Mutations in Yeast Replication Proteins That Increase CAG/CTG Expansions Also Increase Repeat Fragility

Molecular and Cellular Biology

Volumn 23, Issue 21, 2003, Pages 7849-7860

  Callahan, Julie L ^a,c   Andrews, Kenneth J ^a,d   Zakian, Virginia A ^b   Freudenreich, Catherine H ^a  

^a TUFTS UNIVERSITY   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYTOSINE; DNA DIRECTED DNA POLYMERASE DELTA; DNA FRAGMENT; DNA PRIMASE; DNA2 HELICASE; ENDONUCLEASE; EXONUCLEASE; FEN1 PROTEIN; FUNGAL PROTEIN; GUANINE; HELICASE; NUCLEASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RAD27 PROTEIN; REPLICATION PROTEIN; RIBONUCLEASE III; THYMINE; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME ANALYSIS; CHROMOSOME BREAKAGE; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA REPAIR; DNA REPLICATION; DNA STRAND; DNA STRAND BREAKAGE; FUNGAL STRAIN; GENE DELETION; GENE LOSS; GENE MUTATION; GENETIC ANALYSIS; GENETIC DISORDER; MARKER GENE; MOLECULAR CLONING; MOLECULAR STABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; TELOMERE; TRINUCLEOTIDE REPEAT; YEAST; YEAST ARTIFICIAL CHROMOSOME;

ADENOSINE TRIPHOSPHATASES; BIOLOGICAL ASSAY; CHROMOSOMES, ARTIFICIAL; DNA DAMAGE; DNA HELICASES; DNA LIGASES; DNA POLYMERASE III; DNA PRIMASE; DNA REPLICATION; FLAP ENDONUCLEASES; FUNGAL PROTEINS; HUMANS; MUTATION; REPRODUCIBILITY OF RESULTS; RIBONUCLEASE H, CALF THYMUS; SACCHAROMYCES CEREVISIAE PROTEINS; TRINUCLEOTIDE REPEAT EXPANSION; YEASTS;

EID: 0142027842     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.21.7849-7860.2003     Document Type: Article

References (93)

1. Adams Martin, A., I. Dionne, R. J. Wellinger, and C. Holm. 2000. The function of DNA polymerase α at telomeric G tails is important for telomere homeostasis. Mol. Cell. Biol. 20:786-796.
2. Anderson, S., and M. L. DePamphilis. 1979. Metabolism of Okazaki fragments during simian virus 40 DNA replication. J. Biol. Chem. 254:11495-11504.
3. Ayyagari, R., X. V. Gomes, D. A. Gordenin, and P. M. Burgers. 2003. Okazaki fragment maturation in yeast. I. Distribution of functions between FEN1 and DNA2. J. Biol. Chem. 278:1618-1625.
4. Bae, S. H., K. H. Bae, J. A. Kim, and Y. S. Seo. 2001. RPA governs endonuclease switching during processing of Okazaki fragments in eukaryotes. Nature 412:456-461.
5. Bae, S.-H., E. Choi, K.-H. Lee, J. S. Park, S.-H. Lee, and Y.-S. Seo. 1998. Dna2 of Saccharomyces cerevisiae possesses a single-stranded DNA-specific endonuclease activity that is able to act on double-stranded DNA in the presence of ATP. J. Biol. Chem. 273:26880-26890.
6. Bae, S. H., D. W. Kim, J. Kim, J. H. Kim, D. H. Kim, H. D. Kim, H. Y. Kang, and Y. S. Seo. 2002. Coupling of DNA helicase and endonuclease activities of yeast Dna2 facilitates Okazaki fragment processing. J. Biol. Chem. 277: 26632-26641.
7. Bae, S. H., and Y. S. Seo. 2000. Characterization of the enzymatic properties of the yeast Dna2 helicase/endonuclease suggests a new model for Okazaki fragment processing. J. Biol. Chem. 275:38022-38031.
8. 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.
9. Bambara, R. A., R. S. Murante, and L. A. Henricksen. 1997. Enzymes and reactions at the eukaryotic DNA replication fork. J. Biol. Chem. 272:4647-4650.
