Inhibition of DNA synthesis facilitates expansion of low-complexity repeats: Is strand slippage stimulated by transient local depletion of specific dNTPs?

BioEssays

Volumn 35, Issue 4, 2013, Pages 306-313

  Kuzminov, Andrei ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

DNA synthesis inhibition; DNTP pools; Repeat instability; Strand slippage; Trinucleotide repeats

Indexed keywords

DNA MINISATELLITE; MICROSATELLITE DNA; REPETITIVE DNA;

ARTICLE; DNA REPLICATION; DNA STRAND; DNA STRUCTURE; DNA SYNTHESIS INHIBITION; TANDEM REPEAT; TRINUCLEOTIDE REPEAT;

DEOXYRIBONUCLEOTIDES; DNA; DNA PRIMERS; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; MICROSATELLITE INSTABILITY; MICROSATELLITE REPEATS; MINISATELLITE REPEATS; NUCLEIC ACID CONFORMATION; TEMPLATES, GENETIC; TRINUCLEOTIDE REPEATS;

EID: 84874992775     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201200128     Document Type: Article

References (89)

1. Richards RI, Sutherland GR. 1997. Dynamic mutation: possible mechanisms and significance in human disease. Trends Biochem Sci 22: 432- 6.
2. Ashley CTJ, Warren ST. 1995. Trinucleotide repeat expansion and human disease. Annu Rev Genet 29: 703- 28.
3. Mirkin SM. 2007. Expandable DNA repeats and human disease. Nature 447: 932- 40.
4. Timchenko LT, Caskey CT. 1996. Trinucleotide repeat disorders in humans: discussions of mechanisms and medical issues. FASEB J 10: 1589- 97.
5. Usdin K, Grabczyk E. 2000. DNA repeat expansions and human disease. Cell Mol Life Sci 57: 914- 31.
6. Kurosaki T, Ueda S, Ishida T, Abe K, et al. 2012. The unstable CCTG repeat responsible for myotonic dystrophy type 2 originates from an AluSx element insertion into an early primate genome. PLoS ONE 7: e38379.
7. Buard J, Vergnaud G. 1994. Complex recombination events at the hypermutable minisatellite CEB1 (D2S90). EMBO J 13: 3203- 10.
8. Murray J, Buard J, Neil DL, Yeramian E, et al. 1999. Comparative sequence analysis of human minisatellites showing meiotic repeat instability. Genome Res 9: 130- 6.
9. Mitas M. 1997. Trinucleotide repeats associated with human disease. Nucleic Acid Res 25: 2245- 54.
10. Sinden RR. 1999. Biological implications of the DNA structures associated with disease-causing triplet repeats. Am J Hum Genet 64: 346- 53.
11. Gacy AM, Goellner GM, Spiro C, Chen X, et al. 1998. GAA instability in Friedreich's Ataxia shares a common, DNA-directed and intraallelic mechanism with other trinucleotide diseases. Mol Cell 1: 583- 93.
12. Kang S, Ohshima K, Shimizu M, Amirhaeri S, et al. 1995. Pausing of DNA synthesis in vitro at specific loci in CTG and CGG triplet repeats from human hereditary disease genes. J Biol Chem 270: 27014- 21.
13. Usdin K, Woodford KJ. 1995. CGG repeats associated with DNA instability and chromosome fragility form structures that block DNA synthesis in vitro. Nucleic Acid Res 23: 4202- 9.
14. Rolfsmeier ML, Dixon MJ, Pessoa-Brandão L, Pelletier R, et al. 2001. Cis-elements governing trinucleotide repeat instability in Saccharomyces cerevisiae. Genetics 157: 1569- 79.
15. Debrauwère H, Buard J, Tessier J, Aubert D, et al. 1999. Meiotic instability of human minisatellite CEB1 in yeast requires DNA double-strand breaks. Nat Genet 23: 367- 71.
16. Ribeyre C, Lopes J, Boulé JB, Piazza A, et al. 2009. The yeast Pif1 helicase prevents genomic instability caused by G-quadruplex-forming CEB1 sequences in vivo. PLoS Genet 5: e1000475.
17. Chandok GS, Patel MP, Mirkin SM, Krasilnikova MM. 2012. Effects of Friedreich's ataxia GAA repeats on DNA replication in mammalian cells. Nucleic Acid Res 40: 3964- 74.
18. Liu G, Chen X, Gao Y, Lewis T, et al. 2012. Altered replication in human cells promotes DMPK (CTG)(n) (CAG)(n) repeat instability. Mol Cell Biol 32: 1618- 32.
19. Ohshima K, Montermini L, Wells RD, Pandolfo M. 1998. Inhibitory effects of expanded GAA.TTC triplet repeats from intron I of the Friedreich ataxia gene on transcription and replication in vivo. J Biol Chem 273: 14588- 95.
