Chronic Oxidative DNA Damage Due to DNA Repair Defects Causes Chromosomal Instability in Saccharomyces cerevisiae

REFERENCES

• Admire, A., L. Shanks, N. Danzl, M. Wang, U. Weier, W. Stevens, E. Hunt, and T. Weinert. 2006. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes Dev. 20:159–173.
   PubMed Web of Science ®Google Scholar
• Al-Tassan, N., N. H. Chmiel, J. Maynard, N. Fleming, A. L. Livingston, G. T. Williams, A. K. Hodges, D. R. Davies, S. S. David, J. R. Sampson, and J. P. Cheadle. 2002. Inherited variants of MYH associated with somatic G:C→T:A mutations in colorectal tumors. Nat. Genet. 30:227–232.
   PubMed Web of Science ®Google Scholar
• Augeri, L., Y. M. Lee, A. B. Barton, and P. W. Doetsch. 1997. Purification, characterization, gene cloning, and expression of Saccharomyces cerevisiae redoxyendonuclease, a homolog of Escherichia coli endonuclease III. Biochemistry 36:721–729.
   PubMed Web of Science ®Google Scholar
• Bach, M. L., F. Lacroute, and D. Botstein. 1979. Evidence for transcriptional regulation of orotidine-5′-phosphate decarboxylase in yeast by hybridization of mRNA to the yeast structural gene cloned in Escherichia coli. Proc. Natl. Acad. Sci. USA 76:386–390.
   PubMedGoogle Scholar
• Balakumaran, B. S., C. H. Freudenreich, and V. A. Zakian. 2000. CGG/CCG repeats exhibit orientation-dependent instability and orientation-independent fragility in Saccharomyces cerevisiae. Hum. Mol. Genet. 9:93–100.
   PubMed Web of Science ®Google Scholar
• Boiteux, S., and M. Guillet. 2004. Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae. DNA Repair (Amsterdam) 3:1–12.
   PubMed Web of Science ®Google Scholar
• Budanov, A. V., A. A. Sablina, E. Feinstein, E. V. Koonin, and P. M. Chumakov. 2004. Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304:596–600.
   PubMed Web of Science ®Google Scholar
• Cheadle, J. P., M. Krawczak, M. W. Thomas, A. K. Hodges, N. Al-Tassan, N. Fleming, and J. R. Sampson. 2002. Different combinations of biallelic APC mutation confer different growth advantages in colorectal tumours. Cancer Res. 62:363–366.
   PubMedGoogle Scholar
• Chen, C., and R. D. Kolodner. 1999. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat. Genet. 23:81–85.
   PubMed Web of Science ®Google Scholar
• Coussens, L. M., and Z. Werb. 2002. Inflammation and cancer. Nature 420:860–867.
   PubMed Web of Science ®Google Scholar
• Debrauwere, H., J. Buard, J. Tessier, D. Aubert, G. Vergnaud, and A. Nicolas. 1999. Meiotic instability of human minisatellite CEB1 in yeast requires DNA double-strand breaks. Nat. Genet. 23:367–371.
   PubMedGoogle Scholar
• Debrauwere, H., S. Loeillet, W. Lin, J. Lopes, and A. Nicolas. 2001. Links between replication and recombination in Saccharomyces cerevisiae: a hypersensitive requirement for homologous recombination in the absence of Rad27 activity. Proc. Natl. Acad. Sci. USA 98:8263–8269.
   PubMedGoogle Scholar
• de Lange, T. 2005. Telomere-related genome instability in cancer. Cold Spring Harbor Symp. Quant. Biol. 70:197–204.
   PubMedGoogle Scholar
• Doetsch, P. W., N. J. Morey, R. L. Swanson, and S. Jinks-Robertson. 2001. Yeast base excision repair: interconnections and networks. Prog. Nucleic Acid Res. Mol. Biol. 68:29–39.
   PubMedGoogle Scholar
• Draviam, V. M., S. Xie, and P. K. Sorger. 2004. Chromosome segregation and genomic stability. Curr. Opin. Genet. Dev. 14:120–125.
   PubMed Web of Science ®Google Scholar
• Evert, B. A., T. B. Salmon, B. Song, L. Jingjing, W. Siede, and P. W. Doetsch. 2004. Spontaneous DNA damage in Saccharomyces cerevisiae elicits phenotypic properties similar to cancer cells. J. Biol. Chem. 279:22585–22594.
   PubMed Web of Science ®Google Scholar
• Frosina, G. 2004. Commentary: DNA base excision repair defects in human pathologies. Free Radic. Res. 38:1037–1054.
