Large-Scale Expansions of Friedreich's Ataxia GAA Repeats in Yeast

Molecular Cell

Volumn 35, Issue 1, 2009, Pages 82-92

  Shishkin, Alexander A ^a   Voineagu, Irina ^a   Matera, Robert ^a   Cherng, Nicole ^a   Chernet, Brook T ^a   Krasilnikova, Maria M ^b   Narayanan, Vidhya ^c   Lobachev, Kirill S ^c   Mirkin, Sergei M ^a  

^a TUFTS UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

DNA; HUMDISEASE

Indexed keywords

DNA HELICASE SGS1; HELICASE; NUCLEIC ACID BINDING PROTEIN; RAD5 PROTEIN; RAD6 PROTEIN; REPETITIVE DNA; UNCLASSIFIED DRUG;

ARTICLE; DNA REPAIR; EXPERIMENTAL STUDY; FRIEDREICH ATAXIA; GENE; GENE INACTIVATION; GENE REPLICATION; NONHUMAN; REPLICON; YEAST;

DNA REPLICATION; FRIEDREICH ATAXIA; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; INTRONS; IRON-BINDING PROTEINS; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRINUCLEOTIDE REPEAT EXPANSION; TRINUCLEOTIDE REPEATS; YEASTS;

EID: 67649639511     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.06.017     Document Type: Article

References (85)