20. Pelletier R, Krasilnikova MM, Samadashwily GM, Lahue R, et al. 2003. Replication and expansion of trinucleotide repeats in yeast. Mol Cell Biol 23: 1349- 57.
21. Samadashwily GM, Raca G, Mirkin SM. 1997. Trinucleotide repeats affect DNA replication in vivo. Nat Genet 17: 298- 304.
22. Voineagu I, Surka CF, Shishkin AA, Krasilnikova MM, et al. 2009. Replisome stalling and stabilization at CGG repeats, which are responsible for chromosomal fragility. Nat Struct Mol Biol 16: 226- 8.
23. Yang Z, Lau R, Marcadier JL, Chitayat D, et al. 2003. Replication inhibitors modulate instability of an expanded trinucleotide repeat at the myotonic dystrophy type 1 disease locus in human cells. Am J Hum Genet 73: 1092- 105.
24. Cleary JD, Pearson CE. 2005. Replication fork dynamics and dynamic mutations: the fork-shift model of repeat instability. Trends Genet 21: 272- 80.
25. Ranum LP, Chung MY, Banfi S, Bryer A, et al. 1994. Molecular and clinical correlations in spinocerebellar ataxia type I: evidence for familial effects on the age at onset. Am J Hum Genet 55: 244- 52.
26. Telenius H, Kremer HP, Theilmann J, Andrew SE, et al. 1993. Molecular analysis of juvenile Huntington disease: the major influence on (CAG)n repeat length is the sex of the affected parent. Hum Mol Genet 2: 1535- 40.
27. Murray A, Macpherson JN, Pound MC, Sharrock A, et al. 1997. The role of size, sequence and haplotype in the stability of FRAXA and FRAXE alleles during transmission. Hum Mol Genet 6: 173- 84.
28. Pizzi C, Di Maio M, Daniele S, Mastranzo P, et al. 2007. Triplet repeat instability correlates with dinucleotide instability in primary breast cancer. Oncol Rep 17: 193- 9.
29. Lavedan C, Grabczyk E, Usdin K, Nussbaum RL. 1998. Long uninterrupted CGG repeats within the first exon of the human FMR1 gene are not intrinsically unstable in transgenic mice. Genomics 50: 229- 40.
30. Wheeler VC, Auerbach W, White JK, Srinidhi J, et al. 1999. Length-dependent gametic CAG repeat instability in the Huntington's disease knock-in mouse. Hum Mol Genet 8: 115- 22.
31. Du J, Campau E, Soragni E, Ku S, et al. 2012. Role of mismatch repair enzymes in GAA-TTC triplet-repeat expansion in Friedreich's ataxia induced pluripotent stem cells (iPSCs). J Biol Chem 287: 29861- 72.
32. López Castel A, Cleary JD, Pearson CE. 2010. Repeat instability as the basis for human diseases and as a potential target for therapy. Nat Rev Mol Cell Biol 11: 165- 70.
33. Delagoutte E, Goellner GM, Guo J, Baldacci G, et al. 2008. Single-stranded DNA-binding protein in vitro eliminates the orientation-dependent impediment to polymerase passage on CAG/CTG repeats. J Biol Chem 283: 13341- 56.
34. Lopes J, Piazza A, Bermejo R, Kriegsman B, et al. 2011. G-quadruplex-induced instability during leading-strand replication. EMBO J 30: 4033- 46.
35. Iyer RR, Wells RD. 1999. Expansion and deletion of triplet repeat sequences in Escherichia coli occur on the leading strand of DNA replication. J Biol Chem 274: 3865- 77.
36. Kang S, Jaworski A, Ohshima K, Wells RD. 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- 8.
37. Petruska J, Arnheim N, Goodman MF. 1996. Stability of intrastrand hairpin structures formed by the CAG/CTG class of DNA triplet repeats associated with neurological diseases. Nucleic Acid Res 24: 1992- 8.
38. Entezam A, Usdin K. 2008. ATR protects the genome against CGG.CCG-repeat expansion in Fragile X premutation mice. Nucleic Acids Res 36: 1050- 6.
39. Gonitel R, Moffitt H, Sathasivam K, Woodman B, et al. 2008. DNA instability in postmitotic neurons. Proc Natl Acad Sci USA 105: 3467- 72.
40. Jung J, Bonini N. 2007. CREB-binding protein modulates repeat instability in a Drosophila model for polyQ disease. Science 315: 1857- 9.
41. Nakamori M, Pearson CE, Thornton CA. 2011. Bidirectional transcription stimulates expansion and contraction of expanded (CTG)*(CAG) repeats. Hum Mol Genet 20: 580- 8.
