Damage-induced recombination in the yeast Saccharomyces cerevisiae

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 451, Issue 1-2, 2000, Pages 91-105

  Kupiec, Martin ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

DNA Repair; Eukaryotic cell; Genetic recombination; Saccharomyces cerevisiae

Indexed keywords

ALKYLATING AGENT; CARCINOGEN;

CELL CYCLE; DNA CROSS LINKING; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; EVOLUTION; GENOTOXICITY; MATING TYPE; MITOSIS; MUTATION; PRIORITY JOURNAL; RADIATION INJURY; REVIEW; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; ULTRAVIOLET IRRADIATION;

ALKYLATING AGENTS; CELL CYCLE; CROSS-LINKING REAGENTS; DNA DAMAGE; HUMANS; RECOMBINATION, GENETIC; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS;

EUKARYOTA; MAMMALIA; PROKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 0034733693     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0027-5107(00)00042-7     Document Type: Review

References (129)

1. Aboussekhra A., Vialard J.E., Morrison D.E., Torre-Ruiz M.A., Cernakova L., Fabre F., Lowndes N.F. A novel role for the budding yeast RAD9 checkpoint gene in DNA damage-dependent transcription. EMBO J. 15:1996;3912-3922.
2. Aguilera A., Klein H.L. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae: I. Isolation and genetic characterization of hyper-recombination mutations. Genetics. 119:1988;779-790.
3. Averbeck D., Averbeck S. Induction of the genes RAD54 and RNR2 by various DNA damaging agents in Saccharomyces cerevisiae. Mutat. Res. 315:1994;123-138.
4. Averbeck D., Averbeck S. DNA photodamage, repair, gene induction and genotoxicity following exposures to 254 nm UV and 8-methoxyposoralen plus UVA in a eukaryotic cell system. Photochem. Photobiol. 68:1998;289-295.
5. Bierne H., Michel B. When replication forks stop. Mol. Microbiol. 13:1994;17-23.
6. Boiteaux S., Huisman O., Laval J. 3-Methyladenine residues in DNA induce the SOS function sfiA in Escherichia coli. EMBO J. 3:1984;2569-2573.
7. Boreham D.R., Mitchel R.E. DNA lesions that signal the induction of radioresistance and DNA repair in yeast. Radiat. Res. 128:1991;19-28.
8. Brennan R.J., Swoboda B.E.P., Schiestl R.H. Oxidative mutagens induce intrachromosomal recombination in yeast. Mutat. Res. 308:1994;159-167.
9. Brugarolas J., Chandrasekaran C., Gordon J.I., Beach D., Jacks T., Hannon G.J. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature. 377:1995;552-557.
10. Brunborg G., Resnick M., Williamson D.H. Cell cycle-specific repair of DNA DSBs in Saccharomyces cerevisiae. Radiat. Res. 82:1980;547-558.
11. Chen W., Jinks-Robertson S. Mismatch repair proteins regulate heteroduplex formation during mitotic recombination in yeast. Mol. Cell. Biol. 18:1998;6525-6537.
12. Clever B., Schmuckli-Maurer J., Sigrist M., Glassner B.J., Heyer W.D. Specific negative effects resulting from elevated levels of the recombinational repair protein Rad54p in Saccharomyces cerevisiae. Yeast. 15:1999;721-740.
13. Cole R.S. Repair of DNA containing interstrand crosslinks in E. coli: sequential excision and recombination. Proc. Natl. Acad. Sci. U. S. A. 70:1973;1064-1068.
14. Cole G.M., Schild D., Lovett S.T., Mortimer R.K. Regulation of RAD54 and RAD52-lacZ gene fusions in S. cerevisiae in response to DNA damage. Mol. Cell. Biol. 7:1987;1078-1084.
15. Cole G.M., Lovett S.T., Schild D., Mortimer R.K. Failure to induce a DNA repair gene, RAD54, in Saccharomyces cerevisiae does not affect DNA repair or recombination pathways. Mol. Cell. Biol. 9:1989;3314-3322.
16. Cooper A.J., Waters R. A complex pattern of sensitivity to simple monofunctional alkylating agents exists amongst the rad mutants of Saccharomyces cerevisiae. Mol. Gen. Genet. 209:1987;142-148.