10. Baudin, A., O. Ozier-Kalogeropoulos, A. Denouel, F. Lacroute, and C. Cullen. 1993. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 21:3329-3330.
11. Bielinsky, A. K., and S. A. Gerbi. 1998. Discrete start sites for DNA synthesis in the yeast ARS1 origin. Science 279:95-98.
12. Budd, M. E., and J. L. Campbell. 1995. A yeast gene required for DNA replication encodes a protein with homology to DNA helicases. Proc. Natl. Acad. Sci. USA 92:7642-7646.
13. Budd, M. E., and J. L. Campbell. 1997. A yeast replicative helicase, Dna2 helicase, interacts with yeast FEN-1 nuclease in carrying out its essential function. Mol. Cell. Biol. 17:2136-2142.
14. Budd, M. E., W. Choe, and J. L. Campbell. 2000. The nuclease activity of the yeast DNA2 protein, which is related to the RecB-like nucleases, is essential in vivo. J. Biol. Chem. 275:16518-16529.
15. Chen, C., and R. Kolodner. 1999. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat. Genet. 23:81-85.
16. Cleary, J. D., K. Nichol, Y. H. Wang, and C. E. Pearson. 2002. Evidence of cis-acting factors in replication-mediated trinucleotide repeat instability in primate cells. Nat. Genet. 31:37-46.
17. Cleary, J. D., and C. E. Pearson. The contribution of cis-elements to disease-associated repeat instability. Cytogenet. Genome Res., in press.
18. Cohen, H., D. D. Sears, D. Zenvirth, P. Hieter, and G. Simchen. 1999. Increased instability of human CTG repeat tracts on yeast artificial chromosomes during gametogenesis. Mol. Cell. Biol. 19:4153-4158.
19. Cummings, C. J., and H. Y. Zoghbi. 2000. Fourteen and counting: unraveling trinucleotide repeat diseases. Hum. Mol. Genet. 9:909-916.
20. 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.
21. Diede, S. J., and D. E. Gottschling. 1999. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 99:723-733.
22. Dutcher, S. K. 1981. Internuclear transfer of genetic information in kar1/ KAR1 heterokaryons in Saccharomyces cerevisiae. Mol. Cell. Biol. 1:245-253.
23. Francesconi, S., M. P. Longhese, A. Piseri, C. Santocanale, G. Lucchini, and P. Plevani. 1991. Mutations in conserved yeast DNA primase domains impair DNA replication in vivo. Proc. Natl. Acad. Sci. USA 88:3877-3881.
24. Frank, P., C. Craunshofer-Reiter, and U. Wintersberger. 1998. Yeast RNase H(35) is the counterpart of the mammalian RNase HI, and is evolutionarily related to prokaryotic RNase HII. FEBS Lett. 421:23-26.
25. Freudenreich, C. H., S. M. Kantrow, and V. Zakian. 1998. Expansion and length-dependent fragility of CTG repeats in yeast. Science 279:853-856.
26. Freudenreich, C. H., J. B. Stavenhagen, and V. A. Zakian. 1997. Stability of a CTG/CAG trinucleotide repeat in yeast is dependent on its orientation in the genome. Mol. Cell. Biol. 17:2090-2098.
27. Gacy, A. M., G. Goellner, N. Juranic, S. Macura, and C. T. McMurray. 1995. Trinucleotide repeats that expand in human disease form hairpin structures in vitro. Cell 81:533-540.
28. Gary, R., M. S. Park, J. P. Nolan, H. L. Cornelius, O. G. Kozyreva, H. T. Tran, K. S. Lobachev, M. A. Resnick, and D. A. Gordenin. 1999. A novel role in DNA metabolism for the binding of Fen1/Rad27 to PCNA and implications for genetic risk. Mol. Cell. Biol. 19:5373-5382.
29. Gordenin, D. A., T. A. Kunkel, and M. A. Resnick. 1997. Repeat expansion-all in a flap? Nat. Genet. 16:116-118.
30. Hartenstine, M. J., M. F. Goodman, and J. Petruska. 2002. Weak strand displacement activity enables human DNA polymerase beta to expand CAG/ CTG triplet repeats at strand breaks. J. Biol. Chem. 277:41379-41389.