1. Anderson S., and DePamphilis M.L. Metabolism of Okazaki fragments during simian virus 40 DNA replication. J. Biol. Chem. 254 (1979) 11495-11504
2. Andersen P.L., Xu F., and Xiao W. Eukaryotic DNA damage tolerance and translesion synthesis through covalent modifications of PCNA. Cell Res. 18 (2008) 162-173
3. Baralle M., Pastor T., Bussani E., and Pagani F. Influence of Friedreich ataxia GAA noncoding repeat expansions on pre-mRNA processing. Am. J. Hum. Genet. 83 (2008) 77-88
4. Bhattacharyya S., and Lahue R.S. Saccharomyces cerevisiae Srs2 DNA helicase selectively blocks expansions of trinucleotide repeats. Mol. Cell. Biol. 24 (2004) 7324-7330
5. Bidichandani S.I., Ashizawa T., and Patel P.I. The GAA triplet-repeat expansion in Friedreich ataxia interferes with transcription and may be associated with an unusual DNA structure. Am. J. Hum. Genet. 62 (1998) 111-121
6. Blastyak A., Pinter L., Unk I., Prakash L., Prakash S., and Haracska L. Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol. Cell 28 (2007) 167-175
7. Boeke J.D., Trueheart J., Natsoulis G., and Fink G.R. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 154 (1987) 164-175
8. Boule J.B., and Zakian V.A. Roles of Pif1-like helicases in the maintenance of genomic stability. Nucleic Acids Res. 34 (2006) 4147-4153
9. Calzada A., Hodgson B., Kanemaki M., Bueno A., and Labib K. Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes Dev. 19 (2005) 1905-1919
10. Campuzano V., Montermini L., Molto M.D., Pianese L., Cossee M., Cavalcanti F., Monros E., Rodius F., Duclos F., Monticelli A., et al. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271 (1996) 1423-1427
11. Chakraverty R.K., Kearsey J.M., Oakley T.J., Grenon M., de La Torre Ruiz M.A., Lowndes N.F., and Hickson I.D. Topoisomerase III acts upstream of Rad53p in the S-phase DNA damage checkpoint. Mol. Cell. Biol. 21 (2001) 7150-7162
12. Cleary J.D., Nichol K., Wang Y.H., and Pearson C.E. Evidence of cis-acting factors in replication-mediated trinucleotide repeat instability in primate cells. Nat. Genet. 31 (2002) 37-46
13. Daee D.L., Mertz T., Collins N., and Lahue R.S. Post-replication repair inhibits CAG.CTG repeat expansions in Saccharomyces cerevisiae. Mol. Cell. Biol. 27 (2007) 102-110
14. Drake J.W. A constant rate of spontaneous mutation in DNA-based microbes. Proc. Natl. Acad. Sci. USA 88 (1991) 7160-7164
15. Foss E.J. Tof1p regulates DNA damage responses during S phase in Saccharomyces cerevisiae. Genetics 157 (2001) 567-577
16. Freudenreich C.H., Kantrow S.M., and Zakian V.A. Expansion and length-dependent fragility of CTG repeats in yeast. Science 279 (1998) 853-856
17. Fu Y.H., Kuhl D.P., Pizzuti A., Pieretti M., Sutcliffe J.S., Richards S., Verkerk A.J., Holden J.J., Fenwick Jr. R.G., Warren S.T., et al. Variation of the CGG repeat at the fragile X site results in genetic instability: resolution of the Sherman paradox. Cell 67 (1991) 1047-1058
18. Gacy A.M., Goellner G.M., Spiro C., Chen X., Gupta G., Bradbury E.M., Dyer R.B., Mikesell M.J., Yao J.Z., Johnson A.J., et al. GAA instability in Friedreich's ataxia shares a common, DNA-directed and intraallelic mechanism with other trinucleotide diseases. Mol. Cell 1 (1998) 583-593
19. Gangloff S., McDonald J.P., Bendixen C., Arthur L., and Rothstein R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14 (1994) 8391-8398
20. Goldfless S.J., Morag A.S., Belisle K.A., Sutera Jr. V.A., and Lovett S.T. DNA repeat rearrangements mediated by DnaK-dependent replication fork repair. Mol. Cell 21 (2006) 595-604
21. Gomes-Pereira M., Foiry L., Nicole A., Huguet A., Junien C., Munnich A., and Gourdon G. CTG trinucleotide repeat "big jumps": large expansions, small mice. PLoS Genet. 3 (2007) e52
22. *TTC triplet repeat expanded in Friedreich's ataxia impedes transcription elongation by T7 RNA polymerase in a length and supercoil dependent manner. Nucleic Acids Res. 28 (2000) 2815-2822
23. Harfe B.D., and Jinks-Robertson S. DNA mismatch repair and genetic instability. Annu. Rev. Genet. 34 (2000) 359-399
24. Ii M., and Brill S.J. Roles of SGS1, MUS81, and RAD51 in the repair of lagging-strand replication defects in Saccharomyces cerevisiae. Curr. Genet. 48 (2005) 213-225
25. Jakupciak J.P., and Wells R.D. Genetic instabilities in (CTG.CAG) repeats occur by recoombination. J. Biol. Chem. 274 (1999) 23468-23479
26. Jankowski C., Nasar F., and Nag D.K. Meiotic instability of CAG repeat tracts occurs by double-strand break repair in yeast. Proc. Natl. Acad. Sci. USA 97 (2000) 2134-2139
27. Jaworski A., Rosche W.A., Gellibolian R., Kang S., Shimizu M., Bowater R.P., Sinden R.R., and Wells R.D. Mismatch repair in Escherichia coli enhances instability of (CTG)n triplet repeats from human hereditary diseases. Proc. Natl. Acad. Sci. USA 92 (1995) 11019-11023