17. Crutzen P.J. Ultraviolet on the increase. Nature. 356:1992;104-105.
18. Dardalhon M., Averbeck D. Pulsed-field gel electrophoresis analysis of the repair of psoralen plus UVA induced DNA photoadducts in Saccharomyces cerevisiae. Mutat. Res. 336:1995;49-60.
19. Davies P.J., Tippins R.S., Parry J.M. Cell cycle variation in the inducibility of lethality and mitotic recombination after treatment with UV and nitrous acid in the yeast Saccharomyces cerevisiae. Mutat. Res. 51:1978;327-346.
20. DiCaprio L., Cox B.S. The effect of UV irradiation on the molecular weight of preexisting and newly-synthesized DNA of yeast. Mutat. Res. 82:1981;69-85.
21. Dolling J.A., Boreham D.R., Brown D.L., Raaphorst G.P., Mitchel R.E. Cisplatin-modification of DNA repair and ionizing radiation lethality in yeast Saccharomyces cerevisiae. Mutat. Res. 433:1999;127-136.
22. Eckardt-Schupp F., Klaus C. Radiation inducible DNA repair processes in eukaryotes. Biochimie. 81:1999;161-171.
23. Esposito M.S., Wagstaff J.E. Mechanisms of mitotic recombination. Strathern J.N., Jones E.W., Broach J.R. The Molecular Biology of the Yeast Saccharomyces. 1981;341-370 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
24. Esposito R.E. Genetic recombination in synchronized cultures of Saccharomyces cerevisiae. Genetics. 59:1968;191-202.
25. Evensen G., Seeberg E. Adaptation to alkylation resistance involves the induction of a DNA glycosylase. Nature. 296:1982;773-775.
26. Fabre F. Induced intragenic recombination in yeast can occur during the G1 mitotic phase. Nature. 272:1978;795-798.
27. Fabre F. Mitotic recombination and repair in relation to cell cycle. von Wettstein D., Friis J., Kielland-Brandt M., Stenderup A. Molecular Genetics of Yeast. 1981;399-409 Munskgaad, Copenhagen.
28. Fabre F., Boulet A., Roman H. Gene conversion at different points in the mitotic cycle of Saccharomyces cerevisiae. Mol. Gen. Genet. 195:1984;139-143.
29. Fabre F., Roman H. Genetic evidence for the inducibility of recombination competence in yeast. Proc. Natl. Acad. Sci. U. S. A. 74:1977;1667-1671.
30. Fahrig R. Evidence that induction and suppression of mutations and recombinations by chemical mutagens in S. cerevisiae during mitosis are jointly correlated. Mol. Gen. Genet. 168:1979;125-139.
31. Fasullo M., Bennet T., Dave P. Expression of Saccharomyces cerevisiae MATa and MATα enhances the HO endonuclease-stimulation of chromosomal rearrangements directed by his3 recombinational substrates. Mutat. Res. 433:1999;33-44.
32. Fasullo M., Dave P. Mating type regulates the radiation-associated stimulation of reciprocal translocation events in Saccharomyces cerevisiae. Mol. Gen. Genet. 243:1994;63-70.
33. Fasullo M.T., Dave P., Rothstein R. DNA damaging agents stimulate the formation of directed reciprocal translocations in Saccharomyces cerevisiae. Mutat. Res. 314:1994;121-133.
34. Fasullo M.T., Davis R.W. Recombinational substrates designed to study recombination between unique and repetitive sequences in vivo. Proc. Natl. Acad. Sci. U. S. A. 84:1987;6215-6219.
35. Fasullo M.T., Davis R.W. Direction of chromosome rearrangements in Saccharomyces cerevisiae by use of his3 recombinational substrates. Mol. Cell. Biol. 8:1988;4370-4380.
36. Frankenberg D., Frankenberg-Schwager M., Blocher D., Harbich R. Evidence for DNA DSBs as the critical lesions in yeast cells irradiated with sparsely or densely ionizing radiation under oxic and anoxic conditions. Radiat. Res. 88:1981;524-532.
37. Frankenberg-Schwager M., Frankenberg D. DNA double-strand breaks: their repair and relationship to cell killing in yeast. Intl. J. Radiat. Biol. 58:1990;569-575.
38. Friedberg E.C., Walker G.C., Siede W. DNA Repair and Mutagenesis. 1995;American Society for Microbiology, Washington, DC.
39. Friedl A.A., Kiechle M., Fellerhoff B., Eckardt-Schupp F. Radiation-induced chromosome aberrations in Saccharomyces cerevisiae: influence of DNA repair pathways. Genetics. 148:1998;975-988.