31. Hartwell, L. H., R. K. Mortimer, J. Culotti, and M. Culotti. 1973. Genetic control of the cell division cycle in yeast: genetic analysis of cdc mutants. Genetics 74:267-286.
32. Henricksen, L. A., S. Tom, Y. Liu, and R. A. Bambara. 2000. Inhibition of flap endonuclease 1 by flap secondary structure and relevance to repeat sequence expansion. J. Biol. Chem. 275:16420-16427.
33. Henricksen, L. A., J. Veeraraghavan, D. R. Chafin, and R. A. Bambara. 2002. DNA ligase I competes with FEN1 to expand repetitive DNA sequences in vitro. J. Biol. Chem. 277:22361-22369.
34. Holmes, A. M., and J. E. Haber. 1999. Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell 96:415-424.
35. Hosfield, D. J., C. D. Mol, B. Shen, and J. A. Tainer. 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.
36. Ireland, M. J., S. S. Reinke, and D. M. Livingston. 2000. The impact of lagging strand replication mutations on the stability of CAG repeat tracts in yeast. Genetics 155:1657-1665.
37. Jakupciak, J. P., and R. D. Wells. 1999. Genetic instabilities in (CTG-CAG) repeats occur by recombination. J. Biol. Chem. 274:23468-23479.
38. Jankowski, C., and D. K. Nag. 2002. Most meiotic CAG repeat tract-length alterations in yeast are SPO11 dependent. Mol. Genet. Genomics 267:64-70.
39. Jankowski, C., F. Nasar, and D. K. Nag. 2000. Meiotic instability of CAG repeat tracts occurs by double-strand break repair in yeast. Proc. Natl. Acad. Sci. USA 97:2134-2139.
40. Johnson, R., G. Kovvali, L. Prakash, and S. Prakash. 1998. Role of yeast Rth1 nuclease and its homologs in mutation avoidance, DNA repair, and DNA replication. Curr. Genet. 34:21-29.
41. Johnson, R. E., G. K. Kowali, L. Prakash, and S. Prakash. 1995. Requirement of the yeast RTH1 5′ to 3′ exonuclease for the stability of simple repetitive DNA. Science 269:238-240.
42. Kang, S., A. Jaworski, K. Ohshima, and R. D. Wells. 1995. Expansion and deletion of CTG repeats from human disease genes are determined by the direction of replication in E. coli. Nat. Genet. 10:213-218.
43. Kao, H.-I., L. A. Henricksen, Y. Liu, and R. A. Bambara. 2002. Cleavage specificity of Saccharomyces cerevisiae Flap endonuclease 1 suggests a double-flap structure as the cellular substrate. J. Biol. Chem. 277:14379-14389.
44. Kim, K., S. Biade, and Y. Matsumoto. 1998. Involvement of flap endonuclease 1 in base excision DNA repair. J. Biol. Chem. 273:8842-8848.
45. Klungland, A., and T. Lindahl. 1997. Second pathway for completion of human DNA base excision -repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J. 16:3341-3348.
46. Kokoska, R. J., L. Stefanovic, H. T. Tran, M. A. Resnick, D. A. Gordenin, and T. D. Petes. 1998. Destabilization of yeast micro- and minisatellite DNA sequences by mutations affecting a nuclease involved in Okazaki fragment processing (rad27) and DNA polymerase 8 (pol3-t). Mol. Cell. Biol. 18:2779-2788.
47. Kovtun, I., and C. McMurray. 2001. Trinucleotide expansion in haploid germ cells by gap repair. Nat. Genet. 27:407-411.
48. Kovtun, I. V., G. Goellner, and C. T. McMurray. 2001. Structural features of trinucleotide repeats associated with DNA expansion. Biochem. Cell Biol. 79:325-336.
49. Lea, D. E., and C. A. Coulson. 1949. The distribution of the numbers of mutants in bacterial populations. J. Genet. 49:264-285.
50. Lee, K. H., D. W. Kim, S. H. Bae, J. A. Kim, G. H. Ryu, Y. N. Kwon, K. A. Kim, H. S. Koo, and Y. S. Seo. 2000. The endonuclease activity of the yeast Dna2 enzyme is essential in vivo. Nucleic Acids Res. 28:2873-2881.
