The DNA damage checkpoint allows recombination between divergent DNA sequences in budding yeast

DNA Repair

Volumn 10, Issue 11, 2011, Pages 1086-1094

  George, Carolyn M ^a   Lyndaker, Amy M ^a   Alani, Eric ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

DNA damage response; DNA mismatch repair; Heteroduplex rejection; Rad9

Indexed keywords

FUNGAL DNA; HETERODUPLEX; NOCODAZOLE; PROTEIN RAD9;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CONTROLLED STUDY; DNA DAMAGE; DNA DAMAGE RESPONSE; DNA RECOMBINATION; DNA REPAIR; DNA SEQUENCE; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; FUNGAL STRAIN; FUNGUS MUTANT; GENE FUNCTION; GENE REARRANGEMENT; NONHUMAN; PRIORITY JOURNAL; WILD TYPE; YEAST;

CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPAIR; DNA, FUNGAL; HOMOLOGOUS RECOMBINATION; MUTATION; NOCODAZOLE; NUCLEIC ACID HETERODUPLEXES; RECOMBINATION, GENETIC; SACCHAROMYCETALES;

SACCHAROMYCETALES;

EID: 80054752833     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2011.07.007     Document Type: Article

References (78)

1. Schlissel M.S., Kaffer C.R., Curry J.D. Leukemia and lymphoma: a cost of doing business for adaptive immunity. Genes Dev. 2006, 20:1539-1544.
2. Richardson C., Horikoshi N., Pandita T.K. The role of the DNA double-strand break response network in meiosis. DNA Repair (Amst.) 2004, 3:1149-1164.
3. De Lange T. Telomere-related genome instability in cancer. Cold Spring Harb. Symp. Quant. Biol. 2005, 70:197-204.
4. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
5. Lindahl T., Barnes D.E. Repair of endogenous DNA damage. Cold Spring Harb. Symp. Quant. Biol. 2000, 65:127-133.
6. Ward J.F. DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability. Prog. Nucleic Acid Res. Mol. Biol. 1988, 35:95-125.
7. Doll R., Peto R. The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J. Natl. Cancer Inst. 1981, 66:1191-1308.
8. Wogan G.N., Hecht S.S., Felton J.S., Conney A.H., Loeb L.A. Environmental and chemical carcinogenesis. Semin. Cancer Biol. 2004, 14:473-486.
9. Ohnishi T., Mori E., Takahashi A. DNA double-strand breaks: their production, recognition, and repair in eukaryotes. Mutat. Res./Fundam. Mol. Mech. Mutagen. 2009, 669:8-12.
10. Mahadevaiah S.K., Turner J.M., Baudat F., Rogakou E.P., de Boer P., Blanco-Rodríguez J., et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 2001, 27:271-276.
11. Petersen S., Casellas R., Reina-San-Martin B., Chen H.T., Difilippantonio M.J., Wilson P.C., et al. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 2001, 414:660-665.
12. Takahashi A., Matsumoto H., Nagayama K., Kitano M., Hirose S., Tanaka H., et al. Evidence for the involvement of double-strand breaks in heat-induced cell killing. Cancer Res. 2004, 64:8839-8845.
13. Bryant H.E., Schultz N., Thomas H.D., Parker K.M., Flower D., Lopez E., et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
14. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993, 362:709-715.
15. Bresler S.E., Noskin L.A., Suslov A.V. Induction by gamma irradiation of double-strand breaks of Escherichia coli chromosomes and their role in cell lethality. Biophys. J. 1984, 45:749-754.
16. Percy A.J., Chipman J.K. The measurement of DNA strand breaks in rat colonic mucosa by fluorometric analysis of DNA unwinding. Toxicol. Lett. 1991, 56:69-77.
17. Fanning E., Klimovich V., Nager A.R. A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 2006, 34:4126-4137.
18. Durocher D., Jackson S.P. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme?. Curr. Opin. Cell Biol. 2001, 13:225-231.
19. Toh G.W.-L., Lowndes N.F. Role of the Saccharomyces cerevisiae Rad9 protein in sensing and responding to DNA damage. Biochem. Soc. Trans. 2003, 31:242-246.
20. Sanchez Y., Bachant J., Wang H., Hu F., Liu D., Tetzlaff M., et al. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 1999, 286:1166-1171.
21. Sanchez Y., Desany B.A., Jones W.J., Liu Q., Wang B., Elledge S.J. Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 1996, 271:357-360.
22. Bennett C.B., Snipe J.R., Resnick M.A. A persistent double-strand break destabilizes human DNA in yeast and can lead to G2 arrest and lethality. Cancer Res. 1997, 57:1970-1980.
23. Bennett C.B., Lewis A.L., Baldwin K.K., Resnick M.A. Lethality induced by a single site-specific double-strand break in a dispensable yeast plasmid. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:5613-5617.
