The Saccharomyces cerevisiae ETH1 Gene, an Inducible Homolog of Exonuclease III That Provides Resistance to DNA-Damaging Agents and Limits Spontaneous Mutagenesis

REFERENCES

• Alani, E., L. Cao, and J. Kleckner 1987. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics 116:541–545.
   PubMed Web of Science ®Google Scholar
• Ausubel F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, K. Struhl 1987. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
   Google Scholar
• Berbee, M. L., and J. Taylor 1993. Dating the evolutionary radiations of the true funghi. Can. J. Bot. 71:1114–1127.
   Google Scholar
• Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and J. Shao 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453–1474.
   PubMed Web of Science ®Google Scholar
• Chan, E., and J. Weiss 1987. Endonuclease IV of Escherichia coli is induced by paraquat. Proc. Natl. Acad. Sci. USA 84:3189–3193.
   PubMed Web of Science ®Google Scholar
• Cunningham, R. P., S. M. Saporito, S. G. Spitzer, and J. Weiss 1986. Endonuclease IV (nfo) mutant of Escherichia coli. J. Bacteriol. 168:1120–1127.
   PubMed Web of Science ®Google Scholar
• Demple, B., and J. Harrison 1994. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63:915–948.
   PubMed Web of Science ®Google Scholar
• Demple, B., T. Herman, and J. Chen 1991. Cloning and expression of APE, the cDNA encoding the major human apurinic endonuclease: definition of a family of DNA repair enzymes. Proc. Natl. Acad. Sci. USA 88:11450–11454.
   PubMed Web of Science ®Google Scholar
• Elder, R. H., R. J. Weeks, M. A. Willington, D. P. Cooper, J. A. Rafferty, B. Deans, J. H. Hendry, G. P. Margison 1997. Alkylpurine-DNA-N-glycosylase (APNG) knockout mice, abstr. 2411. Meeting of the American Association for Cancer Research. American Association for Cancer Research, San Diego, Calif.
   Google Scholar
• Engelward, B. P., G. Weeda, M. D. Wyatt, J. L. Broekhof, J. de Wit, I. Donker, J. M. Allan, B. Gold, J. H. Hoeijmakers, and J. Samson 1997. Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase. Proc. Natl. Acad. Sci. USA 94:13087–13092.
   PubMed Web of Science ®Google Scholar
• Feldmann, H., M. Aigle, G. Aljinovic, B. Andre, M. C. Baclet, C. Barthe, A. Baur, A. M. Becam, N. Biteau, E. Boles et al.. 1994. Complete DNA sequence of yeast chromosome II. EMBO J. 13:5795–5809.
   PubMedGoogle Scholar
• Feng, Q., J. V. Moran, H. H. Kazazian Jr., and J. Boeke 1996. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87:905–916.
   PubMed Web of Science ®Google Scholar
• Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, K. A. Ketchum, R. Dodson, E. K. Hickey, M. Gwinn, B. Dougherty, J. F. Tomb, R. D. Fleischmann, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. van Vugt, N. Palmer, M. D. Adams, J. Gocayne, J. C. Venter et al.. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580–586.
   PubMed Web of Science ®Google Scholar
• Friedberg, E. C., G. C. Walker, W. Siede 1995. DNA repair and mutagenesis. ASM Press, Washington, D.C.
   Google Scholar
• Genetics Computer Group. 1994. Program manual for the Wisconsin Package, 8th ed. GCG Inc., Madison, Wis.
   Google Scholar
• Gentil, A., J. B. Cabral-Neto, R. Mariage-Samson, A. Margot, J. L. Imbach, B. Rayner, and J. Sarasin 1992. Mutagenicity of a unique apurinic/apyrimidinic site in mammalian cells. J. Mol. Biol. 227:981–984.
   PubMedGoogle Scholar
• Goffeau, A., B. G. Barrell, H. Bussey, R. W. Davis, B. Dujon, H. Feldmann, F. Galibert, J. D. Hoheisel, C. Jacq, M. Johnston, E. J. Louis, H. W. Mewes, Y. Murakami, P. Philippsen, H. Tettelin, and J. Oliver 1996. Life with 6000 genes. Science 274:546, 563–567.
   PubMed Web of Science ®Google Scholar
• Gorman, M. A., S. Morera, D. G. Rothwell, E. de La Fortelle, C. D. Mol, J. A. Tainer, I. D. Hickson, and J. Freemont 1997. The crystal structure of the human DNA repair endonuclease HAP1 suggests the recognition of extra-helical deoxyribose at DNA abasic sites. EMBO J. 16:6548–6558.
   PubMed Web of Science ®Google Scholar
• Halas, A., H. Baranowska, Z. Policinska, and J. Jachymczyk 1997. Involvement of the REV3 gene in the methylated base-excision repair system. Cooperation of two DNA polymerases, delta and Rev3p, in the repair of MMS-induced lesions in the DNA of Saccharomyces cerevisiae. Curr. Genet. 31:292–301.
