Instability of (CTG)n•(CAG)n trinucleotide repeats and DNA synthesis

Cell and Bioscience

Volumn 2, Issue 1, 2012, Pages

  Liu, Guoqi ^a   Leffak, Michael ^a  

^a WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA;

EID: 84862890783     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/2045-3701-2-7     Document Type: Review

References (162)

1. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 1996, 87:493-506. 10.1016/S0092-8674(00)81369-0, 8898202.
2. Mirkin SM. Expandable DNA repeats and human disease. Nature 2007, 447:932-940. 10.1038/nature05977, 17581576.
3. Voineagu I, Narayanan V, Lobachev KS, Mirkin SM. Replication stalling at unstable inverted repeats: interplay between DNA hairpins and fork stabilizing proteins. Proc Natl Acad Sci USA 2008, 105:9936-9941. 10.1073/pnas.0804510105, 2481305, 18632578.
4. Cleary JD, Tome S, Lopez Castel A, Panigrahi GB, Foiry L, Hagerman KA, Sroka H, Chitayat D, Gourdon G, Pearson CE. Tissue- and age-specific DNA replication patterns at the CTG/CAG-expanded human myotonic dystrophy type 1 locus. Nat Struct Mol Biol 2010, 17:1079-1087. 10.1038/nsmb.1876, 20711191.
5. Pearson CE, Edamura KN, Cleary JD. Repeat instability: mechanisms of dynamic mutations. Nat Rev Genet 2005, 6:729-742. 10.1038/nrg1689, 16205713.
6. Cleary JD, Pearson CE. Replication fork dynamics and dynamic mutations: the fork-shift model of repeat instability. Trends Genet 2005, 21:272-280. 10.1016/j.tig.2005.03.008, 15851063.
7. Liu G, Chen X, Bissler JJ, Sinden RR, Leffak M. Replication-dependent instability at (CTG) × (CAG) repeat hairpins in human cells. Nat Chem Biol 2010, 6:652-659. 10.1038/nchembio.416, 2924473, 20676085.
8. Liu G, Bissler JJ, Sinden RR, Leffak M. Unstable Spinocerebellar Ataxia Type 10 (ATTCT)*(AGAAT) repeats are associated with aberrant replication at the ATX10 locus and replication origin-dependent expansion at an ectopic site in human cells. MolCell Biol 2007, 27:7828-7838.
9. Panaite PA, Gantelet E, Kraftsik R, Gourdon G, Kuntzer T, Barakat-Walter I. Myotonic dystrophy transgenic mice exhibit pathologic abnormalities in diaphragm neuromuscular junctions and phrenic nerves. J Neuropathol Exp Neurol 2008, 67:763-772. 10.1097/NEN.0b013e318180ec64, 18648326.
10. Kunkel TA. Nucleotide repeats. Slippery DNA and diseases. Nature 1993, 365:207-208. 10.1038/365207a0, 8371775.
11. Schweitzer JK, Livingston DM. The effect of DNA replication mutations on CAG tract stability in yeast. Genetics 1999, 152:953-963. 1460650, 10388815.
12. Ireland MJ, Reinke SS, Livingston DM. The impact of lagging strand replication mutations on the stability of CAG repeat tracts in yeast. Genetics 2000, 155:1657-1665. 1461208, 10924464.
13. Hartenstine MJ, Goodman MF, Petruska J. Base stacking and even/odd behavior of hairpin loops in DNA triplet repeat slippage and expansion with DNA polymerase. J Biol Chem 2000, 275:18382-18390. 10.1074/jbc.275.24.18382, 10849445.
14. Kunkel TA. Misalignment-mediated DNA synthesis errors. Biochemistry 1990, 29:8003-8011. 10.1021/bi00487a001, 1702019.
15. Kerrest A, Anand RP, Sundararajan R, Bermejo R, Liberi G, Dujon B, Freudenreich CH, Richard GF. SRS2 and SGS1 prevent chromosomal breaks and stabilize triplet repeats by restraining recombination. Nat Struct Mol Biol 2009, 16:159-167. 10.1038/nsmb.1544, 19136956.
16. Kovtun IV, Thornhill AR, McMurray CT. Somatic deletion events occur during early embryonic development and modify the extent of CAG expansion in subsequent generations. Hum Mol Genet 2004, 13:3057-3068. 10.1093/hmg/ddh325, 15496421.
17. Miret JJ, Pessoa-Brandao L, Lahue RS. Orientation-dependent and sequence-specific expansions of CTG/CAG trinucleotide repeats in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1998, 95:12438-12443. 10.1073/pnas.95.21.12438, 22849, 9770504.
18. Gordenin DA, Kunkel TA, Resnick MA. Repeat expansion--all in a flap?. Nat Genet 1997, 16:116-118. 10.1038/ng0697-116, 9171819.
19. Callahan JL, Andrews KJ, Zakian VA, Freudenreich CH. Mutations in yeast replication proteins that increase CAG/CTG expansions also increase repeat fragility. Mol Cell Biol 2003, 23:7849-7860. 10.1128/MCB.23.21.7849-7860.2003, 207578, 14560028.
20. Kovtun IV, Liu Y, Bjoras M, Klungland A, Wilson SH, McMurray CT. OGG1 initiates age-dependent CAG trinucleotide expansion in somatic cells. Nature 2007, 447:447-452. 10.1038/nature05778, 2681094, 17450122.
21. Jarem DA, Wilson NR, Schermerhorn KM, Delaney S. Incidence and persistence of 8-oxo-7,8-dihydroguanine within a hairpin intermediate exacerbates a toxic oxidation cycle associated with trinucleotide repeat expansion. DNA Repair (Amst) 2011, 10:887-896.
