Altered Replication and Inverted Repeats Induce Mismatch Repair-Independent Recombination between Highly Diverged DNAs in Yeast

REFERENCES

• Abastado, J.-P., B. Cami, T. H. Dinh, J. Igolen, and P. Kourilsky. 1984. Processing of complex heteroduplexes in Escherichia coli and Cos-1 monkey cells. Proc. Natl. Acad. Sci. USA 81:5792–5796.
   PubMedGoogle Scholar
• Abastado, J.-P., S. Darche, F. Godeau, B. Cami, and P. Kourilsky. 1987. Intramolecular recombination between partially homologous sequences in Escherichia coli and Xenopus laevis oocytes. Proc. Natl. Acad. Sci. USA 84:6496–6500.
   PubMedGoogle Scholar
• Aguilera, A., and H. L. Klein. 1988. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic characterization of hyper-recombination mutations. Genetics 119:779–790.
   PubMed Web of Science ®Google Scholar
• Alani, E., N.-W. Chi, and R. D. Kolodner. 1995. The Saccharomyces cerevisiae Msh2 protein specifically binds to duplex oligonucleotides containing mismatched DNA base pairs and insertions. Genes Dev. 9:234–247.
   PubMedGoogle Scholar
• Alani, E., R. A. G. Reenan, and R. D. Kolodner. 1994. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics 173:19–39.
   Google Scholar
• Baker, S. M., C. E. Bronner, L. Zang, A. W. Plug, M. Robatzek, G. Warren, E. A. Elliott, J. Yu, T. Ashley, N. Arnheim, R. A. Flavell, and R. M. Liskay. 1995. Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis. Cell 82:309–319.
   PubMed Web of Science ®Google Scholar
• Berg, D. E., C. Egner, and J. B. Lowe. 1983. Mechanism of F factor-enhanced excision of Tn5. Gene 22:1–7.
   PubMedGoogle Scholar
• Bi, X., and L. F. Liu. 1996. DNA rearrangement mediated by inverted repeats. Proc. Natl. Acad. Sci. USA 93:819–823.
   PubMedGoogle Scholar
• Bierne, H., and B. Michel. 1994. When replication folk stops. Mol. Microbiol. 13:17–23.
   PubMedGoogle Scholar
• Boeke, J. D., F. LaCroute, and G. R. Fink. 1984. A positive selection for mutants lacking orotidine-5-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345–346.
   PubMedGoogle Scholar
• Brosius, J., and S. J. Gould. 1992. On “genomenclature”: a comprehensive (and respectful) taxonomy for pseudogenes and other “junk DNA”. Proc. Natl. Acad. Sci. USA 89:10706–10710.
   PubMed Web of Science ®Google Scholar
• Cami, B., P. Chambon, and P. Kourilsky. 1984. Correction of complex heteroduplexes made of mouse H-2 gene sequences in Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 81:503–507.
   PubMedGoogle Scholar
• Canceill, D., and S. D. Ehrlich. 1996. Copy-choice recombination mediated by DNA polymerase III holoenzyme from Escherichia coli. Proc. Natl. Acad. Sci. USA 93:6647–6652.
   PubMedGoogle Scholar
• Celniker, S. E., K. Sweder, F. Srienc, J. E. Bailey, and J. L. Campbell. 1984. Deletion mutation affecting autonomously replicating sequence ARS1 of Saccharomyces cerevisiae. Mol. Cell. Biol. 4:2455–2466.
   PubMedGoogle Scholar
• Chiu, S. K., B. J. Rao, R. M. Story, and C. M. Radding. 1993. Interactions of three strands in joints made by RecA protein. Biochemistry 32:13146–13155.
   PubMed Web of Science ®Google Scholar
• Collick, A., J. Drew, J. Penberth, P. Bois, J. Luckett, F. Scaerou, A. Jeffreys, and W. Reik. 1996. Instability of long inverted repeats within mouse transgenes. EMBO J. 15:1163–1171.
   PubMedGoogle Scholar
• Collins, J. 1980. The instability of palindromic DNA. Cold Spring Harbor Symp. Quant. Biol. 45:409–416.
   Google Scholar
• Collins, J., G. Volckaert, and P. Nevers. 1982. Precise and nearly precise excision of the symmetrical inverted repeats of Tn5: common features of recA-independent deletion events in E. coli. Gene 19:139–146.
   PubMedGoogle Scholar
• Cunningham, R. P., A. M. Wu, T. Shibata, C. DasGupta, and C. M. Radding. 1981. Homologous pairing and topological linkage of DNA molecules by combined action of E. coli RecA protein and topoisomerase I. Cell 24:213–223.