28. Kang S., Jaworski A., Ohshima K., and Wells R.D. Expansion and deletion of CTG repeats from human disease genes are determined by the direction of replication in E.coli. Nat. Genet. 10 (1995) 213-218
29. Katou Y., Kanoh Y., Bando M., Noguchi H., Tanaka H., Ashikari T., Sugimoto K., and Shirahige K. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424 (2003) 1078-1083
30. Khakhar R.R., Cobb J.A., Bjergbaek L., Hickson I.D., and Gasser S.M. RecQ helicases: multiple roles in genome maintenance. Trends Cell Biol. 13 (2003) 493-501
31. Kim H.M., Narayanan V., Mieczkowski P.A., Petes T.D., Krasilnikova M.M., Mirkin S.M., and Lobachev K.S. Chromosome fragility at GAA tracts in yeast depends on repeat orientation and requires mismatch repair. EMBO J. 27 (2008) 2896-2906
32. Klein H.L. Reversal of fortune: Rad5 to the rescue. Mol. Cell 28 (2007) 181-183
33. Kovtun I.V., and McMurray C.T. Trinucleotide expansion in haploid germ cells by gap repair. Nat. Genet. 27 (2001) 407-411
34. Kovtun I.V., and McMurray C.T. Features of trinucleotide repeat instability in vivo. Cell Res. 18 (2008) 198-213
35. Kovtun I.V., Liu Y., Bjoras M., Klungland A., Wilson S.H., and McMurray C.T. OGG1 initiates age-dependent CAG trinucleotide expansion in somatic cells. Nature 447 (2007) 447-452
36. Krasilnikova M.M., and Mirkin S.M. Replication stalling at Friedreich's ataxia (GAA)n repeats in vivo. Mol. Cell. Biol. 24 (2004) 2286-2295
37. Krogh B.O., and Symington L.S. Recombination proteins in yeast. Annu. Rev. Genet. 38 (2004) 233-271
38. Lahue R.S., and Slater D.L. DNA repair and trinucleotide repeat instability. Front. Biosci. 8 (2003) s663-s665
39. Lawrence C. The RAD6 DNA repair pathway in Saccharomyces cerevisiae: what does it do, and how does it do it?. Bioessays 16 (1994) 253-258
40. Lia A.S., Seznec H., Hofmann-Radvanyi H., Radvanyi F., Duros C., Saquet C., Blanche M., Junien C., and Gourdon G. Somatic instability of the CTG repeat in mice transgenic for the myotonic dystrophy region is age dependent but not correlated to the relative intertissue transcription levels and proliferative capacities. Hum. Mol. Genet. 7 (1998) 1285-1291
41. Lobachev K.S., Gordenin D.A., and Resnick M.A. The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108 (2002) 183-193
42. Manley K., Shirley T.L., Flaherty L., and Messer A. Msh2 deficiency prevents in vivo somatic instability of the CAG repeat in Huntington disease transgenic mice. Nat. Genet. 23 (1999) 471-473
43. McMurray C.T. DNA secondary structure: A common and causative factor for expansion in human disease. Proc. Natl. Acad. Sci. USA 96 (1999) 1823-1825
44. Miret J.J., Pessoa-Brandao L., and Lahue R.S. Orientation-dependent and sequence-specific expansions of CTG/CAG trinucleotide repeats in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 95 (1998) 12438-12443
45. Mirkin S.M. DNA structures, repeat expansions and human hereditary disorders. Curr. Opin. Struct. Biol. 16 (2006) 351-358
46. Mirkin S.M. Expandable DNA repeats and human disease. Nature 447 (2007) 932-940
47. Mohanty B.K., Bairwa N.K., and Bastia D. The Tof1p-Csm3p protein complex counteracts the Rrm3p helicase to control replication termination of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 103 (2006) 897-902
48. Montermini L., Andermann E., Labuda M., Richter A., Pandolfo M., Cavalcanti F., Pianese L., Iodice L., Farina G., Monticelli A., et al. The Friedreich ataxia GAA triplet repeat: premutation and normal alleles. Hum. Mol. Genet. 6 (1997) 1261-1266
49. Nag D.K., Suri M., and Stenson E.K. Both CAG repeats and inverted DNA repeats stimulate spontaneous unequal sister-chromatid exchange in Saccharomyces cerevisiae. Nucleic Acids Res. 32 (2004) 5677-5684
50. Napierala M., Parniewski P., Pluciennik A., and Wells R.D. Long CTG.CAG repeat sequences markedly stimulate intramolecular recombination. J. Biol. Chem. 277 (2002) 34087-34100
51. Napierala M., Dere R., Vetcher A., and Wells R.D. Structure-dependent recombination hot spot activity of GAA.TTC sequences from intron 1 of the Friedreich's ataxia gene. J. Biol. Chem. 279 (2004) 6444-6454
52. Nedelcheva M.N., Roguev A., Dolapchiev L.B., Shevchenko A., Taskov H.B., Shevchenko A., Stewart A.F., and Stoynov S.S. Uncoupling of unwinding from DNA synthesis implies regulation of MCM helicase by Tof1/Mrc1/Csm3 checkpoint complex. J. Mol. Biol. 347 (2005) 509-521
53. Ohshima K., and Wells R.D. Hairpin formation during DNA synthesis primer realignment in vitro in triplet repeat sequences from human hereditary disease genes. J. Biol. Chem. 272 (1997) 16798-16806
54. Ohshima K., Montermini L., Wells R.D., and Pandolfo M. Inhibitory effects of expanded GAA.TTC triplet repeats from intron I of the Freidreich's ataxia gene on transcription and replication in vivo. J. Biol. Chem. 273 (1998) 14588-14595
55. Orr H.T., and Zoghbi H.Y. Trinucleotide repeat disorders. Annu. Rev. Neurosci. 30 (2007) 575-621
