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DNA Dynamics and Chromosome Structure

Saccharomyces cerevisiae Flap Endonuclease 1 Uses Flap Equilibration To Maintain Triplet Repeat Stability

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Pages 4049-4064 | Received 13 Nov 2003, Accepted 09 Feb 2004, Published online: 27 Mar 2023

REFERENCES

  • Ayyagari, R., Gomes X. V., Gordenin D. A., and Burgers P. M.. 2003. Okazaki fragment maturation in yeast. I. Distribution of functions between FEN1 and DNA2. J. Biol. Chem. 278:1618–1625.
  • Bae, S. H., Kim D. W., Kim J., Kim J. H., Kim D. H., Kim H. D., Kang H. Y., and Seo Y. S.. 2002. Coupling of DNA helicase and endonuclease activities of yeast Dna2 facilitates Okazaki fragment processing. J. Biol. Chem. 277:26632–26641.
  • Balakumaran, B. S., Freudenreich C. H., and Zakian V. A.. 2000. CGG/CCG repeats exhibit orientation-dependent instability and orientation-independent fragility in Saccharomyces cerevisiae. Hum. Mol. Genet. 9:93–100.
  • Brosh, R. J., Driscoll H., Dianov G., and Sommers J.. 2002. Biochemical characterization of the WRN-FEN-1 functional interaction. Biochemistry 41:12204–12216.
  • Brosh, R. J., von Kobbe C., Sommers J., Karmakar P., Opresko P., Piotrowski J., Dianova I., Dianov G., and Bohr V.. 2001. Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity. EMBO J. 20:5791–5801.
  • Budd, M. E., and Campbell J. L.. 2000. The pattern of sensitivity of yeast dna2 mutants to DNA damaging agents suggests a role in DSB and postreplication repair pathways. Mutat. Res. 459:173–186.
  • Budd, M. E., and Campbell J. L.. 1995. A yeast gene required for DNA replication encodes a protein with homology to DNA helicases. Proc. Natl. Acad. Sci. USA 92:7642–7646.
  • Callahan, J. L., Andrews K. J., Zakian V. A., and Freudenreich C. H.. 2003. Mutations in yeast replication proteins that increase CAG/CTG expansions also increase repeat fragility. Mol. Cell. Biol. 23:7849–7860.
  • Ceska, T. A., Sayers J. R., Stier G., and Suck D.. 1996. A helical arch allowing single-stranded DNA to thread through T5 5′-exonuclease. Nature 382:90–93.
  • Culotti, J., and Hartwell L. H.. 1971. Genetic control of the cell division cycle in yeast. 3. Seven genes controlling nuclear division. Exp. Cell Res. 67:389–401.
  • Debrauwere, H., Loeillet S., Lin W., Lopes J., and Nicolas A.. 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.
  • DeMott, M. S., Shen B., Park M. S., Bambara R. A., and Zigman S.. 1996. Human RAD2 homolog 1 5′- to 3′-exo/endonuclease can efficiently excise a displaced DNA fragment containing a 5′-terminal abasic lesion by endonuclease activity. J. Biol. Chem. 271:30068–30076.
  • Dervan, J., Feng M., Patel D., Grasby J., Artymiuk P., Ceska T., and Sayers J.. 2002. Interactions of mutant and wild-type flap endonucleases with oligonucleotide substrates suggest an alternative model of DNA binding. Proc. Natl. Acad. Sci. USA 99:8542–8547.
  • Dutcher, S. K. 1981. Internuclear transfer of genetic information in kar1-1/KAR1 heterokaryons in Saccharomyces cerevisiae. Mol. Cell. Biol. 1:245–253.
  • Freudenreich, C. H., Kantrow S. M., and Zakian V. A.. 1998. Expansion and length-dependent fragility of CTG repeats in yeast. Science 279:853–856.
