Different mating-type-regulated genes affect the DNA repair defects of saccharomyces RAD51, RAD52 and RAD55 mutants

Genetics

Volumn 174, Issue 1, 2006, Pages 41-55

  Valencia Burton, Maria ^a,c   Oki, Masaya ^b,d   Johnson, Jean ^a   Seier, Tracey A ^a   Kamakaka, Rohinton ^b,e   Haber, James E ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c BOSTON UNIVERSITY   (United States)

^d NAGASAKI UNIVERSITY   (Japan)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; FLAVODOXIN; FUNGAL PROTEIN; ISOMERASE; MUTANT PROTEIN; PROTEIN RAD55; RAD51 PROTEIN; RAD52 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DRUG SENSITIVITY; FUNGAL CELL; GENE CONTROL; GENE DELETION; GENE MUTATION; GENE REPRESSION; GENETIC CODE; GENETIC RECOMBINATION; HETEROZYGOSITY; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; RADIOSENSITIVITY; SACCHAROMYCES CEREVISIAE;

CHROMATIN; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; FLAVOPROTEINS; GENE DELETION; GENES, FUNGAL; GENES, MATING TYPE, FUNGAL; HAPLOIDY; HISTONE DEACETYLASES; MUTATION; PEPTIDYLPROLYL ISOMERASE; PROTEIN STRUCTURE, TERTIARY; RAD51 RECOMBINASE; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN-CONJUGATING ENZYMES;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 33748885242     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.106.058685     Document Type: Article

References (65)