56. Owen B.A., Yang Z., Lai M., Gajek M., Badger II J.D., Hayes J.J., Edelmann W., Kucherlapati R., Wilson T.M., and McMurray C.T. (CAG)(n)-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition. Nat. Struct. Mol. Biol. 12 (2005) 663-670
57. Pandolfo M. The molecular basis of Friedreich ataxia. Adv. Exp. Med. Biol. 516 (2002) 99-118
58. *(CAG) repeats can be correctly repaired, escape repair or undergo error-prone repair. Nat. Struct. Mol. Biol. 12 (2005) 654-662
59. Patel P.I., and Isaya G. Friedreich ataxia: From GAA triplet-repeat expansion to frataxin deficiency. Am. J. Hum. Genet. 69 (2001) 15-24
60. Pearson C.E., Nichol Edamura K., and Cleary J.D. Repeat instability: mechanisms of dynamic mutations. Nat. Rev. Genet. 6 (2005) 729-742
61. Pelletier R., Krasilnikova M.M., Samadashwily G.M., Lahue R.S., and Mirkin S.M. Replication and expansion of trinucleotide repeats in yeast. Mol. Cell. Biol. 23 (2003) 1349-1357
62. Raschle M., Knipsheer P., Enoiu M., Angelov T., Sun J., Griffith J.D., Ellenberger T.E., Scharer O.D., and Walter J.C. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134 (2008) 969-980
63. Razidlo D.F., and Lahue R.S. Mrc1, Tof1 and Csm3 inhibit CAG·CTG repeat instability by at least two mechanisms. DNA Repair (Amst.) 7 (2008) 633-640
64. Richard G.F., Goellner G.M., McMurray C.T., and Haber J.E. Recombination-induced CAG trinucleotide repeat expansions in yeast involve the MRE11-RAD50-XRS2 complex. EMBO J. 19 (2000) 2381-2390
65. Richard G.F., Cyncynatus C., and Dujon B. Contractions and expansions of CAG/CTG trinucleotide repeats occur during ectopic gene conversion in yeast, by a MUS81-independent mechanism. J. Mol. Biol. 326 (2003) 769-782
66. Rindler P.M., Clark R.M., Pollard L.M., De Biase I., and Bidichandani S.I. Replication in mammalian cells recapitulates the locus-specific differences in somatic instability of genomic GAA triplet-repeats. Nucleic Acids Res. 34 (2006) 6352-6361
67. Rolfsmeier M.L., Dixon M.J., Pessoa-Brandao L., Pelletier R., Miret J.J., and Lahue R.S. Cis-elements governing trinucleotide repeat instability in Saccharomyces cerevisiae. Genetics 157 (2001) 1569-1579
68. *TTC repeats in intron 1 of the frataxin gene, inhibits transcription. J. Biol. Chem. 276 (2001) 27171-27177
69. Samadashwily G.M., Raca G., and Mirkin S.M. Trinucleotide repeats affect DNA replication in vivo. Nat. Genet. 17 (1997) 298-304
70. Savouret C., Garcia-Cordier C., Megret J., te Riele H., Junien C., and Gourdon G. MSH2-dependent germinal CTG repeat expansions are produced continuously in spermatogonia from DM1 transgenic mice. Mol. Cell. Biol. 24 (2004) 629-637
71. Torres J.Z., Schnakenberg S.L., and Zakian V.A. Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol. Cell. Biol. 24 (2004) 3198-3212
72. Tran H.T., Keen J.D., Kricker M., Resnick M.A., and Gordenin D.A. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol. Cell. Biol. 17 (1997) 2859-2865
73. Usdin K., and Woodford K.J. CGG repeats associated with DNA instability and chromosome fragility from structures that block DNA synthesis in vitro. Nucleic Acids Res. 23 (1995) 4202-4209
74. van den Broek W.J., Nelen M.R., Wansink D.G., Coerwinkel M.M., te Riele H., Groenen P.J., and Wieringa B. 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 (2002) 191-198
75. Voineagu I., Narayanan V., Lobachev K.S., and Mirkin S.M. Replication stalling at unstable inverted repeats: Interplay between DNA hairpins and fork stabilizing proteins. Proc. Natl. Acad. Sci. USA 105 (2008) 9936-9941
76. Voineagu I., Surka C.F., Shishkin A.A., Krasilnikova M.M., and Mirkin S.M. Replisome stalling and stabilization at CGG repeats, which are responsible for chromosomal fragility. Nat. Struct. Mol. Biol. 16 (2009) 226-228
77. Von Borstel R.C., Cain K.T., and Steinberg C.M. Inheritance of spontaneous mutability in yeast. Genetics 69 (1971) 17-27
78. Wach A., Brachat A., Poehlmann R., and Philippsen P. New heterologous modules for classical or PCR-based gene disruption in S. cerevisiae. Yeast 10 (1994) 1793-1808
79. Wang G., and Vasquez K.M. Naturally occurring H-DNA-forming sequences are mutagenic in mammalian cells. Proc. Natl. Acad. Sci. USA 101 (2004) 13448-13453
80. Wang G., and Vasquez K.M. Non-B DNA structure-induced genetic instability. Mutat. Res. 598 (2006) 103-119
81. Watt P.M., Hickson I.D., Borts R.H., and Louis E.J. SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics 144 (1996) 935-945
82. Wells R.D. DNA triplexes and Friedreich ataxia. FASEB J. 22 (2008) 1625-1634
83. Wells R.D., Dere R., Hebert M.L., Napierala M., and Son L.S. Advances in mechanisms of genetic instability related to hereditary neurological diseases. Nucleic Acids Res. 33 (2005) 3785-3798
84. Wu J.R., and Gilbert D.M. Rapid DNA preparation for 2D gel analysis of replicaton intermediates. Nucleic Acids Res. 23 (1995) 3997-3998
85. Yu X., and Gabriel A. Patching broken chromosomes with extranuclear cellular DNA. Mol. Cell 4 (1999) 873-881