40. Friis J., Roman H. The effect of the mating type alleles on intragenic recombination in yeast. Genetics. 59:1968;33-36.
41. Galli A., Schiestl R.H. On the mechanism of UV and Gamma-ray induced intrachromosomal recombination in yeast cells synchronized in different stages of the cell cycle. Mol. Gen. Genet. 248:1995;301-310.
42. Galli A., Schiestl R.H. Effects of DNA double-strand and single-strand breaks on intrachromosomal recombination events in cell cycle-arrested yeast cells. Genetics. 149:1998;1235-1250.
43. Galli A., Schiestl R.H. Cell division transforms mutagenic lesions into deletion-recombinogenic lesions in yeast cells. Mutat. Res. 429:1999;13-26.
44. Galloway S.M. Chromosome aberrations induced in vitro: mechanism, delayed expression, and intriguing questions. Environ. Mol. Mutagen. 23:1994;44-53.
45. Game J.C. DNA double-strand breaks and the RAD50-RAD57 genes in Saccharomyces cerevisiae. Sem. Cancer Biol. 4:1993;73-83.
46. Game J.C., Sitney K.C., Cook V.E., Mortimer R.K. Use of a ring chromosome and pulse-field gels to study interhomolog recombination, double-strand DNA breaks and sister-chromatid exchange in yeast. Genetics. 123:1989;695-713.
47. Grossman K.F., Brown J., Moses R.E. Cisplatin DNA cross-links do not inhibit S-phase and cause only a G2/M arrest in Saccharomyces cerevisiae. Mutat. Res. 434:1999;29-39.
48. Hagmar L., Bonassi S., Stromberg U., Brogger A., Knudsen L.E., Norppa H., Reuterwall C. Chromosomal aberrations in lymphocytes predict human cancer: a report from the European Study Group on Cytogenic Biomarkers and Health (ESCH). Cancer Res. 58:1998;4117-4121.
49. Halas A., Baranowska H., Policinska Z., Jachymczyk W.J. Involvement of the RE V3 gene in the methylated base-excision repair system. Co-operation of two DNA polymerases, delta and Rev3p, in the repair of MMS-induced lesions in the DNA of Saccharomyces cerevisiae. Curr. Genet. 31:1997;292-301.
50. Hall P., Holm L.E. Radiation-associated thyroid cancer - facts and fiction. Acta Oncol. 37:1998;325-330.
51. Haynes R.H., Kunz B.A. DNA repair and mutagenesis. Strathern J.N., Jones E.W., Broach J.R. The Molecular Biology of the Yeast Saccharomyces. 1981;371-414 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
52. Heude M., Fabre F. a/α control of DNA repair in the yeast Saccharomyces cerevisiae: genetic and physiological aspects. Genetics. 133:1993;489-498.
53. Hopper A.K., Kirsch J., Hall B.D. Mating type and sporulation in yeast: II. Meiosis, recombination and radiation-sensitivity in an α/α diploid with altered sporulation control. Genetics. 80:1975;61-76.
54. Huang M., Zhou Z., Elledge S.J. The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell. 94:1998;595-605.
55. Hunnable E.G., Cox B.S. The genetic control of dark recombination in yeast. Mutat. Res. 13:1971;297-309.
56. Jablonovich Z., Liefshitz B., Steinlauf R., Kupiec M. Characterization of the role played by the RAD59 gene of Saccharomyces cerevisiae in ectopic recombination. Curr. Genet. 36:1999;13-20.
57. Jachymczyk W.J., Chlebowicz E., Swietlinska Z., Zuk J. Alkaline sucrose sedimentation studies of MMS-induced DNA single-strand breakage and rejoining in the wild type and in UV-sensitive mutants of Saccharomyces cerevisiae. Mutat. Res. 43:1977;1-10.
58. Jelinsky S.A., Samson L.D. Global response of Saccharomyces cerevisiae to an alkylating agent. Proc. Nat. Acad. Sci. U. S. A. 96:1999;1486-1491.
59. Jinks-Robertson S., Petes T.D. Chromosomal translocations generated by high frequency meiotic recombination between repeated yeast genes. Genetics. 114:1986;731-752.
60. Johnston L.H., Johnson A.L. Induced recombination in the mitotic cell cycle of the yeast Saccharomyces cerevisiae. Genet. Res. Camb. 43:1983;1-10.