24. Lee S.E., Pellicioli A., Demeter J., Vaze M.P., Gasch A.P., Malkova A., et al. Arrest, adaptation, and recovery following a chromosome double-strand break in Saccharomyces cerevisiae. Cold Spring Harb. Symp. Quant. Biol. 2000, 65:303-314.
25. Krogh B.O., Symington L.S. Recombination proteins in yeast. Annu. Rev. Genet. 2004, 38:233-271.
26. Rothkamm K., Krüger I., Thompson L.H., Löbrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 2003, 23:5706-5715.
27. Kass E.M., Jasin M. Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett. 2010, 584:3703-3708.
28. Pâques F., Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 1999, 63:349-404.
29. Li W.-H., Gu Z., Wang H., Nekrutenko A. Evolutionary analyses of the human genome. Nature 2001, 409:847-849.
30. Stark J.M., Pierce A.J., Oh J., Pastink A., Jasin M. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol. Cell. Biol. 2004, 24:9305-9316.
31. Mazoyer S. Genomic rearrangements in the BRCA1 and BRCA2 genes. Hum. Mutat. 2005, 25:415-422.
32. Puget N., Gad S., Perrin-Vidoz L., Sinilnikova O.M., Stoppa-Lyonnet D., Lenoir G.M., et al. Distinct BRCA1 rearrangements involving the BRCA1 pseudogene suggest the existence of a recombination hot spot. Am. J. Hum. Genet. 2002, 70:858-865.
33. del Valle J., Feliubadaló L., Nadal M., Teulé A., Miró R., Cuesta R., et al. Identification and comprehensive characterization of large genomic rearrangements in the BRCA1 and BRCA2 genes. Breast Cancer Res. Treat. 2010, 122:733-743.
34. Chance P.F., Abbas N., Lensch M.W., Pentao L., Roa B.B., Patel P.I., et al. Two autosomal dominant neuropathies result from reciprocal DNA duplication/deletion of a region on chromosome 17. Hum. Mol. Genet. 1994, 3:223-228.
35. Sugawara N., Goldfarb T., Studamire B., Alani E., Haber J.E. Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:9315-9320.
36. Goldfarb T., Alani E. Distinct roles for the Saccharomyces cerevisiae mismatch repair proteins in heteroduplex rejection, mismatch repair and nonhomologous tail removal. Genetics 2005, 169:563-574.
37. Nicholson A., Hendrix M., Jinks-Robertson S., Crouse G.F. Regulation of mitotic homeologous recombination in yeast. Functions of mismatch repair and nucleotide excision repair genes. Genetics 2000, 154:133-146.
38. Selva E.M., New L., Crouse G.F., Lahue R.S. Mismatch correction acts as a barrier to homeologous recombination in Saccharomyces cerevisiae. Genetics 1995, 139:1175-1188.
39. Welz-Voegele C., Jinks-Robertson S. Sequence divergence impedes crossover more than noncrossover events during mitotic gap repair in yeast. Genetics 2008, 179:1251-1262.
40. Spell R.M., Jinks-Robertson S. Examination of the roles of Sgs1 and Srs2 helicases in the enforcement of recombination fidelity in Saccharomyces cerevisiae. Genetics 2004, 168:1855-1865.
41. Chen W., Jinks-Robertson S. The role of the mismatch repair machinery in regulating mitotic and meiotic recombination between diverged sequences in yeast. Genetics 1999, 151:1299-1313.
42. Datta A., Hendrix M., Lipsitch M., Jinks-Robertson S. Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:9757-9762.
43. Rose M., Winston F., Hieter P. Methods in Yeast Genetics: A Laboratory Course Manual 1990, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 1990th ed.
44. Amberg D.C., Burke D.J., Strathern J.N. Methods in Yeast Genetics 2005, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 2005th ed.
45. Lyndaker A.M., Goldfarb T., Alani E. Mutants defective in Rad1-Rad10-Slx4 exhibit a unique pattern of viability during mating-type switching in Saccharomyces cerevisiae. Genetics 2008, 179:1807-1821.
46. Weinert T.A., Hartwell L.H. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 1988, 241:317-322.
47. Kolodner R.D., Putnam C.D., Myung K. Maintenance of genome stability in Saccharomyces cerevisiae. Science 2002, 297:552-557.
48. Zierhut C., Diffley J.F.X. Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J. 2008, 27:1875-1885.
49. Lazzaro F., Sapountzi V., Granata M., Pellicioli A., Vaze M., Haber J.E., et al. Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J. 2008, 27:1502-1512.
50. Fasullo M., Bennett T., AhChing P., Koudelik J. The Saccharomyces cerevisiae RAD9 checkpoint reduces the DNA damage-associated stimulation of directed translocations. Mol. Cell. Biol. 1998, 18:1190-1200.