22. Lahue RS, Slater DL. DNA repair and trinucleotide repeat instability. Front Biosci 2003, 8:s653-665. 10.2741/1107, 12700078.
23. Hubert L, Lin Y, Dion V, Wilson JH. Topoisomerase 1 and Single-Strand Break Repair Modulate Transcription-Induced CAG Repeat Contraction in Human Cells. Mol Cell Biol 2011, 31:3105-3112. 10.1128/MCB.05158-11, 3147608, 21628532.
24. Lin Y, Dent SY, Wilson JH, Wells RD, Napierala M. R loops stimulate genetic instability of CTG.CAG repeats. Proc Natl Acad Sci USA 2010, 107:692-697. 10.1073/pnas.0909740107, 2818888, 20080737.
25. Lin Y, Hubert L, Wilson JH. Transcription destabilizes triplet repeats. Mol Carcinog 2009, 48:350-361. 10.1002/mc.20488, 18973172.
26. Lin Y, Wilson JH. Transcription-induced CAG repeat contraction in human cells is mediated in part by transcription-coupled nucleotide excision repair. Mol Cell Biol 2007, 27:6209-6217. 10.1128/MCB.00739-07, 1952160, 17591697.
27. Nakamori M, Pearson CE, Thornton CA. Bidirectional transcription stimulates expansion and contraction of expanded (CTG)*(CAG) repeats. Hum Mol Genet 2011, 20:580-588. 10.1093/hmg/ddq501, 3016912, 21088112.
28. Wang G, Vasquez KM. Models for chromosomal replication-independent non-B DNA structure-induced genetic instability. Mol Carcinog 2009, 48:286-298. 10.1002/mc.20508, 2766916, 19123200.
29. Wang G, Vasquez KM. Non-B DNA structure-induced genetic instability. Mutat Res 2006, 598:103-119. 10.1016/j.mrfmmm.2006.01.019, 16516932.
30. Gonitel R, Moffitt H, Sathasivam K, Woodman B, Detloff PJ, Faull RL, Bates GP. DNA instability in postmitotic neurons. Proc Natl Acad Sci USA 2008, 105:3467-3472. 10.1073/pnas.0800048105, 2265187, 18299573.
31. Parniewski P, Jaworski A, Wells RD, Bowater RP. Length of CTG.CAG repeats determines the influence of mismatch repair on genetic instability. J Mol Biol 2000, 299:865-874. 10.1006/jmbi.2000.3796, 10843843.
32. Harley HG, Brook JD, Rundle SA, Crow S, Reardon W, Buckler AJ, Harper PS, Housman DE, Shaw DJ. Expansion of an unstable DNA region and phenotypic variation in myotonic dystrophy. Nature 1992, 355:545-546. 10.1038/355545a0, 1346923.
33. Aslanidis C, Jansen G, Amemiya C, Shutler G, Mahadevan M, Tsilfidis C, Chen C, Alleman J, Wormskamp NG, Vooijs M, et al. Cloning of the essential myotonic dystrophy region and mapping of the putative defect. Nature 1992, 355:548-551. 10.1038/355548a0, 1346925.
34. Buxton J, Shelbourne P, Davies J, Jones C, Van Tongeren T, Aslanidis C, de Jong P, Jansen G, Anvret M, Riley B, et al. Detection of an unstable fragment of DNA specific to individuals with myotonic dystrophy. Nature 1992, 355:547-548. 10.1038/355547a0, 1346924.
35. Mahadevan M, Tsilfidis C, Sabourin L, Shutler G, Amemiya C, Jansen G, Neville C, Narang M, Barcelo J, O'Hoy K, et al. Myotonic dystrophy mutation: an unstable CTG repeat in the 3' untranslated region of the gene. Science 1992, 255:1253-1255. 10.1126/science.1546325, 1546325.
36. Brook JD, McCurrach ME, Harley HG, Buckler AJ, Church D, Aburatani H, Hunter K, Stanton VP, Thirion JP, Hudson T, et al. Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3' end of a transcript encoding a protein kinase family member. Cell 1992, 69:385.
37. Tsilfidis C, MacKenzie AE, Mettler G, Barcelo J, Korneluk RG. Correlation between CTG trinucleotide repeat length and frequency of severe congenital myotonic dystrophy. Nat Genet 1992, 1:192-195. 10.1038/ng0692-192, 1303233.
38. Illarioshkin SN, Igarashi S, Onodera O, Markova ED, Nikolskaya NN, Tanaka H, Chabrashwili TZ, Insarova NG, Endo K, Ivanova-Smolenskaya IA, et al. Trinucleotide repeat length and rate of progression of Huntington's disease. Ann Neurol 1994, 36:630-635. 10.1002/ana.410360412, 7944295.
39. Rosenblatt A, Brinkman RR, Liang KY, Almqvist EW, Margolis RL, Huang CY, Sherr M, Franz ML, Abbott MH, Hayden MR, Ross CA. Familial influence on age of onset among siblings with Huntington disease. Am J Med Genet 2001, 105:399-403. 10.1002/ajmg.1400, 11449389.
40. Brinkman RR, Mezei MM, Theilmann J, Almqvist E, Hayden MR. The likelihood of being affected with Huntington disease by a particular age, for a specific CAG size. Am J Hum Genet 1997, 60:1202-1210. 1712445, 9150168.
41. Cho DH, Tapscott SJ. Myotonic dystrophy: emerging mechanisms for DM1 and DM2. Biochim Biophys Acta 2007, 1772:195-204.