61. Kadyk L.C., Hartwell L.H. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics. 132:1992;387-402.
62. Kadyk L.C., Hartwell L.H. Replication-dependent sister chromatid recombination in rad1 mutants of Saccharomyces cerevisiae. Genetics. 133:1993;469-487.
63. Kanaar R., Hoeijmakers J.H.J., van Gent D.C. Molecular mechanisms of double-strand break repair. Trends Cell Biol. 8:1998;483-489.
64. Kaufmann W.K., Paules R.S. DNA damage and cell cycle checkpoints. FASEB J. 10:1996;238-247.
65. Kern R., Zimmermann F.K. The influence of defects in excision and error prone repair on spontaneous and induced mitotic recombination and mutation in Saccharomyces cerevisiae. Mol. Gen. Genet. 161:1978;81-88.
66. Klein H.L. RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis. Genetics. 147:1997;1533-1543.
67. Klein H.L., Petes T.D. Intrachromosomal gene conversion in yeast. Nature. 289:1981;144-148.
68. Kupiec M., Byers B., Esposito R.E., Mitchell A.P. Meiosis and sporulation in Saccharomyces cerevisiae. The Molecular Biology of the Yeast Saccharomyces. 1997;889-1036 Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
69. Kupiec M., Petes T.D. Meiotic recombination between repeated transposable elements in Saccharomyces cerevisiae. Mol. Cell Biol. 8:1988;2942-2954.
70. Kupiec M., Petes T.D. Allelic and ectopic recombination between Ty elements in yeast. Genetics. 119:1998;549-559.
71. Kupiec M., Simchen G. Arrest of the mitotic cell cycle and of meiosis in Saccharomyces cerevisiae by MMS. Mol. Gen. Genet. 201:1985;558-564.
72. Kupiec M., Steinlauf R. Damage-induced ectopic recombination in the yeast Saccharomyces cerevisiae. Mutat. Res. 384:1997;33-44.
73. Leder P., Battey J., Lenoir G., Moulding C., Murphy W., Porter H., Stewart T., Taub T. Translocations among antibody genes and human cancer. Science. 222:1983;765-770.
74. Lehnert S., Chow T.Y. Low doses of ionizing radiation induce nuclear activity in human tumor cell lines which catalyzes homologous double-strand recombination. Radiat. Environ. Biophys. 36:1997;67-70.
75. Lichten M., Haber J.E. Position effects in ectopic and allelic mitotic recombination in Saccharomyces cerevisiae. Genetics. 123:1989;261-268.
76. Liefshitz B., Parket A., Maya R., Kupiec M. The role of DNA repair genes in recombination between repeated sequences in yeast. Genetics. 140:1995;1199-1211.
77. Liefshitz B., Steinlauf R., Friedl A., Eckardt-Schupp F., Kupiec M. Genetic interactions between mutants of the "error-prone" repair group of Saccharomyces cerevisiae and their effect on recombination and mutagenesis. Mutat. Res. 407:1998;135-145.
78. Lovett S.T., Drapkin P.T., Sutera V.A., Gluckman-Peskind T.J. A sister-strand exchange mechanism for recA-independent deletion of repeated DNA sequences in E. coli. Genetics. 135:1993;631-642.
79. Malkova A., Ross L., Dawson D., Hoekstra M.F., Haber J.E. Meiotic recombination initiated by a double-strand break in rad50 delta yeast cells otherwise unable to initiate meiotic recombination. Genetics. 143:1996;741-754.
80. Manney T.R., Mortimer R.K. Allelic mapping in yeast by X-ray induced mitotic reversion. Science. 143:1964;581-583.
81. Meira L.B., Fonseca M.B., Averbeck D., Schenberg A.C.G., Henriques J.A.P. The pso4-1 mutation reduces spontaneous mitotic gene conversion and reciprocal recombination in Saccharomyces cerevisiae. Mol. Gen. Genet. 235:1992;311-316.
82. Mitra S., Kaina B. Regulation of repair of alkylation damage in mammalian genomes. Progr. Nucleic Acid Res. Mol. Biol. vol. 44:1993;109-142 Academic Press, New York.
83. Mortimer R.K., Fogel S. Genetic interference and gene conversion. Grell R.F. Mechanisms in Recombination. 1969;263-275 Plenum, New York.