51. Manthey G.M., Bailis A.M. Rad51 inhibits translocation formation by non-conservative homologous recombination in Saccharomyces cerevisiae. PLoS One 2010, 5:e11889.
52. Richardson C., Stark J.M., Ommundsen M., Jasin M. Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability. Oncogene 2004, 23:546-553.
53. Argueso J.L., Westmoreland J., Mieczkowski P.A., Gawel M., Petes T.D., Resnick M.A. Double-strand breaks associated with repetitive DNA can reshape the genome. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:11845-11850.
54. Friedberg E.C. Suffering in silence: the tolerance of DNA damage. Nat. Rev. Mol. Cell Biol. 2005, 6:943-953.
55. Kokoska R.J., Stefanovic L., Tran H.T., Resnick M.A., Gordenin D.A., Petes T.D. Destabilization of yeast micro- and minisatellite DNA sequences by mutations affecting a nuclease involved in Okazaki fragment processing (rad27) and DNA polymerase delta (pol3-t). Mol. Cell. Biol. 1998, 18:2779-2788.
56. Tran H.T., Keen J.D., Kricker M., Resnick M.A., Gordenin D.A. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol. Cell. Biol. 1997, 17:2859-2865.
57. Lambert S., Watson A., Sheedy D.M., Martin B., Carr A.M. Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell 2005, 121:689-702.
58. Kai M., Wang T.S.-F. Checkpoint activation regulates mutagenic translesion synthesis. Genes Dev. 2003, 17:64-76.
59. Kai M., Wang T.S.-F. Checkpoint responses to replication stalling: inducing tolerance and preventing mutagenesis. Mutat. Res. 2003, 532:59-73.
60. Göhler T., Sabbioneda S., Green C.M., Lehmann A.R. ATR-mediated phosphorylation of DNA polymerase η is needed for efficient recovery from UV damage. J. Cell. Biol. 2011, 192:219-227.
61. Murakami-Sekimata A., Huang D., Piening B.D., Bangur C., Paulovich A.G. The Saccharomyces cerevisiae RAD9, RAD17 and RAD24 genes are required for suppression of mutagenic post-replicative repair during chronic DNA damage. DNA Repair (Amst.) 2010, 9:824-834.
62. Smolka M.B., Albuquerque C.P., Chen S.-H., Zhou H. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:10364-10369.
63. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 2001, 15:2177-2196.
64. Toh G.W.-L., Sugawara N., Dong J., Toth R., Lee S.E., Haber J.E., et al. Mec1/Tel1-dependent phosphorylation of Slx4 stimulates Rad1-Rad10-dependent cleavage of non-homologous DNA tails. DNA Repair (Amst.) 2010, 9:718-726.
65. Vilenchik M.M., Knudson A.G. Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:12871-12876.
66. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., et al. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
67. Hoskins R.A., Carlson J.W., Kennedy C., Acevedo D., Evans-Holm M., Frise E., et al. Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 2007, 316:1625-1628.
68. Léger-Silvestre I., Trumtel S., Noaillac-Depeyre J., Gas N. Functional compartmentalization of the nucleus in the budding yeast Saccharomyces cerevisiae. Chromosoma 1999, 108:103-113.
69. Peng J.C., Karpen G.H. Epigenetic regulation of heterochromatic DNA stability. Curr. Opin. Genet. Dev. 2008, 18:204-211.
70. Chiolo I., Minoda A., Colmenares S.U., Polyzos A., Costes S.V., Karpen G.H. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 2011, 144:732-744.
71. Costes S.V., Chiolo I., Pluth J.M., Barcellos-Hoff M.H., Jakob B. Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization. Mutat. Res. 2010, 704:78-87.
72. Torres-Rosell J., Sunjevaric I., De Piccoli G., Sacher M., Eckert-Boulet N., Reid R., et al. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 2007, 9:923-931.
73. Goodarzi A.A., Noon A.T., Deckbar D., Ziv Y., Shiloh Y., Löbrich M., et al. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 2008, 31:167-177.
74. Nagai S., Dubrana K., Tsai-Pflugfelder M., Davidson M.B., Roberts T.M., Brown G.W., et al. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 2008, 322:597-602.
75. Oza P., Jaspersen S.L., Miele A., Dekker J., Peterson C.L. Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev. 2009, 23:912-927.
76. Morin I., Ngo H.-P., Greenall A., Zubko M.K., Morrice N., Lydall D. Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response. EMBO J. 2008, 27:2400-2410.
77. Barlow J.H., Lisby M., Rothstein R. Differential regulation of the cellular response to DNA double-strand breaks in G1. Mol. Cell 2008, 30:73-85.
78. Rich T., Allen R.L., Wyllie A.H. Defying death after DNA damage. Nature 2000, 407:777-783.