1. ADACHI, N., S. SO and H. KOYAMA, 2004 Loss of nonhomologous end joining confers camptothecin resistance in DT40 cells. Implications for the repair of topoisomerase I-mediated DNA damage. J. Biol. Chem. 279: 37343-37348.
2. ASLESON, E. N., R. J. OKAGAKI and D. M. LIVINGSTON, 1999 A core activity associated with the N terminus of the yeast RAD52 protein is revealed by RAD51 overexpression suppression of C-terminal rad52 truncation alleles. Genetics 153: 681-692.
3. ÅSTRÖM, S. U., S. M. OKAMURA and J. RINE, 1999 Yeast cell-type regulation of DNA repair. Nature 397: 310.
4. BENTON, B. M., J. H. ZANG and J. THORNER, 1994 A novel FK506- and rapamycin-binding protein (FPR3 gene product) in the yeast Saccharomyces cerevisiae is a proline rotamase localized to the nucleolus. J. Cell Biol. 127: 623-639.
5. BIRD, A. W., D. Y. YU, M. G. PRAY-GRANT, Q. QIU, K. E. HARMON et al., 2002 Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 419: 411-415.
6. BISHOP, D. K., D. PARK, L. XU and N. KLECKNER, 1992 DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69: 439-456.
7. BLUMENTAL-PERRY, A., W. LI, G. SIMCHEN and A. P. MITCHELL, 2002 Repression and activation domains of RME1p structurally overlap, but differ in genetic requirements. Mol. Biol. Cell 13: 1709-1721.
8. BOULTON, S. J., and S. P. JACKSON, 1996a Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res. 24: 4639-4648.
9. BOULTON, S. J., and S. P. JACKSON, 1996b Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J. 15: 5093-5103.
10. BOUNDY-MILLS, K. L., and D. M. LIVINGSTON, 1993 A Saccharomyces cerevisiae RAD52 allele expressing a C-terminal truncation protein: activities and intragenic complementation of missense mutations. Genetics 133: 39-49.
11. CHAI, B., J. HUANG, B. R. CAIRNS and B. C. LAURENT, 2005 Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19: 1656-1661.
12. COVITZ, P. A., and A. P. MITCHELL, 1993 Repression by the yeast meiotic inhibitor RME1. Genes Dev. 7: 1598-1608.
13. DAVEY, M., C. HANNAM, C. WONG and C. J. BRANDL, 2000 The yeast peptidyl proline isomerases FPR3 and FPR4, in high copy numbers, suppress defects resulting from the absence of the E3 ubiquitin ligase TOM1. Mol. Gen. Genet. 263: 520-526.
14. DOWNS, J. A., N. F. LOWNDES and S. P. JACKSON, 2000 A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408: 1001-1004.
15. FASULLO, M., and P. DAVE, 1994 Mating type regulates the radiation-associated stimulation of reciprocal translocation events in Saccharomyces cerevisiae. Mol. Gen. Genet. 243: 63-70.
16. FRANK-VAILLANT, M., and S. MARCAND, 2001 NHEJ regulation by mating type is exercised through a novel protein, Lif2p, essential to the ligase IV pathway. Genes Dev. 15: 3005-3012.
17. FRENZ, L. M., A. L. JOHNSON and L. H. JOHNSTON, 2001 Rme1, which controls CLN2 expression in Saccharomyces cerevisiae, is a nuclear protein that is cell cycle regulated. Mol. Genet. Genomics 266: 374-384.
18. FRIIS, J., and H. ROMAN, 1968 The effect of the mating-type alleles on intragenic recombination in yeast. Genetics 59: 33-36.
19. GALITSKI, T., A. J. SALDANHA, C. A. STYLES, E. S. LANDER and G. R. FINK, 1999 Ploidy regulation of gene expression. Science 285: 251-254.
20. HAYS, S. L., A. A. FIRMENICH and P. BERG, 1995 Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc. Natl. Acad. Sci. USA 92: 6925-6929.
21. HERRMANN, G., T. LINDAHL and P. SCHAR, 1998 Saccharomyces cerevisiae LIF1: a function involved in DNA double-strand break repair related to mammalian XRCC4. EMBO J. 17: 4188-4198.
22. HEUDE, M., and F. FABRE, 1993 a/α-control of DNA repair in the yeast Saccharomyces cerevisiae: genetic and physiological aspects. Genetics 133: 489-498.
23. HO, Y., A. GRUHLER, A. HEILBUT, G. D. BADER, L. MOORE et al., 2002 Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415: 180-183.
24. HOCHWAGEN, A., W. H. THAM, G. A. BRAR and A. AMON, 2005 The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell 122: 861-873.
25. HSIANG, Y. H., M. G. LIHOU and L. F. LIU, 1989 Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res. 49: 5077-5082.
26. JOHNSON, R. D., and L. S. SYMINGTON, 1995 Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol. Cell. Biol. 15: 4843-4850.
27. KEGEL, A., J. O. SJOSTRAND and S. U. ASTROM, 2001 Nej1p, a cell type-specific regulator of nonhomologous end joining in yeast. Curr. Biol. 11: 1611-1617.
28. KURDISTANI, S. K., D. ROBYR, S. TAVAZOIE and M. GRUNSTEIN, 2002 Genome-wide binding map of the histone deacetylase Rpd3 in yeast. Nat. Genet. 31: 248-254.
29. LEE, S. E., F. PÂQUES, J. SYLVAN and J. E. HABER, 1999 Role of yeast SIR genes and mating type in channeling double-strand breaks to homologous and nonhomologous recombination pathways. Curr. Biol. 9: 767-770.
30. LEE, S. E., A. PELLICIOLI, A. MALKOVA, M. FOIANI and J. E. HABER, 2001 The Saccharomyces recombination protein Tid1p is required for adaptation from G2/M arrest induced by a double-strand break. Curr. Biol. 11: 1053-1057.
31. LITT, M. D., M. SIMPSON, F. RECILLAS-TARGA, M. N. PRIOLEAU and G. FELSENFELD, 2001 Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 20: 2224-2235.