   PubMedGoogle Scholar
• Hang, B., B. Singer, G. P. Margison, and J. Elder 1997. Targeted deletion of alkylpurine-DNA-N-glycosylase in mice eliminates repair of 1,N6-ethenoadenine and hypoxanthine but not of 3,N4-ethenocytosine or 8-oxoguanine. Proc. Natl. Acad. Sci. USA 94:12869–12874.
   PubMedGoogle Scholar
• Jelinsky, S. A. Personal communication.
   Google Scholar
• Jelinsky, S. A., and L. D. Samson. Global response of Saccharomyces cerevisiae to an alkylating agent. Proc. Natl. Acad. Sci., in press.
   Google Scholar
• Karahalil, B., T. Roldan-Arjona, and J. Dizdaroglu 1998. Substrate specificity of Schizosaccharomyces pombe Nth protein for products of oxidative DNA damage. Biochemistry 37:590–595.
   PubMed Web of Science ®Google Scholar
• Klenk, H. P., R. A. Clayton, J. F. Tomb, O. White, K. E. Nelson, K. A. Ketchum, R. J. Dodson, M. Gwinn, E. K. Hickey, J. D. Peterson, D. L. Richardson, A. R. Kerlavage, D. E. Graham, N. C. Kyrpides, R. D. Fleischmann, J. Quackenbush, N. H. Lee, G. G. Sutton, S. Gill, E. F. Kirkness, B. A. Dougherty, K. McKenney, M. D. Adams, B. Loftus, J. C. Venter et al.. 1997. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390:364–370.
   PubMed Web of Science ®Google Scholar
• Lindahl, T. 1993. Instability and decay of the primary structure of DNA. Nature 362:709–715.
   PubMed Web of Science ®Google Scholar
• Lindahl, T., P. Karran, and J. Wood 1997. DNA excision repair pathways. Curr. Opin. Genet. Dev. 7:158–169.
   PubMed Web of Science ®Google Scholar
• Ljungquist, S., T. Lindahl, and J. Howard-Flanders 1976. Methyl methane sulfonate-sensitive mutant of Escherichia coli deficient in an endonuclease specific for apurinic sites in deoxyribonucleic acid. J. Bacteriol. 126:646–653.
   PubMed Web of Science ®Google Scholar
• Loeb, L. A., and J. Preston 1986. Mutagenesis by apurinic/apyrimidinic sites. Annu. Rev. Genet. 20:201–230.
   PubMed Web of Science ®Google Scholar
• Masson, J. Y., and J. Ramotar 1997. Normal processing of AP sites in Apn1-deficient Saccharomyces cerevisiae is restored by Escherichia coli genes expressing either exonuclease III or endonuclease III. Mol. Microbiol. 24:711–721.
   PubMedGoogle Scholar
• Masuda, Y., R. A. O. Bennett, and J. Demple 1998. Dynamics of the interaction of human apurinic endonuclease (Ape1) with its substrate and product. J. Biol. Chem. 273:30352–30359.
   PubMedGoogle Scholar
• Masuda, Y., R. A. O. Bennett, and J. Demple 1998. Rapid dissociation of human apurinic endonuclease (Ape1) from incised DNA induced by magnesium. J. Biol. Chem. 273:30360–30365.
   PubMedGoogle Scholar
• Mol, C. D., C. F. Kuo, M. M. Thayer, R. P. Cunningham, and J. Tainer 1995. Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature 374:381–386.
   PubMed Web of Science ®Google Scholar
• Moore, C. W. 1989. Cleavage of cellular and extracellular Saccharomyces cerevisiae DNA by bleomycin and phleomycin. Cancer Res. 49:6935–6940.
   PubMedGoogle Scholar
• Pennisi, E. 1997. Laboratory workhorse decoded. Science 277:1432–1434.
   PubMedGoogle Scholar
• Pierce, M. K., C. N. Giroux, and J. Kunz 1987. Development of a yeast system to assay mutational specificity. Mutat. Res. 182:65–74.
   PubMedGoogle Scholar
• Popoff, S. C., A. I. Spira, A. W. Johnson, and J. Demple 1990. Yeast structural gene (APN1) for the major apurinic endonuclease: homology to Escherichia coli endonuclease IV. Proc. Natl. Acad. Sci. USA 87:4193–4197.
   PubMed Web of Science ®Google Scholar
• Ramotar, D., C. Kim, R. Lillis, and J. Demple 1993. Intracellular localization of the Apn1 DNA repair enzyme of Saccharomyces cerevisiae. Nuclear transport signals and biological role. J. Biol. Chem. 268:20533–20539.
   PubMedGoogle Scholar
• Ramotar, D., S. C. Popoff, and J. Demple 1991. Complementation of DNA repair-deficient Escherichia coli by the yeast Apn1 apurinic/apyrimidinic endonuclease gene. Mol. Microbiol. 5:149–155.
   PubMed Web of Science ®Google Scholar
• Ramotar, D., S. C. Popoff, E. B. Gralla, and J. Demple 1991. Cellular role of yeast Apn1 apurinic endonuclease/3′-diesterase: repair of oxidative and alkylation DNA damage and control of spontaneous mutation. Mol. Cell. Biol. 11:4537–4544.
