kolodner. 2001. Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411:1073-1076.
39. Niwa, O., T. Matsumoto, and M. Yanagida. 1986. Construction of a minichromosome by deletion and its mitotic and meiotic behaviour in fission yeast. Mol. Gen. Genet. 203:397-405.
40. Osman, F., J. Dixon, C. L. Doe, and M. C. Whitby. 2003. Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol. Cell 12:761-774.
41. Paques, F., and J. E. Haber. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. MoI. Biol. Rev. 63:349-404.
42. Pastink, A., J. C. Eeken, and P. H. Lohman. 2001. Genomic integrity and the repair of double-strand DNA breaks. Mutat. Res. 480-481:37-50.
43. Pennaneach, V., C. D. Putnam, and R. D. Kolodner. 2006. Chromosome healing by de novo telomere addition in Saccharomyces cerevisiae. Mol. Microbiol. 59:1357-1368.
44. Petukhova, G., S. Stratton, and P. Sung. 1998. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393:91-94.
45. Prudden, J., J. S. Evans, S. P. Hussey, B. Deans, P. O'Neill, J. Thacker, and T. Humphrey. 2003. Pathway utilization in response to a site-specific DNA double-strand break in fission yeast. EMBO J. 22:1419-1430.
46. Putnam, C. D., V. Pennaneach, and R. D. Kolodner. 2004. Chromosome healing through terminal deletions generated by de novo telomere additions in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101:13262- 13267.
47. Schulz, V. P., and V. A. Zakian. 1994. The Saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 76:145-155.
48. Signon, L., A. Malkova, M. L. Naylor, H. Klein, and J. E. Haber. 2001. Genetic requirements for RAD51- and RAD54-indcpendent break-induced replication repair of a chromosomal double-strand break. Mol. Cell. Biol. 21:2048-2056.
49. Smith, S., A. Gupta, R. D. Kolodner, and K. Myung. 2005. Suppression of gross chromosomal rearrangements by the multiple functions of the Mre11-Rad50-Xrs2 complex in Saccharomyces cerevisiae. DNA Repair 4:606-617.
50. Stark, J. M., and M. Jasin. 2003. Extensive loss of heterozygosity is suppressed during homologous repair of chromosomal breaks. Mol. Cell. Biol. 23:733-743.
51. Stellwagen, A. E., Z. W. Haimberger, J. R. Veatch, and D. E. Gottschling. 2003. Ku interacts with telomerase RNA to promote telomere addition at native and broken chromosome ends. Genes Dev. 17:2384-2395.
52. +, a fission yeast gene related to the Bloom's and Werner's syndrome genes, is required for reversible S phase arrest. EMBO J. 16:2682-2692.
53. Sugawara, N., X. Wang, and J. E. Haber. 2003. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediatcd recombination. Mol. Cell 12:209-219.
54. Sugiyama, T., J. H. New, and S. C. Kowalczykowski. 1998. DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc. Natl. Acad. Sci. USA 95:6049-6054.
55. Suguwara, N. F. 1988. DNA sequences at the telomeres of the fission yeast S. pombe. Ph.D. thesis. Harvard University, Cambridge, MA.
56. Sung, P. 1997. Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem. 272:28194-28197.
57. Sung, P. 1997. 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.
58. Tomita, K., A. Matsuura, T. Caspari, A. M. Carr, Y. Akamatsu, H. Iwasaki, K. Mizuno, K. Ohta, M. Uritani, T. Ushimaru, K. Yoshinaga, and M. Ueno. 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.
59. Trujillo, K. M., and P. Sung. 2001. DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50*Mre11 complex. J. Biol. Chem. 276: 35458-35464.
60. Tsubouchi, H., and H. Ogawa. 1998. A novel Mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol. Cell. Biol. 18:260-268.
61. + gene involved in DNA repair and telomere maintenance. Mol. Cell. Biol. 23:6553-6563.
62. Usui, T., T. Ohta, H. Oshiumi, J. Tomizawa, H. Ogawa, and T. Ogawa. 1998. Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95:705-716.
63. Varga, T., and P. D. Aplan. 2005. Chromosomal aberrations induced by double strand DNA breaks. DNA Repair 4:1038-1046.
64. Verdun, R. E., and J. Karlseder. 2006. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127:709-720.
65. Wang, X., and J. E. Haber. 2004. Role of Saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. PLoS Biol. 2:e21.
66. Weterings, E., and D. C. van Gent. 2004. The mechanism of non-homologous end-joining: a synopsis of synapsis. DNA Repair 3:1425-1435.
67. Wilkie, A. O., J. Lamb, P. C. Harris, R. D. Finney, and D. R. Higgs. 1990. A truncated human chromosome 16 associated with alpha thalassaemia is stabilized by addition of telomeric repeat (TTAGGG)n. Nature 346:868-871.
68. Wong, A. C., Y. Ning, J. Flint, K. Clark, J. P. Dumanski, D. H. Ledbetter, and H. E. McDermid. 1997. Molecular characterization of a 130-kb terminal microdeletion at 22q in a child with mild mental retardation. Am. J. Hum. Genet. 60:113-120.