  • Freudenreich, C. H., Stavenhagen J. B., and Zakian V. A.. 1997. Stability of a CTG/CAG trinucleotide repeat in yeast is dependent on its orientation in the genome. Mol. Cell. Biol. 17:2090–2098.
  • Gacy, A. M., Goellner G., Juranic N., Macura S., and McMurray C. T.. 1995. Trinucleotide repeats that expand in human disease form hairpin structures in vitro. Cell 81:533–540.
  • Gangloff, S., McDonald J. P., Bendixen C., Arthur L., and Rothstein R.. 1994. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14:8391–8398.
  • Gordenin, D. A., Kunkel T. A., and Resnick M. A.. 1997. Repeat expansion-all in a flap? Nat. Genet. 16:116–118.
  • Harrington, J. J., and Lieber M. R.. 1994. The characterization of a mammalian DNA structure-specific endonuclease. EMBO J. 13:1235–1246.
  • Henricksen, L., Veeraraghavan J., Chafin D. R., and Bambara R. A.. 2002. DNA ligase I competes with FEN1 to expand repetitive DNA sequences in vitro. J. Biol. Chem. 277:22361–22369.
  • Henricksen, L. A., Tom S., Liu Y., and Bambara R. A.. 2000. Inhibition of flap endonuclease 1 by flap secondary structure and relevance to repeat sequence expansion. J. Biol. Chem. 275:16420–16427.
  • Hosfield, D. J., Mol C. D., Shen B., and Tainer J. A.. 1998. Structure of the DNA repair and replication endonuclease and exonuclease FEN-1: coupling DNA and PCNA binding to FEN-1 activity. Cell 95:135–146.
  • Hwang, K. Y., Baek K., Kim H. Y., and Cho Y.. 1998. The crystal structure of flap endonuclease-1 from Methanococcus jannaschii. Nat. Struct. Biol. 5:707–713.
  • Jankowski, C., Nasar F., and Nag D. K.. 2000. Meiotic instability of CAG repeat tracts occurs by double-strand break repair in yeast. Proc. Natl. Acad. Sci. USA 97:2134–2139.
  • Jin, Y. H., Ayyagari R., Resnick M. A., Gordenin D. A., and Burgers P. M.. 2003. Okazaki fragment maturation in yeast. II. Cooperation between the polymerase and 3′-5′-exonuclease activities of Pol delta in the creation of a ligatable nick. J. Biol. Chem. 278:1626–1633.
  • Johnson, R. E., Kovvali G. K., Prakash L., and Prakash S.. 1995. Requirement of the yeast RTH1 5′ to 3′ exonuclease for the stability of simple repetitive DNA. Science 269:238–240.
  • Kao, H. I., Henricksen L. A., Liu Y., and Bambara R. A.. 2002. Cleavage specificity of Saccharomyces cerevisiae flap endonuclease 1 suggests a double-flap structure as the cellular substrate. J. Biol. Chem. 277:14379–14389.
  • Kokoska, R. J., Stefanovic L., Tran H. T., Resnick M. A., Gordenin D. A., and Petes T. D.. 1998. Destabilization of yeast micro- and minisatellite DNA sequences by mutations affecting a nuclease involved in Okazaki fragment processing (rad27) and DNA polymerase δ (pol3-t). Mol. Cell. Biol. 18:2779–2788.
  • Kucherlapati, M., Yang K., Kuraguchi M., Zhao J., Lia M., Heyer J., Kane M., Fan K., Russell R., Brown A., Kneitz B., Edelmann W., Kolodner R., Lipkin M., and Kucherlapati R.. 2002. Haploinsufficiency of flap endonuclease (Fen1) leads to rapid tumor progression. Proc. Natl. Acad. Sci. USA 99:9924–9929.
  • Lea, D. E., and Coulson C. A.. 1949. The distribution of the numbers of mutants in bacterial populations. J. Genet. 49:264–285.
  • Lee, S., and Park M.. 2002. Human FEN-1 can process the 5′-flap DNA of CTG/CAG triplet repeat derived from human genetic diseases by length and sequence dependent manner. Exp. Mol. Med. 34:313–317.