42. Otten AD, Tapscott SJ. Triplet repeat expansion in myotonic dystrophy alters the adjacent chromatin structure. Proc Natl Acad Sci USA 1995, 92:5465-5469. 10.1073/pnas.92.12.5465, 41715, 7777532.
43. Saveliev A, Everett C, Sharpe T, Webster Z, Festenstein R. DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing. Nature 2003, 422:909-913. 10.1038/nature01596, 12712207.
44. Sicot G, Gourdon G, Gomes-Pereira M. Myotonic dystrophy, when simple repeats reveal complex pathogenic entities: new findings and future challenges. Hum Mol Genet 2011, 20:R116-R123. 10.1093/hmg/ddr343, 21821673.
45. Kim SH, Pytlos MJ, Rosche WA, Sinden RR. (CAG)*(CTG) repeats associated with neurodegenerative diseases are stable in the Escherichia coli chromosome. J Biol Chem 2006, 281:27950-27955. 10.1074/jbc.M601129200, 16873366.
46. Szwarocka ST, Staczek P, Parniewski P. Chromosomal model for analysis of a long CTG/CAG tract stability in wild-type Escherichia coli and its nucleotide excision repair mutants. Can J Microbiol 2007, 53:860-868. 10.1139/W07-047, 17898841.
47. Blackwood JK, Okely EA, Zahra R, Eykelenboom JK, Leach DR. DNA tandem repeat instability in the Escherichia coli chromosome is stimulated by mismatch repair at an adjacent CAG.CTG trinucleotide repeat. Proc Natl Acad Sci USA 2010, 107:22582-22586. 10.1073/pnas.1012906108, 3012478, 21149728.
48. Zahra R, Blackwood JK, Sales J, Leach DR. Proofreading and secondary structure processing determine the orientation dependence of CAG X CTG trinucleotide repeat instability in Escherichia coli. Genetics 2007, 176:27-41. 10.1534/genetics.106.069724, 1893049, 17339223.
49. Napierala M, Bacolla A, Wells RD. Increased negative superhelical density in vivo enhances the genetic instability of triplet repeat sequences. J Biol Chem 2005, 280:37366-37376. 10.1074/jbc.M508065200, 16166072.
50. Bichara M, Wagner J, Lambert IB. Mechanisms of tandem repeat instability in bacteria. Mutat Res 2006, 598:144-163. 10.1016/j.mrfmmm.2006.01.020, 16519906.
51. Mirkin SM. DNA structures, repeat expansions and human hereditary disorders. Curr Opin Struct Biol 2006, 16:351-358. 10.1016/j.sbi.2006.05.004, 16713248.
52. Avila Figueroa A, Delaney S. Mechanistic studies of hairpin to duplex conversion for trinucleotide repeat sequences. J Biol Chem 2010, 285:14648-14657. 10.1074/jbc.M109.061853, 2863172, 20228068.
53. Figueroa AA, Cattie D, Delaney S. Structure of even/odd trinucleotide repeat sequences modulates persistence of non-B conformations and conversion to duplex. Biochemistry 2011, 50:4441-4450. 10.1021/bi200397b, 21526744.
54. Gacy AM, Goellner G, Juranic N, Macura S, McMurray CT. Trinucleotide repeats that expand in human disease form hairpin structures in vitro. Cell 1995, 81:533-540. 10.1016/0092-8674(95)90074-8, 7758107.
55. Gacy AM, McMurray CT. Influence of hairpins on template reannealing at trinucleotide repeat duplexes: a model for slipped DNA. Biochemistry 1998, 37:9426-9434. 10.1021/bi980157s, 9649325.
56. Zheng GX, Sinden RR. Effect of base composition at the center of inverted repeated DNA sequences on cruciform transitions in DNA. J Biol Chem 1988, 263:5356-5361.
57. Panyutin IG, Hsieh P. Formation of a single base mismatch impedes spontaneous DNA branch migration. J Mol Biol 1993, 230:413-424. 10.1006/jmbi.1993.1159, 8464057.
58. Cote AG, Lewis SM. Mus81-dependent double-strand DNA breaks at in vivo-generated cruciform structures in S. cerevisiae. Mol Cell 2008, 31:800-812. 10.1016/j.molcel.2008.08.025, 18922464.
59. Panigrahi GB, Cleary JD, Pearson CE. In vitro (CTG)*(CAG) expansions and deletions by human cell extracts. J Biol Chem 2002, 277:13926-13934. 10.1074/jbc.M109761200, 11832482.
60. Ilves I, Petojevic T, Pesavento JJ, Botchan MR. Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol Cell 2010, 37:247-258. 10.1016/j.molcel.2009.12.030, 20122406.
61. Costa A, Ilves I, Tamberg N, Petojevic T, Nogales E, Botchan MR, Berger JM. The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat Struct Mol Biol 2011, 18:471-477. 10.1038/nsmb.2004, 21378962.
62. Delagoutte E, Goellner GM, Guo J, Baldacci G, McMurray CT. Single-stranded DNA-binding protein in vitro eliminates the orientation-dependent impediment to polymerase passage on CAG/CTG repeats. J Biol Chem 2008, 283:13341-13356. 10.1074/jbc.M800153200, 2442361, 18263578.
63. Petruska J, Hartenstine MJ, Goodman MF. Analysis of strand slippage in DNA polymerase expansions of CAG/CTG triplet repeats associated with neurodegenerative disease. J Biol Chem 1998, 273:5204-5210. 10.1074/jbc.273.9.5204, 9478975.