51. Lenzmeier, B. A., and C. H. Freudenreich. Trinucleotide repeat instability: a hairpin curve at the crossroads of replication, recombination, and repair. Cytogenet. Genome Res., in press.
52. Liu, Y., and R. A. Bambara. 2003. Analysis of human flap endonuclease 1 mutants reveals a mechanism to prevent triplet repeat expansion. J. Biol. Chem. 278:13728-13739.
53. Lopes, J., H. Debrauwere, J. Buard, and A. Nicolas. 2002. Instability of the human minisatellite CEB1 in rad27Delta and dna2-1 replication-deficient yeast cells. EMBO J. 21:3201-3211.
54. Lyons-Darden, T., and M. D. Topal. 1999. Abasic sites induce triplet-repeat expansion during DNA replication in vitro. J. Biol. Chem. 274:25975-25978.
55. Maleki, S., H. Cederberg, and U. Rannug. 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.
56. Manley, K., T. L. Shirley, L. Flaherty, and A. Messer. 1999. Msh2 deficiency prevents in vivo somatic instability of the CAG repeat in Huntington disease transgenic mice. Nat. Genet. 23:471-473.
57. Maurer, D. J., B. L. O'Callaghan, and D. M. Livingston. 1996. Orientation dependence of trinucleotide CAG repeat instability in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:6617-6622.
58. Michel, B. 2000. Replication fork arrest and DNA recombination. Trends Biochem. Sci. 25:173-178.
59. Michel, B., S. D. Erlich, and M. Uzest. 1997. DNA double-strand breaks caused by replication arrest. EMBO J. 16:430-438.
60. Miret, J. J., L. Pessoa-Brandāo, and R. S. Lahue. 1997. Instability of CAG and CTG trinucleotide repeats in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:3382-3387.
61. Mitas, M. 1997. Trinucleotide repeats associated with human disease. Nucleic Acids Res. 25:2245-2253.
62. Murante, R. S., L. A. Henricksen, and R. A. Bambara. 1998. Junction ribonuclease: an activity in Okazaki fragment processing. Proc. Natl. Acad. Sci. USA 95:2244-2249.
63. Nelson, D. L. 1995. The fragile X syndromes. Cell Biol. 6:5-11.
64. Parenteau, J., and R. J. Wellinger. 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.
65. Pearson, C. E., and R. R. Sinden. 1998. Trinucleotide repeat DNA structures: dynamic mutations from dynamic DNA. Curr. Opin. Struct. Biol. 8:321-330.
66. Pelletier, R., M. M. Krasilnikova, G. M. Samadashwily, R. Lahue, and S. M. Mirkin. 2003. Replication and expansion of trinucleotide repeats in yeast. Mol. Cell. Biol. 23:1349-1357.
67. Pluta, A. F., and V. A. Zakian. 1989. Recombination occurs during telomere formation in yeast. Nature 337:429-433.
68. Qiu, J., Y. Qian, P. Frank, U. Wintersberger, and B. Shen. 1999. Saccharomyces cerevisiae RNase H(35) functions in RNA primer removal during lagging-strand DNA synthesis, most efficiently in cooperation with Rad27 nuclease. Mol. Cell. Biol. 19:8361-8371.
69. Reagan, M. S., C. Pittenger, W. Siede, and E. C. Friedberg. 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.
70. Richard, G.-F., B. Dujon, and J. E. Haber. 1999. Double-strand break repair can lead to high frequencies of deletions within short CAG/CTG trinucleotide repeats. Mol. Gen. Genet. 261:871-882.
71. Richard, G. F., G. M. Goellner, C. T. McMurray, and J. E. Haber. 2000. Recombination-induced CAG trinucleotide repeat expansions in yeast involve the MRE11-RAD50-XRS2 complex. EMBO J. 19:2381-2390.
72. Richard, G. F., and F. Paques. 2000. Mini- and microsatellite expansions: the recombination connection. EMBO Rep. 1:122-126.