   PubMed Web of Science ®Google Scholar
• d’Alencon, E., M. Petranovic, B. Michel, P. Noirot, A. Aucouturier, M. Uzest, and S. D. Ehrlich. 1994. Copy-choice illegitimate DNA recombination revisited. EMBO J. 13:2725–2734.
   PubMedGoogle Scholar
• Datta, A., A. Adouda, L. New, G. Crouse, and S. Jinks-Robertson. 1996. Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:1085–1093.
   PubMed Web of Science ®Google Scholar
• de Wind, N., M. Dekker, A. Berns, M. Radman, and H. te Riele. 1995. Inactivation of the mouse MSH2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell 82:321–330.
   PubMed Web of Science ®Google Scholar
• Ehrlich, D. S. 1989. Illegitimate recombination in bacteria, p. 799–832. In D. E. Berg and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
   Google Scholar
• Feinstein, S. I., and J. A. Low. 1986. Hyper-recombining recipient strains in bacterial conjugation. Genetics 113:13–33.
   PubMedGoogle Scholar
• Fishel, R., A. Ewel, A. Lee, M. K. Lescoe, and J. Griffith. 1994. Binding of mismatched microsatellite DNA sequences by the human Msh2 protein. Science 266:1403–1405.
   PubMed Web of Science ®Google Scholar
• Fishman-Lobell, J., and J. E. Haber. 1992. Removal of nonhomologous DNA ends in double-strand break recombination—the role of the yeast ultraviolet repair gene RAD1. Science 258:480–484.
   PubMedGoogle Scholar
• Formosa, T., and B. Alberts. 1986. DNA synthesis dependent on genetic recombination: characterization of a reaction catalyzed by purified bacteriophage T4 proteins. Cell 47:793–806.
   PubMed Web of Science ®Google Scholar
• Gordenin, D. A., K. S. Lobachov, N. P. Degtyareva, A. L. Malkova, E. Perkins, and M. A. Resnick. 1993. Inverted DNA repeats: a source of eucaryotic genomic instability. Mol. Cell. Biol. 13:5315–5322.
   PubMedGoogle Scholar
• Gordenin, D. A., A. L. Malkova, A. Peterzen, V. N. Kulikov, Y. I. Pavlov, E. Perkins, and M. A. Resnick. 1992. Transposon Tn5 excision in yeast: the influence of DNA polymerases alpha, delta, epsilon and repair genes. Proc. Natl. Acad. Sci. USA 89:3785–3789.
   PubMedGoogle Scholar
• Gordenin, D. A., Y. Y. Proscyavichus, A. L. Malkova, M. V. Trofimova, and A. Peterzen. 1991. Yeast mutants with increased transposon Tn5 excision. Yeast 7:37–50.
   PubMedGoogle Scholar
• Henderson, S. T., and T. D. Petes. 1993. Instability of a plasmid borne inverted repeat in Saccharomyces cerevisiae. Genetics 133:57–62.
   Google Scholar
• Humbert, O., M. Prudhomme, R. Hakenbeck, C. G. Dowson, and J. P. Claverys. 1995. Homeologous recombination and mismatch repair during transformation in Streptococcus pneumoniae: saturation of the Hex mismatch repair system. Proc. Natl. Acad. Sci. USA 92:9052–9056.
   PubMedGoogle Scholar
• Larionov, V., N. Kouprina, M. Eldarov, E. Perkins, G. Porter, and M. A. Resnick. 1994. Transformation-associated recombination between diverged and homologous DNA repeats is induced by strand breaks. Yeast 10:93–104.
   PubMed Web of Science ®Google Scholar
• Matic, I., C. Rayssiguier, and M. Radman. 1995. Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell 80:507–515.
   PubMedGoogle Scholar
• Mezard, C., and A. Nicolas. 1994. Homologous, homeologous, and illegitimate repair of double-strand breaks during transformation of a wild-type strain and a rad52 mutant strain of Saccharomyces cerevisiae. Mol. Cell. Biol. 14:1278–1292.
   PubMedGoogle Scholar
• Mezard, C., D. Pompon, and A. Nicolas. 1992. Recombination between similar but not identical DNA sequences during yeast transformation occurs within short stretches of identity. Cell 70:659–670.
   PubMed Web of Science ®Google Scholar
• Modrich, P., and R. Lahue. 1996. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu. Rev. Biochem. 65:101–133.
   PubMed Web of Science ®Google Scholar
• Morrison, A., A. L. Johnston, L. H. Johnston, and A. Sugino. 1993. Pathway correcting DNA replication errors in S. cerevisiae. EMBO J. 12:1467–1473.
   PubMed Web of Science ®Google Scholar
• Nowak, R. 1994. Mining treasures from “junk DNA”. Science 263:608–610.