  • Lenzmeier, B. A., and Freudenreich C. H.. 2003. Trinucleotide repeat instability: a hairpin curve at the crossroads of replication, recombination, and repair. Cytogenet. Genome Res. 100:7–24.
  • Liu, Y., and Bambara R.. 2003. Analysis of human flap endonuclease 1 mutants reveals a mechanism to prevent triplet repeat expansion. J. Biol. Chem. 278:13728–13739.
  • Lopes, J., Debrauwere H., Buard J., and Nicolas A.. 2002. Instability of the human minisatellite CEB1 in rad27Δ and dna2-1 replication-deficient yeast cells. EMBO J. 21:3201–3211.
  • Maleki, S., Cederberg H., and Rannug U.. 2002. The human minisatellites MS1, MS32, MS205 and CEB1 integrated into the yeast genome exhibit different degrees of mitotic instability but are all stabilised by RAD27. Curr. Genet. 41:333–341.
  • Matsumoto, Y., Kim K., Hurwitz J., Gary R., Levin D. S., Tomkinson A. E., and Park M. S.. 1999. Reconstitution of proliferating cell nuclear antigen-dependent repair of apurinic/apyrimidinic sites with purified human proteins. J. Biol. Chem. 274:33703–33708.
  • Maurer, D. J., O'Callaghan B. L., and Livingston D. M.. 1998. Mapping the polarity of changes that occur in interrupted CAG repeat tracts in yeast. Mol. Cell. Biol. 18:4597–4604.
  • Miret, J., Pessoa-Brandao L., and Lahue R.. 1997. Instability of CAG and CTG trinucleotide repeats in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:3382–3387.
  • Mirkin, S., and Smirnova E.. 2002. Positioned to expand. Nat. Genet. 31:5–6.
  • Mueser, T. C., Nossal N. G., and Hyde C. C.. 1996. Structure of bacteriophage T4 RNase H, a 5′ to 3′ RNA-DNA and DNA-DNA exonuclease with sequence similarity to the RAD2 family of eukaryotic proteins. Cell 85:1101–1112.
  • Murante, R. S., Rumbaugh J. A., Barnes C. J., Norton J. R., and Bambara R. A.. 1996. Calf RTH1 nuclease can remove the initiator RNAs of Okazaki fragments by endonuclease activity. J. Biol. Chem. 271:25888–25897.
  • Murray, J. M., Tavassoli M., al-Harithy R., Sheldrick K. S., Lehmann A. R., Carr A. M., and Watts F. Z.. 1994. Structural and functional conservation of the human homolog of the Schizosaccharomyces pombe rad2 gene, which is required for chromosome segregation and recovery from DNA damage. Mol. Cell. Biol. 14:4878–4888.
  • Negritto, M. C., Qiu J., Ratay D. O., Shen B., and Bailis A. M.. 2001. Novel function of Rad27 (FEN-1) in restricting short-sequence recombination. Mol. Cell. Biol. 21:2349–2358.
  • Parenteau, J., and Wellinger R.. 2002. Differential processing of leading- and lagging-strand ends at Saccharomyces cerevisiae telomeres revealed by the absence of Rad27p nuclease. Genetics 162:1583–1594.
  • Parenteau, J., and Wellinger R. J.. 1999. Accumulation of single-stranded DNA and destabilization of telomeric repeats in yeast mutant strains carrying a deletion of RAD27. Mol. Cell. Biol. 19:4143–4152.
  • Reagan, M. S., Pittenger C., Siede W., and Friedberg E. C.. 1995. Characterization of a mutant strain of Saccharomyces cerevisiae with a deletion of the RAD27 gene, a structural homolog of the RAD2 nucleotide excision repair gene. J. Bacteriol. 177:364–371.