32. LOVETT, S. T., 1994 Sequence of the RAD55 gene of Saccharomyces cerevisiae: similarity of Rad55 to prokaryotic RecA and other RecA-like proteins. Gene 142: 103-106.
33. LOVETT, S. T., and R. K. MORTIMER, 1987 Characterization of null mutants of the RAD55 gene of Saccharomyces cerevisiae: effects of temperature, osmotic strength and mating type. Genetics 116: 547-553.
34. LOWELL, J. E., A. I. ROUGHTON, V. LUNDBLAD and L. PILLUS, 2003 Telomerase-independent proliferation is influenced by cell type in Saccharomyces cerevisiae. Genetics 164: 909-921.
35. MILNE, G. T., S. JIN, K. B. SHANNON and D. T. WEAVER, 1996 Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 4189-4198.
36. MIZUNO, T., and S. HARASHIMA, 2000 Activation of basal transcription by a mutation in SIN4, a yeast global repressor, occurs through a mechanism different from activator-mediated transcriptional enhancement. Mol. Gen. Genet. 263: 48-59.
37. 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.
38. MORGAN, E. A., N. SHAH and L. S. SYMINGTON, 2002 The requirement for ATP hydrolysis by Saccharomyces cerevisiae Rad51 is by-passed by mating-type heterozygosity or RAD54 in high copy. Mol. Cell. Biol. 22: 6336-6343.
39. MORRISON, A. J., J. HIGHLAND, N. J. KROGAN, A. ARBEL-EDEN, J. F. GREENBLATT et al., 2004 INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119: 767-775.
40. MYUNG, K., and R. D. KOLODNER, 2003 Induction of genome instability by DNA damage in Saccharomyces cerevisiae. DNA Rep. 2: 243-258.
41. NARESH, A., S. SAINI and J. SINGH, 2003 Identification of Uhp1, a ubiquitinated histone-like protein, as a target/mediator of Rhp6 in mating-type silencing in fission yeast. J. Biol. Chem. 278: 9185-9194.
42. OOI, S. L., and J. D. BOEKE, 2001 A DNA microarray-based genetic screen for nonhomologous end-joining mutants in Saccharomyces cerevisiae. Science 294: 2552-2556.
43. PÂQUES, F., and J. E. HABER, 1999 Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63: 349-404.
44. REDON, C., D. R. PILCH, E. P. ROGAKOU, A. H. ORR, N. F. LOWNDES et al., 2003 Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint-blind DNA damage. EMBO Rep. 4: 678-684.
45. RESNICK, M. A., J. NITISS, C. EDWARDS and R. E. MALONE, 1986 Meiosis can induce recombination in rad52 mutants of Saccharomyces cerevisiae. Genetics 113: 531-550.
46. SAEKI, T., I. MACHIDA and S. NAKAI, 1980 Genetic control of diploid recovery after gamma-irradiation in the yeast Saccharomyces cerevisiae. Mutat. Res. 73: 251-265.
47. SCHÄR, P., G. HERRMANN, G. DALY and T. LINDAHL, 1997 A newly identified DNA ligase of Saccharomyces cerevisiae involved in RAD52-independent repair of DNA double-strand breaks. Genes Dev. 11: 1912-1924.
48. SCHILD, D., 1995 Suppression of a new allele of the yeast RAD52 gene by overexpression of RAD51, mutations in srs2 and ccr4, or mating-type heterozygosity. Genetics 140: 115-127.
49. SHIM, E. Y., J. L. MA, J. H. OUM, Y. YANEZ and S. E. LEE, 2005 The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell. Biol. 25: 3934-3944.
50. SHINOHARA, A., H. OGAWA and T. OGAWA, 1992 Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69: 457-470.
51. SHINOHARA, A., S. GASIOR, T. OGAWA, N. KLECKNER and D. K. BISHOP, 1997 Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 2: 615-629.
52. SIGNON, L., A. MALKOVA, M. NAYLOR and J. E. HABER, 2001 Genetic requirements for RAD51- and RAD54-independent break-induced replication repair of a chromosomal double-strand break. Mol. Cell. Biol. 21: 2048-2056.
53. SUGAWARA, N., X. WANG and J. E. HABER, 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. SUNG, P., and S. A. STRATTON, 1996 Yeast Rad51 recombinase mediates polar DNA strand exchange in the absence of ATP hydrolysis. J. Biol. Chem. 271: 27983-27986.
57. SYMINGTON, L. S., 2002 Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66: 630-670.
58. TEO, S. H., and S. P. JACKSON, 1997 Identification of Saccharomyces cerevisiae DNA ligase IV: involvement in DNA double-strand break repair. EMBO J. 16: 4788-4795.
59. TSUKAMOTO, M., K. YAMASHITA, T. MIYAZAKI, M. SHINOHARA and A. SHINOHARA, 2003 The N-terminal DNA-binding domain of Rad52 promotes RAD51-independent recombination in Saccharomyces cerevisiae. Genetics 165: 1703-1715.
60. TSUKAMOTO, Y., J. KATO and H. IKEDA, 1996 Effects of mutations of RAD50, RAD51, RAD52, and related genes on illegitimate recombination in Saccharomyces cerevisiae. Genetics 142: 383-391.
61. VALENCIA, M., M. BENTELE, M. B. VAZE, G. HERRMANN, E. KRAUS et al., 2001 NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae. Nature 414: 666-669.
62. WILSON, T. E., U. GRAWUNDER and M. R. LIEBER, 1997 Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 388: 495-498.
63. WOLNER, B., S. VAN KOMEN, P. SUNG and C. L. PETERSON, 2003 Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12: 221-232.
64. WU, J., and L. F. LIU, 1997 Processing of topoisomerase I cleavable complexes into DNA damage by transcription. Nucleic Acids Res. 25: 4181-4186.
65. WYRICK, J. J., F. C. HOLSTEGE, E. G. JENNINGS, H. C. CAUSTON, D. SHORE et al., 1999 Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature 402: 418-421.