   PubMed Web of Science ®Google Scholar
• Fruehauf, J. P., and F. L. Meyskens, Jr. 2007. Reactive oxygen species: a breath of life or death? Clin. Cancer Res. 13:789–794.
   PubMed Web of Science ®Google Scholar
• Goebl, M. G., and T. D. Petes. 1986. Most of the yeast genomic sequences are not essential for cell growth and division. Cell 46:983–992.
   PubMed Web of Science ®Google Scholar
• Goldstein, A. L., and J. H. McCusker. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15:1541–1553.
   PubMed Web of Science ®Google Scholar
• Gordenin, D. A., and M. A. Resnick. 1998. Yeast ARMs (DNA at-risk motifs) can reveal sources of genome instability. Mutat. Res. 400:45–58.
   PubMed Web of Science ®Google Scholar
• Haber, J. E., and M. Debatisse. 2006. Gene amplification: yeast takes a turn. Cell 125:1237–1240.
   PubMedGoogle Scholar
• Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100:57–70.
   PubMed Web of Science ®Google Scholar
• Huang, M. E., and R. D. Kolodner. 2005. A biological network in Saccharomyces cerevisiae prevents the deleterious effects of endogenous oxidative DNA damage. Mol. Cell 17:709–720.
   PubMedGoogle Scholar
• Hussain, S. P., L. J. Hofseth, and C. C. Harris. 2003. Radical causes of cancer. Nat. Rev. Cancer 3:276–285.
   PubMed Web of Science ®Google Scholar
• Jallepalli, P. V., and C. Lengauer. 2001. Chromosome segregation and cancer: cutting through the mystery. Nat. Rev. Cancer 1:109–117.
   PubMed Web of Science ®Google Scholar
• Jin, Y. H., R. Obert, P. M. Burgers, T. A. Kunkel, M. A. Resnick, and D. A. Gordenin. 2001. The 3′→5′ exonuclease of DNA polymerase delta can substitute for the 5′ flap endonuclease Rad27/Fen1 in processing Okazaki fragments and preventing genome instability. Proc. Natl. Acad. Sci. USA 98:5122–5127.
   PubMedGoogle Scholar
• Kokoska, R. J., L. Stefanovic, J. DeMai, and T. D. Petes. 2000. Increased rates of genomic deletions generated by mutations in the yeast gene encoding DNA polymerase delta or by decreases in the cellular levels of DNA polymerase delta. Mol. Cell. Biol. 20:7490–7504.
   PubMedGoogle Scholar
• Kolodner, R. D., C. D. Putnam, and K. Myung. 2002. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297:552–557.
   PubMed Web of Science ®Google Scholar
• Kopnin, P. B., L. S. Agapova, B. P. Kopnin, and P. M. Chumakov. 2007. Repression of sestrin family genes contributes to oncogenic Ras-induced reactive oxygen species up-regulation and genetic instability. Cancer Res. 67:4671–4678.
   PubMedGoogle Scholar
• Lemoine, F. J., N. P. Degtyareva, K. Lobachev, and T. D. Petes. 2005. Chromosomal translocations in yeast induced by low levels of DNA polymerase: a model for chromosome fragile sites. Cell 120:587–598.
   PubMed Web of Science ®Google Scholar
• Lengauer, C., K. W. Kinzler, and B. Vogelstein. 1998. Genetic instabilities in human cancers. Nature 396:643–649.
   PubMed Web of Science ®Google Scholar
• Libuda, D. E., and F. Winston. 2006. Amplification of histone genes by circular chromosome formation in Saccharomyces cerevisiae. Nature 443:1003–1007.
   PubMedGoogle Scholar
• Lindahl, T. 1993. Instability and decay of the primary structure of DNA. Nature 362:709–715.
   PubMed Web of Science ®Google Scholar
• Lobachev, K. S., A. Rattray, and V. Narayanan. 2007. Hairpin- and cruciform-mediated chromosome breakage: causes and consequences in eukaryotic cells. Front. Biosci. 12:4208–4220.
   PubMed Web of Science ®Google Scholar
• McMurray, M. A., and D. E. Gottschling. 2004. Aging and genetic instability in yeast. Curr. Opin. Microbiol. 7:673–679.
   PubMedGoogle Scholar
• Michor, F., Y. Iwasa, B. Vogelstein, C. Lengauer, and M. A. Nowak. 2005. Can chromosomal instability initiate tumorigenesis? Semin. Cancer Biol. 15:43–49.
   PubMedGoogle Scholar
• Mieczkowski, P. A., F. J. Lemoine, and T. D. Petes. 2006. Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair (Amsterdam) 5:1010–1020.