64. Leclercq S, Rivals E, Jarne P. DNA slippage occurs at microsatellite loci without minimal threshold length in humans: a comparative genomic approach. Genome Biol Evol 2010, 2:325-335. 10.1093/gbe/evq023, 2997547, 20624737.
65. Panigrahi GB, Lau R, Montgomery SE, Leonard MR, Pearson CE. Slipped (CTG)*(CAG) repeats can be correctly repaired, escape repair or undergo error-prone repair. Nat Struct Mol Biol 2005, 12:654-662. 10.1038/nsmb959, 16025129.
66. Zhang Y, Yuan F, Presnell SR, Tian K, Gao Y, Tomkinson AE, Gu L, Li GM. Reconstitution of 5'-directed human mismatch repair in a purified system. Cell 2005, 122:693-705. 10.1016/j.cell.2005.06.027, 16143102.
67. Hou C, Zhang T, Tian L, Huang J, Gu L, Li GM. The Role of XPG in Processing (CAG)n/(CTG)n DNA Hairpins. Cell Biosci 2011, 1:11. 10.1186/2045-3701-1-11, 3125201, 21711735.
68. Hou C, Chan NL, Gu L, Li GM. Incision-dependent and error-free repair of (CAG)(n)/(CTG)(n) hairpins in human cell extracts. Nat Struct Mol Biol 2009, 16:869-875. 10.1038/nsmb.1638, 19597480.
69. Panigrahi GB, Slean MM, Simard JP, Gileadi O, Pearson CE. Isolated short CTG/CAG DNA slip-outs are repaired efficiently by hMutSbeta, but clustered slip-outs are poorly repaired. Proc Natl Acad Sci USA 2010, 107:12593-12598. 10.1073/pnas.0909087107, 2906547, 20571119.
70. Gomes-Pereira M, Fortune MT, Ingram L, McAbney JP, Monckton DG. Pms2 is a genetic enhancer of trinucleotide CAG.CTG repeat somatic mosaicism: implications for the mechanism of triplet repeat expansion. Hum Mol Genet 2004, 13:1815-1825. 10.1093/hmg/ddh186, 15198993.
71. Manley K, Shirley TL, Flaherty L, Messer A. Msh2 deficiency prevents in vivo somatic instability of the CAG repeat in Huntington disease transgenic mice. Nat Genet 1999, 23:471-473. 10.1038/70598, 10581038.
72. Wheeler VC, Lebel LA, Vrbanac V, Teed A, te Riele H, MacDonald ME. Mismatch repair gene Msh2 modifies the timing of early disease in Hdh(Q111) striatum. Hum Mol Genet 2003, 12:273-281. 10.1093/hmg/ddg056, 12554681.
73. Bhattacharyya S, Lahue RS. Srs2 helicase of Saccharomyces cerevisiae selectively unwinds triplet repeat DNA. J Biol Chem 2005, 280:33311-33317. 10.1074/jbc.M503325200, 16085654.
74. Daee DL, Mertz T, Lahue RS. Postreplication repair inhibits CAG.CTG repeat expansions in Saccharomyces cerevisiae. Mol Cell Biol 2007, 27:102-110. 10.1128/MCB.01167-06, 1800661, 17060452.
75. Pelletier R, Krasilnikova MM, Samadashwily GM, Lahue R, Mirkin SM. Replication and expansion of trinucleotide repeats in yeast. Mol Cell Biol 2003, 23:1349-1357. 10.1128/MCB.23.4.1349-1357.2003, 141142, 12556494.
76. Razidlo DF, Lahue RS. Mrc1, Tof1 and Csm3 inhibit CAG.CTG repeat instability by at least two mechanisms. DNA Repair (Amst) 2008, 7:633-640.
77. Freudenreich CH, Lahiri M. Structure-forming CAG/CTG repeat sequences are sensitive to breakage in the absence of Mrc1 checkpoint function and S-phase checkpoint signaling: implications for trinucleotide repeat expansion diseases. Cell Cycle 2004, 3:1370-1374. 10.4161/cc.3.11.1246, 15483399.
78. Lahiri M, Gustafson TL, Majors ER, Freudenreich CH. Expanded CAG repeats activate the DNA damage checkpoint pathway. Mol Cell 2004, 15:287-293. 10.1016/j.molcel.2004.06.034, 15260979.
79. Yang J, Freudenreich CH. Haploinsufficiency of yeast FEN1 causes instability of expanded CAG/CTG tracts in a length-dependent manner. Gene 2007, 393:110-115. 10.1016/j.gene.2007.01.025, 1904339, 17383831.
80. Krasilnikova MM, Mirkin SM. Replication stalling at Friedreich's ataxia (GAA)n repeats in vivo. Mol Cell Biol 2004, 24:2286-2295. 10.1128/MCB.24.6.2286-2295.2004, 355872, 14993268.
81. Shishkin AA, Voineagu I, Matera R, Cherng N, Chernet BT, Krasilnikova MM, Narayanan V, Lobachev KS, Mirkin SM. Large-scale expansions of Friedreich's ataxia GAA repeats in yeast. Mol Cell 2009, 35:82-92. 10.1016/j.molcel.2009.06.017, 2722067, 19595718.
82. Voineagu I, Surka CF, Shishkin AA, Krasilnikova MM, Mirkin SM. Replisome stalling and stabilization at CGG repeats, which are responsible for chromosomal fragility. Nat Struct Mol Biol 2009, 16:226-228. 10.1038/nsmb.1527, 2837601, 19136957.