42. Ditch S, Sammarco MC, Banerjee A, Grabczyk E. 2009. Progressive GAA.TTC repeat expansion in human cell lines. PLoS Genet 5: e1000704.
43. Lin Y, Hubert LJ, Wilson JH. 2009. Transcription destabilizes triplet repeats. Mol Carcinog 48: 350- 61.
44. Kovtun IV, Liu Y, Bjoras M, Klungland A, et al. 2007. OGG1 initiates age-dependent CAG trinucleotide expansion in somatic cells. Nature 447: 447- 52.
45. Liu Y, Wilson SH. 2012. DNA base excision repair: a mechanism of trinucleotide repeat expansion. Trends Biochem Sci 37: 162- 72.
46. Cohen A, Barankiewicz J, Lederman HM, Gelfand EW. 1983. Purine and pyrimidine metabolism in human T lymphocytes. Regulation of deoxyribonucleotide metabolism. J Biol Chem 258: 12334- 40.
47. Rampazzo C, Miazzi C, Franzolin E, Pontarin G, et al. 2010. Regulation by degradation, a cellular defense against deoxyribonucleotide pool imbalances. Mutat Res 703: 2- 10.
48. Eckert KA, Yan G, Hile SE. 2002. Mutation rate and specificity analysis of tetranucleotide microsatellite DNA alleles in somatic human cells. Mol Carcinog 34: 140- 50.
49. Bichara M, Pinet I, Schumacher S, Fuchs RP. 2000. Mechanisms of dinucleotide repeat instability in Escherichia coli. Genetics 154: 533- 42.
50. Yu S, Mangelsdorf M, Hewett D, Hobson L, et al. 1997. Human chromosomal fragile site FRA16B is an amplified AT-rich minisatellite repeat. Cell 88: 367- 74.
51. Fungtammasan A, Walsh E, Chiaromonte F, Eckert KA, et al. 2012. A genome-wide analysis of common fragile sites: what features determine chromosomal instability in the human genome? Genome Res 22: 993- 1005.
52. Eckert KA, Hile SE. 2009. Every microsatellite is different: intrinsic DNA features dictate mutagenesis of common microsatellites present in the human genome. Mol Carcinog 48: 379- 88.
53. Krasilnikova MM, Samadashwily GM, Krasilnikov AS, Mirkin SM. 1998. Transcription through a simple DNA repeat blocks replication elongation. EMBO J 17: 5095- 102.
54. Panigrahi GB, Slean MM, Simard JP, Gileadi O, et al. 2010. Isolated short CTG/CAG DNA slip-outs are repaired efficiently by hMutSbeta, but clustered slip-outs are poorly repaired. Proc Natl Acad Sci USA 107: 12593- 8.
55. Goula AV, Pearson CE, Della Maria J, Trottier Y, et al. 2012. The nucleotide sequence, DNA damage location, and protein stoichiometry influence the base excision repair outcome at CAG/CTG repeats. Biochemistry 51: 3919- 32.
56. Henricksen LA, Tom S, Liu Y, Bambara RA. 2000. Inhibition of flap endonuclease 1 by flap secondary structure and relevance to repeat sequence expansion. J Biol Chem 275: 16420- 7.
57. Traut TW. 1994. Physiological concentrations of purines and pyrimidines. Mol Cell Biochem 140: 1- 22.
58. Shah KA, Shishkin AA, Voineagu I, Pavlov YI, et al. 2012. Role of DNA polymerases in repeat-mediated genome instability. Cell Rep 2: 1088- 95.
59. Hirano M, Marti R, Ferreiro-Barros C, Vilà MR, et al. 2001. Defects of intergenomic communication: autosomal disorders that cause multiple deletions and depletion of mitochondrial DNA. Semin Cell Dev Biol 12: 417- 27.
60. Mathews CK. 2006. DNA precursor metabolism and genomic stability. FASEB J 20: 1300- 14.
61. Lukusa T, Fryns JP. 2008. Human chromosome fragility. Biochim Biophys Acta 1779: 3- 16.
62. Sutherland GR. 1988. The role of nucleotides in human fragile site expression. Mutat Res 200: 207- 13.
63. Anglana M, Apiou F, Bensimon A, Debatisse M. 2003. Dynamics of DNA replication in mammalian somatic cells: nucleotide pool modulates origin choice and interorigin spacing. Cell 114: 385- 94.
64. Bjursell G, Reichard P. 1973. Effects of thymidine on deoxyribonucleoside triphosphate pools and deoxyribonucleic acid synthesis in Chinese hamster ovary cells. J Biol Chem 248: 3904- 9.
65. Malínsky J, Koberna K, Staněk D, Masata M, et al. 2001. The supply of exogenous deoxyribonucleotides accelerates the speed of the replication fork in early S-phase. J Cell Sci 114: 747- 50.