   PubMedGoogle Scholar
• Mortimer, R. K., and J. R. Johnston. 1986. Genealogy of principal strains of the yeast genetic stock center. Genetics 113:35–43.
   PubMed Web of Science ®Google Scholar
• Narayanan, V., P. A. Mieczkowski, H. M. Kim, T. D. Petes, and K. S. Lobachev. 2006. The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell 125:1283–1296.
   PubMed Web of Science ®Google Scholar
• Park, S. G., M. K. Cha, W. Jeong, and I. H. Kim. 2000. Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J. Biol. Chem. 275:5723–5732.
   PubMed Web of Science ®Google Scholar
• Pinkel, D., and D. G. Albertson. 2005. Comparative genomic hybridization. Annu. Rev. Genomics Hum. Genet. 6:331–354.
   PubMed Web of Science ®Google Scholar
• Popoff, S. C., A. I. Spira, A. W. Johnson, and B. 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
• Ragu, S., G. Faye, I. Iraqui, A. Masurel-Heneman, R. D. Kolodner, and M. E. Huang. 2007. Oxygen metabolism and reactive oxygen species cause chromosomal rearrangements and cell death. Proc. Natl. Acad. Sci. USA 104:9747–9752.
   PubMed Web of Science ®Google Scholar
• Rajagopalan, H., M. A. Nowak, B. Vogelstein, and C. Lengauer. 2003. The significance of unstable chromosomes in colorectal cancer. Nat. Rev. Cancer 3:695–701.
   PubMed Web of Science ®Google Scholar
• Reitmair, A. H., R. Risley, R. G. Bristow, T. Wilson, A. Ganesh, A. Jang, J. Peacock, S. Benchimol, R. P. Hill, T. W. Mak, R. Fishel, and M. Meuth. 1997. Mutator phenotype in Msh2-deficient murine embryonic fibroblasts. Cancer Res. 57:3765–3771.
   PubMedGoogle Scholar
• Salmon, T. B., B. A. Evert, B. Song, and P. W. Doetsch. 2004. Biological consequences of oxidative stress-induced DNA damage in Saccharomyces cerevisiae. Nucleic Acids Res. 32:3712–3723.
   PubMed Web of Science ®Google Scholar
• Shih, I. M., W. Zhou, S. N. Goodman, C. Lengauer, K. W. Kinzler, and B. Vogelstein. 2001. Evidence that genetic instability occurs at an early stage of colorectal tumorigenesis. Cancer Res. 61:818–822.
   PubMed Web of Science ®Google Scholar
• Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Spencer, F., S. L. Gerring, C. Connelly, and P. Hieter. 1990. Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124:237–249.
   PubMed Web of Science ®Google Scholar
• Swanson, R. L., N. J. Morey, P. W. Doetsch, and S. Jinks-Robertson. 1999. Overlapping specificities of base excision repair, nucleotide excision repair, recombination, and translesion synthesis pathways for DNA base damage in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:2929–2935.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Szatrowski, T. P., and C. F. Nathan. 1991. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 51:794–798.
   PubMed Web of Science ®Google Scholar
• Vafa, O., M. Wade, S. Kern, M. Beeche, T. K. Pandita, G. M. Hampton, and G. M. Wahl. 2002. c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol. Cell 9:1031–1044.
   PubMed Web of Science ®Google Scholar
• van Steensel, B., A. Smogorzewska, and T. de Lange. 1998. TRF2 protects human telomeres from end-to-end fusions. Cell 92:401–413.
   PubMed Web of Science ®Google Scholar
• Wach, A., A. Brachat, R. Pohlmann, and P. Philippsen. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10:1793–1808.
   PubMed Web of Science ®Google Scholar
• Weinstock, D. M., C. A. Richardson, B. Elliott, and M. Jasin. 2006. Modeling oncogenic translocations: distinct roles for double-strand break repair pathways in translocation formation in mammalian cells. DNA Repair (Amsterdam) 5:1065–1074.
   PubMed Web of Science ®Google Scholar
• Wong, C. M., K. L. Siu, and D. Y. Jin. 2004. Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and are genomically unstable. J. Biol. Chem. 279:23207–23213.
   PubMedGoogle Scholar
• You, H. J., R. L. Swanson, C. Harrington, A. H. Corbett, S. Jinks-Robertson, S. Senturker, S. S. Wallace, S. Boiteux, M. Dizdaroglu, and P. W. Doetsch. 1999. Saccharomyces cerevisiae Ntg1p and Ntg2p: broad specificity N-glycosylases for the repair of oxidative DNA damage in the nucleus and mitochondria. Biochemistry 38:11298–11306.
   PubMed Web of Science ®Google Scholar