84. Mothersill C., Seymour C.B. Mechanisms and implications of genomic instability and other delayed effects of ionizing radiation exposure. Mutagenesis. 13:1998;421-426.
85. Moustacchi E., Cassier C., Chanet R., Magana-Schwenke N., Saeki T., Henriques J.A.P. Biological role of photo-induced crosslinks and monoadducts in yeast DNA: genetic control and steps involved in their repair. Friedberg E.C., Bridges B.A. Cellular Responses to DNA Damage. 1983;87-106 A.R. Liss, New York.
86. Nevo-Caspi Y., Kupiec M. Transcriptional induction of Ty recombination in yeast. Proc. Natl. Acad. Sci. U. S. A. 91:1994;12711-12715.
87. Olivieri G., Bodycote J., Wolff S. Adaptive response of human lymphocytes to low concentrations of radioactive thymidine. Science. 223:1984;594-597.
88. Paques F., Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63:1999;349-404.
89. Parket A., Kupiec M. Ectopic recombination between Ty elements in Saccharomyces cerevisiae is not induced by DNA damage. Mol. Cell. Biol. 12:1992;4441-4448.
90. Parket A., Inbar O., Kupiec M. Recombination of Ty elements in yeast can be induced by a double-strand break. Genetics. 140:1995;67-77.
91. Paulovich A.G., Margulies R.U., Garvik B.M., Hartwell L.H. RAD9, RAD17 and RAD24 are required for S phase regulation in Saccharomyces cerevisiae in response to DNA damage. Genetics. 145:1997;45-62.
92. Petes T.D., Malone R.E., Symington L.S. Recombination in yeast. Broach J.R., Pringle J.R., Jones E.W. Molecular and Cellular Biology of the Yeast Saccharomyces cerevisiae. 1991;407-521 Cold Spring Harbor Lab. Press, Plainview, NY.
93. Raaphorst G.P., Wang G., Stewart D., Ng C.E. Concomitant low dose-rate irradiation and cisplatin treatment in ovarian carcinoma cell lines sensitive and resistant to cisplatin treatment. Int. J. Radiat. Biol. 69:1996;623-631.
94. Resnick M.A., Martin P. The repair of double-strand breaks in the nuclear DNA of Saccharomyces cerevisiae and its genetic control. Mol. Gen. Genet. 143:1976;119-129.
95. Richardson C., Moynahan M.E., Jasin M. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12:1998;3831-3842.
96. Roman H., Jacob F. A comparison of spontaneous and UV-induced allelic recombination with reference to the recombination of outside markers. Cold Spring Harbor Symp. Quant. Biol. 23:1959;155-160.
97. Schiestl R.H. Nonmutagenic carcinogens induce intrachromosomal recombination in yeast. Nature. 337:1989;285-288.
98. Schiestl R.H., Igarashi S., Hastings P.J. Analysis of the mechanism for reversion of a disrupted gene. Genetics. 119:1988;237-247.
99. Schiestl R.H., Prakash S. RAD1, an excision repair gene of Saccharomyces cerevisiae, is also involved in recombination. Mol. Cell. Biol. 8:1988;3619-3626.
100. Schild D. Suppression of a new allele of the yeast RAD52 gene by overexpression of RAD51, mutations in srs2 and ccr4 or mating type heterozygosity. Genetics. 140:1996;1150127.
101. Sengstag C., Weibel B., Fasullo M. Genotoxicity of Aflatoxin B1: evidence for a recombination-mediated mechanism in Saccharomyces cerevisiae. Cancer Res. 56:1996;5457-5465.
102. Sherman F., Roman H. Evidence for two types of allelic recombination in yeast. Genetics. 48:1963;253-271.
103. Shulman M.J., Collins C., Connor A., Read L.R., Baker M.D. Interchromosomal recombination is suppressed in mammalian somatic cells. EMBO J. 14:1995;4102-4107.
104. Siede W., Eckardt F. Indications for an inducible component of error-prone DNA repair in yeast. Br. J. Cancer. 6:1984;103-106.
105. Siede W., Robinson G.W., Kalainov D., Malley T., Friedberg E.C. Regulation of the RAD2 gene of Saccharomyces cerevisiae. Mol. Microbiol. 3:1989;1697-1698.
106. Silberman R., Kupiec M. Plasmid-mediated induction of recombination in yeast. Genetics. 137:1994;41-48.
107. Simon J.R., Moore P.D. Induction of homologous recombination in Saccharomyces cerevisiae. Mol. Gen. Genet. 214:1988;37-41.