   PubMed Web of Science ®Google Scholar
• Parker, B. O., and M. G. Marinus. 1992. Repair of DNA heteroduplexes containing small heterologous sequences in E. coli. Proc. Natl. Acad. Sci. USA 89:1730–1734.
   PubMed Web of Science ®Google Scholar
• Petit, M. A., J. Dimpfl, M. Radman, and H. Echols. 1991. Control of large chromosomal duplications in Escherichia coli by the mismatch repair system. Genetics 129:327–332.
   PubMedGoogle Scholar
• Porter, G., J. Westmoreland, S. Priebe, and M. A. Resnick. 1996. Homologous and homeologous intermolecular gene conversion are not differentially affected by mutations in the DNA damage or the mismatch repair genes RAD1, RAD50, RAD51, RAD52, RAD54, PMS1 and MSH2. Genetics 143:755–767.
   PubMedGoogle Scholar
• Priebe, S. D., J. Westmoreland, T. Nilsson-Tillgren, and M. A. Resnick. 1994. Induction of recombination between homologous and diverged DNAs by double-strand gaps and breaks and role of mismatch repair. Mol. Cell. Biol. 14:4802–4814.
   PubMedGoogle Scholar
• Rayssiguier, C., D. S. Thaler, and M. Radman. 1989. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342:396–401.
   PubMed Web of Science ®Google Scholar
• Resnick, M. A. 1976. The repair of double-strand breaks in DNA: a model involving recombination. J. Theor. Biol. 59:97–106.
   PubMed Web of Science ®Google Scholar
• Rothstein, R. J. 1983. One-step gene disruption in yeast. Methods Enzymol. 101:202–210.
   PubMed Web of Science ®Google Scholar
• Ruskin, B., and G. R. Fink. 1993. Mutations in POL1 increase the mitotic instability of tandem inverted repeats in Saccharomyces cerevisiae. Genetics 133:43–56.
   Google Scholar
• Selva, E. M., L. New, G. F. Crouse, and R. Lahue. 1995. Mismatch correction acts as a barrier to homeologous recombination in S. cerevisiae. Genetics 139:1175–1188.
   PubMed Web of Science ®Google Scholar
• Shen, P., and H. V. Huang. 1989. Effect of base pair mismatches on recombination via the RecBCD pathway. Mol. Gen. Genet. 218:358–360.
   PubMedGoogle Scholar
• Sherman, F., G. F. Fink, and J. B. Hicks. 1986. Methods in yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Sinden, R. R. 1994. DNA structure and function. Academic Press, Inc., San Diego, Calif.
   Google Scholar
• Stotz, A., and P. Linder. 1990. The ADE2 gene from Saccharomyces cerevisiae: sequence and new vectors. Gene 95:91–98.
   PubMedGoogle Scholar
• Strand, M., T. A. Prolla, R. M. Liskay, and T. D. Petes. 1993. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365:274–276.
   PubMed Web of Science ®Google Scholar
• Tran, H. T., N. P. Degtyareva, N. N. Koloteva, A. Sugino, H. Masumoto, D. A. Gordenin, and M. A. Resnick. 1995. Replication slippage between distant short repeats in Saccharomyces cerevisiae depends on the direction of replication and the RAD50 and RAD52 genes. Mol. Cell. Biol. 15:5607–5617.
   PubMedGoogle Scholar
• Tran, H. T., D. A. Gordenin, and M. A. Resnick. 1996. The prevention of repeat-associated deletions in Saccharomyces cerevisiae by mismatch repair depends on size and origin of deletions. Genetics 143:1579–1587.
   PubMedGoogle Scholar
• Tran, H. T., V. N. Kulikov, V. N. Noskov, G. I. Sizonenko, Y. O. Chernoff, and Y. I. Pavlov. 1993. The 5′-aminoimidazole ribonucleotide-carboxylase structural gene of methylotrophic yeast Pichia methanolica: cloning, sequencing and homology analysis. Yeast 9:1251–1258.
   PubMedGoogle Scholar
• Westmoreland, J., G. Porter, M. Radman, and M. A. Resnick. Highly mismatched molecules resembling recombination intermediates efficiently transform mismatch repair proficient E. coli. Genetics, in press.
   Google Scholar
• Worth, L., S. Clark, M. Radman, and P. Modrich. 1994. Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs. Proc. Natl. Acad. Sci. USA 91:3238–3241.
   PubMedGoogle Scholar
• Zahrt, T. C., G. C. Mora, and S. Maloy. 1994. Inactivation of mismatch repair overcomes the barrier to transduction between Salmonella typhimurium and Salmonella typhi. J. Bacteriol. 176:1527–1529.
   PubMedGoogle Scholar