   PubMed Web of Science ®Google Scholar
• Ramotar, D., J. Vadnais, J. Y. Masson, and J. Tremblay 1998. Schizosaccharomyces pombe apn1 encodes a homologue of the Escherichia coli endonuclease IV family of DNA repair proteins. Biochim. Biophys. Acta 1396:15–20.
   PubMedGoogle Scholar
• Richardson, C., and J. Kornberg 1964. A deoxyribonucleic acid phosphatase-exonuclease from Escherichia coli. I. Purification of the enzyme and characterization of the phosphatase activity. J. Biol. Chem. 239:242–250.
   PubMed Web of Science ®Google Scholar
• Robson, C. N., and J. Hickson 1991. Isolation of cDNA clones encoding a human apurinic/apyrimidinic endonuclease that corrects DNA repair and mutagenesis defects in E. coli xth (exonuclease III) mutants. Nucleic Acids Res. 19:5519–5523.
   PubMed Web of Science ®Google Scholar
• Roldan-Arjona, T., C. Anselmino, and J. Lindahl 1996. Molecular cloning and functional analysis of a Schizosaccharomyces pombe homologue of Escherichia coli endonuclease III. Nucleic Acids Res. 24:3307–3312.
   PubMed Web of Science ®Google Scholar
• Sander, M., and J. Ramotar 1997. Partial purification of Pde1 from Saccharomyces cerevisiae: enzymatic redundancy for the repair of 3′-terminal DNA lesions and abasic sites in yeast. Biochemistry 36:6100–6106.
   PubMedGoogle Scholar
• Schiestl, R. H., and J. Gietz 1989. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16:339–346.
   PubMed Web of Science ®Google Scholar
• Schmitt, M. E., T. A. Brown, and J. Trumpower 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 18:3091–3092.
   PubMed Web of Science ®Google Scholar
• Seeberg, E., L. Eide, and J. Bjoras 1995. The base excision repair pathway. Trends Biochem. Sci. 20:391–397.
   PubMedGoogle Scholar
• Seki, S., M. Hatsushika, S. Watanabe, K. Akiyama, K. Nagao, and J. Tsutsui 1992. cDNA cloning, sequencing, expression and possible domain structure of human APEX nuclease homologous to Escherichia coli exonuclease III. Biochim. Biophys. Acta 1131:287–299.
   PubMedGoogle Scholar
• Smith, D. R., L. A. Doucette-Stamm, C. Deloughery, H. Lee, J. Dubois, T. Aldredge, R. Bashirzadeh, D. Blakely, R. Cook, K. Gilbert, D. Harrison, L. Hoang, P. Keagle, W. Lumm, B. Pothier, D. Qiu, R. Spadafora, R. Vicaire, Y. Wang, J. Wierzbowski, R. Gibson, N. Jiwani, A. Caruso, D. Bush, J. N. Reeve et al.. 1997. Complete genome sequence of Methanobacterium thermoautotrophicum ΔH: functional analysis and comparative genomics. J. Bacteriol. 179:7135–7155.
   PubMed Web of Science ®Google Scholar
• Srivastava, D. K., B. J. Vandeberg, R. Prasad, J. T. Molina, W. A. Beard, A. E. Tomkinson, and J. Wilson 1998. Mammalian abasic site base excision repair—identification of the reaction sequence and rate-determining steps. J. Biol. Chem. 273:21203–21209.
   PubMed Web of Science ®Google Scholar
• Takeuchi, M., R. Lillis, B. Demple, and J. Takeshita 1994. Interactions of Escherichia coli endonuclease IV and exonuclease III with abasic sites in DNA. J. Biol. Chem. 269:21907–21914.
   PubMed Web of Science ®Google Scholar
• Taylor, A. F., and J. Weiss 1982. Role of exonuclease III in the base excision repair of uracil-containing DNA. J. Bacteriol. 151:351–357.
   PubMedGoogle Scholar
• Von Borstel, R. C. 1978. Measuring spontaneous mutation rates in yeast. Methods Cell Biol. 20:1–24.
   PubMedGoogle Scholar
• Weiss, B. 1976. Endonuclease II of Escherichia coli is exonuclease III. J. Biol. Chem. 251:1896–1901.
   PubMed Web of Science ®Google Scholar
• Wilson, D. M. III, R. A. O. Bennett, J. C. Marquis, P. Ansari, and J. Demple 1995. Trans-complementation by human apurinic endonuclease (Ape) of hypersensitivity to DNA damage and spontaneous mutator phenotype in apn1−yeast. Nucleic Acids Res. 23:5027–5033.
   PubMedGoogle Scholar
• Xu, Y.-J., E. Y. Kim, and J. Demple 1998. Excision of C4′-oxidized deoxyribose lesions from double-stranded DNA by human AP endonuclease (Ape1 protein) and DNA polymerase β. J. Biol. Chem. 273:28837–28844.
   PubMedGoogle Scholar
• Yamamoto, K., and J. Hutchinson 1979. Response to bleomycin of E. coli mutants deficient in DNA repair. J. Antibiot. (Tokyo) 32:1181.
   PubMedGoogle Scholar