  • Richard, G., Hennequin C., Thierry A., and Dujon B.. 1999. Trinucleotide repeats and other microsatellites in yeasts. Res. Microbiol. 150:589–602.
  • Richard, G. F., Goellner G. M., McMurray C. T., and Haber J. E.. 2000. Recombination-induced CAG trinucleotide repeat expansions in yeast involve the MRE11-RAD50-XRS2 complex. EMBO J. 19:2381–2390.
  • Robins, P., Pappin D. J., Wood R. D., and Lindahl T.. 1994. Structural and functional homology between mammalian DNase IV and the 5′-nuclease domain of Escherichia coli DNA polymerase I. J. Biol. Chem. 269:28535–28538.
  • Schulz, V. P., and Zakian V. A.. 1994. The Saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 76:145–155.
  • Schweitzer, J. K., and Livingston D. M.. 1998. Expansions of CAG repeat tracts are frequent in a yeast mutant defective in Okazaki fragment maturation. Hum. Mol. Genet. 7:69–74.
  • Shen, B., Qiu J., Hosfield D., and Tainer J. A.. 1998. Flap endonuclease homologs in archaebacteria exist as independent proteins. Trends Biochem. Sci. 23:171–173.
  • Sommers, C. H., Miller E. J., Dujon B., Prakash S., and Prakash L.. 1995. Conditional lethality of null mutations in RTH1 that encodes the yeast counterpart of a mammalian 5′- to 3′-exonuclease required for lagging strand DNA synthesis in reconstituted systems. J. Biol. Chem. 270:4193–4196.
  • Spiro, C., and McMurray C. T.. 2003. Nuclease-deficient FEN-1 blocks Rad51/BRCA1-mediated repair and causes trinucleotide repeat instability. Mol. Cell. Biol. 23:6063–6074.
  • Spiro, C., Pelletier R., Rolfsmeier M. L., Dixon M. J., Lahue R. S., Gupta G., Park M. S., Chen X., Mariappan S. V., and McMurray C. T.. 1999. Inhibition of FEN-1 processing by DNA secondary structure at trinucleotide repeats. Mol. Cell 4:1079–1085.
  • Symington, L. S. 1998. Homologous recombination is required for the viability of rad27 mutants. Nucleic Acids Res. 26:5589–5595.
  • Tishkoff, D. X., Filosi N., Gaida G. M., and Kolodner R. D.. 1997. A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair. Cell 88:253–263.
  • Tom, S., Henricksen L. A., and Bambara R. A.. 2000. Mechanism whereby proliferating cell nuclear antigen stimulates flap endonuclease 1. J. Biol. Chem. 275:10498–10505.
  • Turchi, J. J., Huang L., Murante R. S., Kim Y., and Bambara R. A.. 1994. Enzymatic completion of mammalian lagging-strand DNA replication. Proc. Natl. Acad. Sci. USA 91:9803–9807.
  • Vallen, E. A., and Cross F. R.. 1995. Mutations in RAD27 define a potential link between G1 cyclins and DNA replication. Mol. Cell. Biol. 15:4291–4302.
  • White, P. J., Borts R. H., and Hirst M. C.. 1999. Stability of the human fragile X (CGG)n triplet repeat array in Saccharomyces cerevisiae deficient in aspects of DNA metabolism. Mol. Cell. Biol. 19:5675–5684.
  • Winston, F., Dollard C., and Ricupero-Hovasse S. L.. 1995. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11:53–55.
  • Wu, X., Li J., Li X., Hsieh C. L., Burgers P. M., and Lieber M. R.. 1996. Processing of branched DNA intermediates by a complex of human FEN-1 and PCNA. Nucleic Acids Res. 24:2036–2043.
  • Xie, Y., Liu Y., Argueso J. L., Henricksen L. A., Kao H. I., Bambara R. A., and Alani E.. 2001. Identification of rad27 mutations that confer differential defects in mutation avoidance, repeat tract instability, and flap cleavage. Mol. Cell. Biol. 21:4889–4899.

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