66. Zannis-Hadjopoulos M, Taylor MW, Hand R. 1980. Inhibition of DNA chain elongation in a purine-auxotrophic mutant of Chinese hamster. J Cell Biol 85: 777- 85.
67. Kumar D, Abdulovic AL, Viberg J, Nilsson AK, et al. 2011. Mechanisms of mutagenesis in vivo due to imbalanced dNTP pools. Nucleic Acid Res 39: 1360- 71.
68. Shishkin AA, Voineagu I, Matera R, Cherng N, et al. 2009. Large-scale expansions of Friedreich's ataxia GAA repeats in yeast. Mol Cell 35: 82- 92.
69. Stamatoyannopoulos JA, Adzhubei I, Thurman RE, Kryukov GV, et al. 2009. Human mutation rate associated with DNA replication timing. Nat Genet 41: 393- 5.
70. Nicander B, Reichard P. 1983. Dynamics of pyrimidine deoxynucleoside triphosphate pools in relationship to DNA synthesis in 3T6 mouse fibroblasts. Proc Natl Acad Sci USA 80: 1347- 51.
71. Wawra E. 1988. Microinjection of deoxynucleotides into mouse cells. No evidence that precursors for DNA synthesis are channeled. J Biol Chem 263: 9908- 12.
72. Pontarin G, Fijolek A, Pizzo P, Ferraro P, et al. 2008. Ribonucleotide reduction is a cytosolic process in mammalian cells independently of DNA damage. Proc Natl Acad Sci USA 105: 17801- 6.
73. Hozák P, Hassan AB, Jackson DA, Cook PR. 1993. Visualization of replication factories attached to nucleoskeleton. Cell 73: 361- 73.
74. Cseresnyes Z, Schwarz U, Green CM. 2009. Analysis of replication factories in human cells by super-resolution light microscopy. BMC Cell Biol 10: 88.
75. Liu G, Chen X, Bissler JJ, Sinden RR, et al. 2010. Replication-dependent instability at (CTG)×(CAG) repeat hairpins in human cells. Nat Chem Biol 6: 652- 9.
76. Schlötterer C, Tautz D. 1992. Slippage synthesis of simple sequence DNA. Nucleic Acid Res 20: 211- 5.
77. Lyons-Darden T, Topal MD. 1999. Abasic sites induce triplet-repeat expansion during DNA replication in vitro. J Biol Chem 274: 25975- 8.
78. Krishnamurthy N, Haraguchi K, Greenberg MM, David SS. 2008. Efficient removal of formamidopyrimidines by 8-oxoguanine glycosylases. Biochemistry 47: 1043- 50.
79. Dutra BE, Lovett ST. 2006. Cis and trans-acting effects on a mutational hotspot involving a replication template switch. J Mol Biol 356: 300- 11.
80. Ripley LS. 1982. Model for the participation of quasi-palindromic DNA sequences in frameshift mutation. Proc Natl Acad Sci USA 79: 4128- 32.
81. Schmidt KH, Abbott CM, Leach DR. 2000. Two opposing effects of mismatch repair on CTG repeat instability in Escherichia coli. Mol Microbiol 35: 463- 71.
82. Pearson CE, Sinden RR. 1996. Alternative structures in duplex DNA formed within the trinucleotide repeats of the myotonic dystrophy and fragile X loci. Biochemistry 35: 5041- 53.
83. Pearson CE, Wang YH, Griffith JD, Sinden RR. 1998. Structural analysis of slipped-strand DNA (S-DNA) formed in (CTG)n. (CAG)n repeats from the myotonic dystrophy locus. Nucleic Acid Res 26: 816- 23.
84. Franklin MC, Wang J, Steitz TA. 2001. Structure of the replicating complex of a pol alpha family DNA polymerase. Cell 105: 657- 67.
85. Mayanagi K, Kiyonari S, Nishida H, Saito M, et al. 2011. Architecture of the DNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complex. Proc Natl Acad Sci USA 108: 1845- 9.
86. Wing RA, Bailey S, Steitz TA. 2008. Insights into the replisome from the structure of a ternary complex of the DNA polymerase III alpha-subunit. J Mol Biol 382: 859- 69.
87. Yao N, Hurwitz J, O'Donnell M. 2000. Dynamics of beta and proliferating cell nuclear antigen sliding clamps in traversing DNA secondary structure. J Biol Chem 275: 1421- 32.
88. Sarkar PS, Chang HC, Boudi FB, Reddy S. 1998. CTG repeats show bimodal amplification in E. coli. Cell 95: 531- 40.
89. Reems JA, McHenry CS. 1994. Escherichia coli DNA polymerase III holoenzyme footprints three helical turns of its primer. J Biol Chem 269: 33091- 6.