83. Miret JJ, Pessoa-Brandao L, Lahue RS. Instability of CAG and CTG trinucleotide repeats in Saccharomyces cerevisiae. Mol Cell Biol 1997, 17:3382-3387. 232191, 9154837.
84. Spiro C, Pelletier R, Rolfsmeier ML, Dixon MJ, Lahue RS, Gupta G, Park MS, Chen X, Mariappan SV, McMurray CT. Inhibition of FEN-1 processing by DNA secondary structure at trinucleotide repeats. Mol Cell 1999, 4:1079-1085. 10.1016/S1097-2765(00)80236-1, 10635332.
85. Bhattacharyya S, Lahue RS. Saccharomyces cerevisiae Srs2 DNA helicase selectively blocks expansions of trinucleotide repeats. Mol Cell Biol 2004, 24:7324-7330. 10.1128/MCB.24.17.7324-7330.2004, 507003, 15314145.
86. Wells RD, Ashizawa T. Genetic instabilities and neurological diseases 2006, Amsterdam; Boston: Elsevier, 2.
87. Wolff RK, Plaetke R, Jeffreys AJ, White R. Unequal crossingover between homologous chromosomes is not the major mechanism involved in the generation of new alleles at VNTR loci. Genomics 1989, 5:382-384. 10.1016/0888-7543(89)90076-1, 2571584.
88. Casper AM, Nghiem P, Arlt MF, Glover TW. ATR regulates fragile site stability. Cell 2002, 111:779-789. 10.1016/S0092-8674(02)01113-3, 12526805.
89. Durkin SG, Glover TW. Chromosome fragile sites. Annu Rev Genet 2007, 41:169-192. 10.1146/annurev.genet.41.042007.165900, 17608616.
90. Sundararajan R, Gellon L, Zunder RM, Freudenreich CH. Double-strand break repair pathways protect against CAG/CTG repeat expansions, contractions and repeat-mediated chromosomal fragility in Saccharomyces cerevisiae. Genetics 2010, 184:65-77. 10.1534/genetics.109.111039, 2815931, 19901069.
91. Gellon L, Razidlo DF, Gleeson O, Verra L, Schulz D, Lahue RS, Freudenreich CH. New functions of Ctf18-RFC in preserving genome stability outside its role in sister chromatid cohesion. PLoS Genet 2011, 7:e1001298. 10.1371/journal.pgen.1001298, 3037408, 21347277.
92. Bermudez VP, Maniwa Y, Tappin I, Ozato K, Yokomori K, Hurwitz J. The alternative Ctf18-Dcc1-Ctf8-replication factor C complex required for sister chromatid cohesion loads proliferating cell nuclear antigen onto DNA. Proc Natl Acad Sci USA 2003, 100:10237-10242. 10.1073/pnas.1434308100, 193545, 12930902.
93. Bylund GO, Burgers PM. Replication protein A-directed unloading of PCNA by the Ctf18 cohesion establishment complex. Mol Cell Biol 2005, 25:5445-5455. 10.1128/MCB.25.13.5445-5455.2005, 1156988, 15964801.
94. Lou H, Komata M, Katou Y, Guan Z, Reis CC, Budd M, Shirahige K, Campbell JL. Mrc1 and DNA polymerase epsilon function together in linking DNA replication and the S phase checkpoint. Mol Cell 2008, 32:106-117. 10.1016/j.molcel.2008.08.020, 2699584, 18851837.
95. Tourriere H, Pasero P. Maintenance of fork integrity at damaged DNA and natural pause sites. DNA Repair (Amst) 2007, 6:900-913.
96. Tourriere H, Versini G, Cordon-Preciado V, Alabert C, Pasero P. Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol Cell 2005, 19:699-706. 10.1016/j.molcel.2005.07.028, 16137625.
97. Gambus A, van Deursen F, Polychronopoulos D, Foltman M, Jones RC, Edmondson RD, Calzada A, Labib K. A key role for Ctf4 in coupling the MCM2-7 helicase to DNA polymerase alpha within the eukaryotic replisome. EMBO J 2009, 28:2992-3004. 10.1038/emboj.2009.226, 2760104, 19661920.
98. Miles J, Formosa T. Evidence that POB1, a Saccharomyces cerevisiae protein that binds to DNA polymerase alpha, acts in DNA metabolism in vivo. Mol Cell Biol 1992, 12:5724-5735. 360512, 1448101.
99. Ricke RM, Bielinsky AK. Mcm10 regulates the stability and chromatin association of DNA polymerase-alpha. Mol Cell 2004, 16:173-185. 10.1016/j.molcel.2004.09.017, 15494305.
100. Kouprina N, Kroll E, Bannikov V, Bliskovsky V, Gizatullin R, Kirillov A, Shestopalov B, Zakharyev V, Hieter P, Spencer F, et al. CTF4 (CHL15) mutants exhibit defective DNA metabolism in the yeast Saccharomyces cerevisiae. Mol Cell Biol 1992, 12:5736-5747. 360513, 1341195.
101. Warren CD, Eckley DM, Lee MS, Hanna JS, Hughes A, Peyser B, Jie C, Irizarry R, Spencer FA. S-phase checkpoint genes safeguard high-fidelity sister chromatid cohesion. Mol Biol Cell 2004, 15:1724-1735. 10.1091/mbc.E03-09-0637, 379270, 14742710.
102. van den Broek WJ, Nelen MR, Wansink DG, Coerwinkel MM, te Riele H, Groenen PJ, 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 2002, 11:191-198. 10.1093/hmg/11.2.191, 11809728.