108. Skov K., MacPhail S. Interaction of platinum drugs with clinically relevant X-ray doses in mammalian cells: a comparison of cisplatin, carboplatin, iproplatin, and teraplatin. Int. J. Radiat. Oncol., Biol., Phys. 20:1991;221-225.
109. Snow R., Korch C.T. Alkylation induced gene conversion in yeast: use in fine structure mapping. Mol. Gen. Genet. 107:1970;201-208.
110. Stahl F. Meiotic recombination in yeast: coronation of the double-strand-break repair model. Cell. 87:1996;965-968.
111. Sun Z., Fay D.S., Marini F., Stern D.F. Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint. Genes Dev. 10:1996;395-406.
112. Szostak J.W., Wu R. Unequal crossing-over in the ribosomal DNA of Saccharomyces cerevisiae. Nature. 284:1980;426-430.
113. Takata M., Sasaki M.S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17:1998;5497-5508.
114. Tan T.L.R., Essers J., Citterio E., Swagemakers S.M.A., de Wit J., Benson F.E., Hoeijmakers J.H.J., Kanaar R. Mouse Rad54 affects DNA conformation and DNA-damage-induced Rad51 foci formation. Curr. Biol. 9:1999;325-328.
115. Thorne L.W., Byers B. Stage-specific effects of X-irradiation on yeast meiosis. Genetics. 134:1993;29-42.
116. Tlsty T.D., Brown P.C., Schimke R.T. UV-irradiation facilitates methotrexate resistance and amplification of the dihidrofolate reductase gene in cultured 3T6 cells. Mol. Cell. Biol. 4:1984;1040-1056.
117. Torres-Ramos C.A., Prakash S., Prakash L. Requirement of yeast DNA polymerase Delta in Post-replicational repair of UV-damaged DNA. J. Biol. Chem. 272:1997;25445-25448.
118. Van Dyck E., Stasiak A.Z., Stasiak A., West S.C. Binding of double-strand breaks in DNA by human Rad52 protein. Nature. 398:1999;728-731.
119. Weeda G., de Boer J., Donker I., de Wit J., Winkler S.B., van der Horst G.T., Vermeulen W., Bootsma D., Hoeijmakers J.H. Molecular basis of DNA repair mechanisms and syndromes. Rec. Results Cancer Res. 154:1998;147-155.
120. Wildenberg J. The relation of mitotic recombination to DNA replication in yeast pedigrees. Genetics. 66:1970;291-304.
121. Willis K.K., Klein H.L. Intrachromosomal recombination in Saccharomyces cerevisiae: reciprocal exchange in an inverted repeat and associated gene conversion. Genetics. 117:1987;633-643.
122. Wilkie D., Lewis D. The effect of UV light on recombination in yeast. Genetics. 48:1963;1701-1716.
123. Wurgler F.E. Recombination and gene conversion. Mutat. Res. 284:1992;3-14.
124. Xiao W., Chow B.L. Synergism between yeast nucleotide and base excision repair pathways in the protection against DNA methylation damage. Curr. Genet. 3:1998;92-99.
125. Xiao W., Chow B.L., Rathgeber L. The repair of DNA methylation damage in Saccharomyces cerevisiae. Curr. Genet. 30:1996;461-468.
126. Yan Y.X., Schiestl R.H., Prakash L. mating-type suppression of the DNA-repair defect of the yeast rad6Δ mutation requires the activity of genes in the RAD52 epistasis group. Curr. Genet. 28:1995;8-12.
127. Zenvirth D., Arbel T., Sherman A., Goldway M., Klein S., Simchen G. Multiple sites for double-strand breaks in whole meiotic chromosomes of Saccharomyces cerevisiae. EMBO J. 11:1992;3441-3447.
128. Zimmermann F.K., von Borstel R.C., von Halle E.S., Parry J.M., Siebert D., Zetterberg G., Barale R., Loprieno N. Testing of chemicals for genetic activity with Saccharomyces cerevisiae: a report of the U.S. Environmental protection agency gene-tox program. Mutat. Res. 133:1984;199-244.
129. Zimmermann F.K., Kern R., Rasenberger H. A yeast strain for simultaneous detection of induced mitotic crossing over, mitotic gene conversion and reverse mutation. Mutat. Res. 28:1975;381-390.