73. Richards, R. I. 2001. Dynamic mutations: a decade of unstable expanded repeats in human genetic disease. Hum. Mol. Genet. 10:2187-2194.
74. Rothstein, R., B. Michel, and S. Gangloff. 2000. Replication fork pausing and recombination or "gimme a break." Genes Dev. 14:1-10.
75. Samadashwily, G. M., G. Raca, and S. M. Mirkin. 1997. Trinucleotide repeats affect DNA replication in vivo. Nat. Genet. 17:298-304.
76. Sarkar, P. S., H.-C. Chang, B. Boudi, and S. Reddy. 1998. CTG repeats show bimodal amplification in E. coli. Cell 95:531-540.
77. Schulz, V. P., and V. A. Zakian. 1994. The Saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 76:145-155.
78. Schweitzer, J. K., and D. M. Livingston. 1999. The effect of DNA replication mutations on CAG tract stability in yeast. Genetics 152:953-963.
79. Schweitzer, J. K., and D. M. Livingston. 1998. Expansions of CAG repeat tracts are frequent in a yeast mutant defective in Okazaki fragment maturation. Hum. Mol. Genet. 7:69-74.
80. Schweitzer, J. K., S. S. Reinke, and D. M. Livingston. 2001. Meiotic alterations in CAG repeat tracts. Genetics 159:1861-1865.
81. Shibata, Y., and T. Nakamura. 2002. Defective flap endonuclease 1 activity in mammalian cells is associated with impaired DNA repair and prolonged S phase delay. J. Biol. Chem. 277:746-754.
82. Sinden, R. R. 1999. Human Genetics '99: trinucleotide repeats. Biological implications of the DNA structures associated with disease-causing triplet repeats. Am. J. Hum. Genet. 64:346-353.
83. Sommers, C. H., E. J. Miller, B. Dujon, S. Prakash, and L. Prakash. 1995. Conditional lethality of null mutations in RTH1 that encodes the yeast counterpart of a mammalian 5′- to 3′-exonuclease required for lagging strand synthesis in reconstituted systems. J. Biol. Chem. 270:4193-4196.
84. Spiro, C., R. Pelletier, M. L. Rolfsmeir, M. J. Dixon, R. S. Lahue, G. Gupta, M. S. Park, X. Chen, S. V. Mariapp, and C. T. McMurray. 1999. Inhibition of FEN-1 processing by DNA secondary structure at trinucleotide repeats. Mol. Cell 4:1079-1085.
85. Sutherland, G. R., E. Baker, and R. I. Richards. 1998. Fragile sites still breaking. Trends Genet. 14:501-506.
86. Symington, L. S. 1998. Homologous recombination is required for the viability of rad27 mutants. Nucleic Acids Res. 26:5589-5595.
87. Tishkoff, D. X., N. Filosi, G. A. Gaida, and R. D. Kolodner. 1997. A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair. Cell 88:253-263.
88. Tran, H. T., N. P. Degtyareva, D. A. Gordenin, and M. A. Resnick. 1999. Genetic factors affecting the impact of DNA polymerase 8 activity on mutation avoidance in yeast. Genetics 152:47-59.
89. 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.
90. van den Broek, W. J., M. R. Nelen, D. G. Wansink, M. M. Coerwinkel, H. te Riele, P. J. Groenen, and B. Wieringa. 2002. Somatic expansion behaviour of the (CTG)n repeat in myotonic dystrophy knock-in mice is differentially affected by Msh3 and Msh6 mismatch-repair proteins. Hum. Mol. Genet. 11:191-198.
91. Wu, X., E. Braithwaite, and Z. Wang. 1999. DNA ligation during excision repair in yeast cell-free extracts is specifically catalyzed by the CDC9 gene product. Biochemistry 38:2628-2635.
92. Wu, X., and Z. Wang. 1999. Relationships between yeast Rad27 and Apn1 in response to apurinic/apyrimidinic (AP) sites in DNA. Nucleic Acids Res. 27:956-962.
93. Wu, X., T. E. Wilson, and M. R. Lieber. 1999. A role for FEN-1 in nonhomologous DNA end joining: the order of strand annealing and nucleolytic processing events. Proc. Natl. Acad. Sci. USA 96:1303-1308.