103. Gomes-Pereira M, Foiry L, Nicole A, Huguet A, Junien C, Munnich A, Gourdon G. CTG trinucleotide repeat "big jumps": large expansions, small mice. PLoS Genet 2007, 3:e52. 10.1371/journal.pgen.0030052, 1847694, 17411343.
104. Fortune MT, Vassilopoulos C, Coolbaugh MI, Siciliano MJ, Monckton DG. Dramatic, expansion-biased, age-dependent, tissue-specific somatic mosaicism in a transgenic mouse model of triplet repeat instability. Hum Mol Genet 2000, 9:439-445. 10.1093/hmg/9.3.439, 10655554.
105. Usdin K. Bending the rules: unusual nucleic acid structures and disease pathology in the repeat expansion diseases. Genetic instabilities and neurological diseases 2006, Amsterdam; Boston: Elsevier, Wells RD, Ashizawa T, 617-635.
106. Shelbourne PF, Monckton DG. Somatic mosaicism of expanded CAG/CTG repeats in humans and mice: and consequences. Genetic instabilities and neurological diseases 2006, 537-561. Amsterdam; Boston: Elsevier, Wells RD, Ashizawa T.
107. Gomes-Pereira M, Foiry L, Gourdon G. Transgenic mouse models of unstable trinucleotide repeats: towards an understanding of disease-associated repeat size mutation. Genetic instabilities and neurological diseases 2006, 563-586. Amsterdam; Boston: Elsevier, Wells RD, Ashizawa T, 2.
108. Savouret C, Junien C, Gourdon G. Analysis of CTG repeats using DM1 model mice. Methods Mol Biol 2004, 277:185-197.
109. Kovtun IV, McMurray CT. Models of repair underlying trinucleotide DNA expansion. Genetic instabilities and neurological diseases 2006, 679-690. Amsterdam; Boston: Elsevier, Wells RD, Ashizawa T, 2.
110. Seznec H, Agbulut O, Sergeant N, Savouret C, Ghestem A, Tabti N, Willer JC, Ourth L, Duros C, Brisson E, et al. Mice transgenic for the human myotonic dystrophy region with expanded CTG repeats display muscular and brain abnormalities. Hum Mol Genet 2001, 10:2717-2726. 10.1093/hmg/10.23.2717, 11726559.
111. Kumari D, Usdin K. Chromatin remodeling in the noncoding repeat expansion diseases. J Biol Chem 2009, 284:7413-7417. 10.1074/jbc.R800026200, 2658035, 18957431.
112. Kumari D, Biacsi RE, Usdin K. Repeat expansion affects both transcription initiation and elongation in friedreich ataxia cells. J Biol Chem 2011, 286:4209-4215. 10.1074/jbc.M110.194035, 3039332, 21127046.
113. Cho DH, Thienes CP, Mahoney SE, Analau E, Filippova GN, Tapscott SJ. Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol Cell 2005, 20:483-489. 10.1016/j.molcel.2005.09.002, 16285929.
114. Libby RT, Hagerman KA, Pineda VV, Lau R, Cho DH, Baccam SL, Axford MM, Cleary JD, Moore JM, Sopher BL, et al. CTCF cis-regulates trinucleotide repeat instability in an epigenetic manner: a novel basis for mutational hot spot determination. PLoS Genet 2008, 4:e1000257. 10.1371/journal.pgen.1000257, 2573955, 19008940.
115. Libby RT, Monckton DG, Fu YH, Martinez RA, McAbney JP, Lau R, Einum DD, Nichol K, Ware CB, Ptacek LJ, et al. Genomic context drives SCA7 CAG repeat instability, while expressed SCA7 cDNAs are intergenerationally and somatically stable in transgenic mice. Hum Mol Genet 2003, 12:41-50. 10.1093/hmg/ddg006, 12490531.
116. Savouret C, Garcia-Cordier C, Megret J, te Riele H, Junien C, Gourdon G. MSH2-dependent germinal CTG repeat expansions are produced continuously in spermatogonia from DM1 transgenic mice. Mol Cell Biol 2004, 24:629-637. 10.1128/MCB.24.2.629-637.2004, 343816, 14701736.
117. Seznec H, Lia-Baldini AS, Duros C, Fouquet C, Lacroix C, Hofmann-Radvanyi H, Junien C, Gourdon G. Transgenic mice carrying large human genomic sequences with expanded CTG repeat mimic closely the DM CTG repeat intergenerational and somatic instability. Hum Mol Genet 2000, 9:1185-1194. 10.1093/hmg/9.8.1185, 10767343.
118. Lia AS, Seznec H, Hofmann-Radvanyi H, Radvanyi F, Duros C, Saquet C, Blanche M, Junien C, 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 1998, 7:1285-1291. 10.1093/hmg/7.8.1285, 9668171.
119. Mangiarini L, Sathasivam K, Mahal A, Mott R, Seller M, Bates GP. Instability of highly expanded CAG repeats in mice transgenic for the Huntington's disease mutation. Nat Genet 1997, 15:197-200. 10.1038/ng0297-197, 9020849.
120. Wahba L, Amon JD, Koshland D, Vuica-Ross M. RNase H and Multiple RNA Biogenesis Factors Cooperate to Prevent RNA:DNA Hybrids from Generating Genome Instability. Mol Cell 2011, 44:978-988. 10.1016/j.molcel.2011.10.017, 22195970.
121. Helmrich A, Ballarino M, Tora L. Collisions between Replication and Transcription Complexes Cause Common Fragile Site Instability at the Longest Human Genes. Mol Cell 2011, 44:966-977. 10.1016/j.molcel.2011.10.013, 22195969.
122. Ljungman M. The transcription stress response. Cell Cycle 2007, 6:2252-2257. 10.4161/cc.6.18.4751, 17700065.
123. Entezam A, Usdin K. ATM and ATR protect the genome against two different types of tandem repeat instability in Fragile X premutation mice. Nucleic Acids Res 2009, 37:6371-6377. 10.1093/nar/gkp666, 2770655, 19710035.
124. Entezam A, Usdin K. ATR protects the genome against CGG.CCG-repeat expansion in Fragile X premutation mice. Nucleic Acids Res 2008, 36:1050-1056. 2241920, 18160412.
125. Lin Y, Leng M, Wan M, Wilson JH. Convergent transcription through a long CAG tract destabilizes repeats and induces apoptosis. Mol Cell Biol 2010, 30:4435-4451. 10.1128/MCB.00332-10, 2937530, 20647539.
126. Lin Y, Wilson JH. Diverse effects of individual mismatch repair components on transcription-induced CAG repeat instability in human cells. DNA Repair (Amst) 2009, 8:878-885.
127. Lin Y, Wilson JH. Transcription-induced DNA toxicity at trinucleotide repeats: double bubble is trouble. Cell Cycle 2011, 10:611-618. 10.4161/cc.10.4.14729, 3173998, 21293182.
128. Reddy K, Tam M, Bowater RP, Barber M, Tomlinson M, Nichol Edamura K, Wang YH, Pearson CE. Determinants of R-loop formation at convergent bidirectionally transcribed trinucleotide repeats. Nucleic Acids Res 2011, 39:1749-1762. 10.1093/nar/gkq935, 3061079, 21051337.
129. Reddy S, Paul S. Cis effects of CTG expansion in myotonic dystrophy type 1. Genetic instabilities and neurological diseases 2006, 55-78. Amsterdam; Boston: Elsevier, Wells RD, Ashizawa T, 2.
130. Tome S, Holt I, Edelmann W, Morris GE, Munnich A, Pearson CE, Gourdon G. MSH2 ATPase domain mutation affects CTG*CAG repeat instability in transgenic mice. PLoS Genet 2009, 5:e1000482. 10.1371/journal.pgen.1000482, 2674216, 19436705.
131. Foiry L, Dong L, Savouret C, Hubert L, Riele HT, Junien C, Gourdon G. Msh3 is a limiting factor in the formation of intergenerational CTG expansions in DM1 transgenic mice. Hum Genet 2006, 119:520-526. 10.1007/s00439-006-0164-7, 16552576.
132. Modrich P, Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem 1996, 65:101-133. 10.1146/annurev.bi.65.070196.000533, 8811176.
133. Modrich P. Mechanisms in eukaryotic mismatch repair. J Biol Chem 2006, 281:30305-30309. 10.1074/jbc.R600022200, 2234602, 16905530.
134. Li GM. Mechanisms and functions of DNA mismatch repair. Cell research 2008, 18:85-98. 10.1038/cr.2007.115, 18157157.
135. Savouret C, Brisson E, Essers J, Kanaar R, Pastink A, te Riele H, Junien C, Gourdon G. CTG repeat instability and size variation timing in DNA repair-deficient mice. EMBO J 2003, 22:2264-2273. 10.1093/emboj/cdg202, 156074, 12727892.
136. Dragileva E, Hendricks A, Teed A, Gillis T, Lopez ET, Friedberg EC, Kucherlapati R, Edelmann W, Lunetta KL, MacDonald ME, Wheeler VC. Intergenerational and striatal CAG repeat instability in Huntington's disease knock-in mice involve different DNA repair genes. Neurobiol Dis 2009, 33:37-47. 10.1016/j.nbd.2008.09.014, 2811282, 18930147.
137. Owen BA, Yang Z, Lai M, Gajec M, Badger JD, Hayes JJ, Edelmann W, Kucherlapati R, Wilson TM, McMurray CT. (CAG)(n)-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition. Nat Struct Mol Biol 2005, 12:663-670. 10.1038/nsmb965, 16025128.
138. McMurray CT. Hijacking of the mismatch repair system to cause CAG expansion and cell death in neurodegenerative disease. DNA Repair (Amst) 2008, 7:1121-1134.
139. Tian L, Hou C, Tian K, Holcomb NC, Gu L, Li GM. Mismatch recognition protein MutSbeta does not hijack (CAG)n hairpin repair in vitro. J Biol Chem 2009, 284:20452-20456. 10.1074/jbc.C109.014977, 2742808, 19525234.
140. Liu Y, Prasad R, Beard WA, Hou EW, Horton JK, McMurray CT, Wilson SH. Coordination between polymerase beta and FEN1 can modulate CAG repeat expansion. J Biol Chem 2009, 284:28352-28366. 10.1074/jbc.M109.050286, 2788885, 19674974.
141. Spiro C, Pelletier R, Rolfsmeier ML, Dixon MJ, Lahue RS, Gupta G, Park MS, Chen X, Mariappan SV, McMurray CT. Inhibition of FEN-1 processing by DNA secondary structure at trinucleotide repeats. Mol Cell 1999, 4:1079-1085. 10.1016/S1097-2765(00)80236-1, 10635332.
142. McMurray CT. Mechanisms of trinucleotide repeat instability during human development. Nat Rev Genet 2010, 11:786-799. 3175376, 20953213.
143. van den Broek WJ, Nelen MR, van der Heijden GW, Wansink DG, Wieringa B. Fen1 does not control somatic hypermutability of the (CTG)(n)*(CAG)(n) repeat in a knock-in mouse model for DM1. FEBS Lett 2006, 580:5208-5214. 10.1016/j.febslet.2006.08.059, 16978612.
144. Spiro C, McMurray CT. Nuclease-deficient FEN-1 blocks Rad51/BRCA1-mediated repair and causes trinucleotide repeat instability. Mol Cell Biol 2003, 23:6063-6074. 10.1128/MCB.23.17.6063-6074.2003, 180932, 12917330.
145. Goula AV, Berquist BR, Wilson DM, Wheeler VC, Trottier Y, Merienne K. Stoichiometry of base excision repair proteins correlates with increased somatic CAG instability in striatum over cerebellum in Huntington's disease transgenic mice. PLoS Genet 2009, 5:e1000749. 10.1371/journal.pgen.1000749, 2778875, 19997493.
146. Lloret A, Dragileva E, Teed A, Espinola J, Fossale E, Gillis T, Lopez E, Myers RH, MacDonald ME, Wheeler VC. Genetic background modifies nuclear mutant huntingtin accumulation and HD CAG repeat instability in Huntington's disease knock-in mice. Hum Mol Genet 2006, 15:2015-2024. 10.1093/hmg/ddl125, 16687439.
147. Lee J-M, Zhang J, Su AI, Walker JR, Wiltshire T, Kang K, Dragileva E, Gillis T, Lopez ET, Boily M-J, et al. A novel approach to investigate tissue-specific trinucleotide repeat instability. BMC Systems Biology 2010, 4:29. 10.1186/1752-0509-4-29, 2856555, 20302627.
148. Tome S, Panigrahi GB, Lopez Castel A, Foiry L, Melton DW, Gourdon G, Pearson CE. Maternal germline-specific effect of DNA ligase I on CTG/CAG instability. Hum Mol Genet 2011, 20:2131-2143. 10.1093/hmg/ddr099, 21378394.
149. Mateizel I, De Temmerman N, Ullmann U, Cauffman G, Sermon K, Van de Velde H, De Rycke M, Degreef E, Devroey P, Liebaers I, Van Steirteghem A. Derivation of human embryonic stem cell lines from embryos obtained after IVF and after PGD for monogenic disorders. Hum Reprod 2006, 21:503-511.
150. Niclis JC, Trounson AO, Dottori M, Ellisdon AM, Bottomley SP, Verlinsky Y, Cram DS. Human embryonic stem cell models of Huntington disease. Reprod Biomed Online 2009, 19:106-113. 10.1016/S1472-6483(10)60053-3, 19573298.
151. De Temmerman N, Seneca S, Van Steirteghem A, Haentjens P, Van der Elst J, Liebaers I, Sermon KD. CTG repeat instability in a human embryonic stem cell line carrying the myotonic dystrophy type 1 mutation. Mol Hum Reprod 2008, 14:405-412. 10.1093/molehr/gan034, 18577525.
152. Seriola A, Spits C, Simard JP, Hilven P, Haentjens P, Pearson CE, Sermon K. Huntington's and myotonic dystrophy hESCs: down-regulated trinucleotide repeat instability and mismatch repair machinery expression upon differentiation. Hum Mol Genet 2011, 20:176-185. 10.1093/hmg/ddq456, 20935170.
153. Lin Y, Dion V, Wilson JH. Transcription promotes contraction of CAG repeat tracts in human cells. Nat Struct Mol Biol 2006, 13:179-180. 10.1038/nsmb1042, 16388310.
154. Hubert L, Lin Y, Dion V, Wilson JH. Xpa deficiency reduces CAG trinucleotide repeat instability in neuronal tissues in a mouse model of SCA1. Hum Mol Genet 2011, 20:4822-4830. 10.1093/hmg/ddr421, 21926083.
155. Cleary JD, Nichol K, Wang YH, Pearson CE. Evidence of cis-acting factors in replication-mediated trinucleotide repeat instability in primate cells. Nat Genet 2002, 31:37-46. 10.1038/ng870, 11967533.
156. Hashem VI, Pytlos MJ, Klysik EA, Tsuji K, Khajavi M, Ashizawa T, Sinden RR. Chemotherapeutic deletion of CTG repeats in lymphoblast cells from DM1 patients. Nucleic Acids Res 2004, 32:6334-6346. 10.1093/nar/gkh976, 535684, 15576360.
157. Nethanel T, Kaufmann G. Two DNA polymerases may be required for synthesis of the lagging DNA strand of simian virus 40. J Virol 1990, 64:5912-5918. 248760, 2173773.
158. Burhans WC, Vassilev LT, Wu J, Sogo JM, Nallaseth FS, DePamphilis ML. Emetine allows identification of origins of mammalian DNA replication by imbalanced DNA synthesis, not through conservative nucleosome segregation. EMBO J 1991, 10:4351-4360. 453188, 1721870.
159. Mladenov E, Anachkova B. DNA breaks induction by mimosine. Z Naturforsch C 2003, 58:732-735.
160. Szuts D, Krude T. Cell cycle arrest at the initiation step of human chromosomal DNA replication causes DNA damage. J Cell Sci 2004, 117:4897-4908. 10.1242/jcs.01374, 15456844.
161. Gomes-Pereira M, Monckton DG. Chemically induced increases and decreases in the rate of expansion of a CAG*CTG triplet repeat. Nucleic Acids Res 2004, 32:2865-2872. 10.1093/nar/gkh612, 419613, 15155855.
162. Mirkin SM, Smirnova EV. Positioned to expand. Nat Genet 2002, 31:5-6. 10.1038/ng0502-5, 11984556.