Oligodeoxynucleotide Binding to (CTG) · (CAG) Microsatellite Repeats Inhibits Replication Fork Stalling, Hairpin Formation, and Genome Instability

REFERENCES

• McMurray CT. 2010. Mechanisms of trinucleotide repeat instability during human development. Nat. Rev. Genet. 11:786–799.
   PubMed Web of Science ®Google Scholar
• Mirkin SM. 2007. Expandable DNA repeats and human disease. Nature 447:932–940.
   PubMed Web of Science ®Google Scholar
• Pearson CE, Edamura KN, Cleary JD. 2005. Repeat instability: mechanisms of dynamic mutations. Nat. Rev. Genet. 6:729–742.
   PubMed Web of Science ®Google Scholar
• Figueroa AA, Cattie D, Delaney S. 2011. Structure of even/odd trinucleotide repeat sequences modulates persistence of non-B conformations and conversion to duplex. Biochemistry 50:4441–4450.
   PubMedGoogle Scholar
• Hartenstine MJ, Goodman MF, Petruska J. 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.
   PubMedGoogle Scholar
• 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 Acids Res. 26:816–823.
   PubMed Web of Science ®Google Scholar
• Petruska J, Hartenstine MJ, Goodman MF. 1998. Analysis of strand slippage in DNA polymerase expansions of CAG/CTG triplet repeats associated with neurodegenerative disease. J. Biol. Chem. 273:5204–5210.
   PubMedGoogle Scholar
• Liu G, Chen X, Bissler JJ, Sinden RR, Leffak M. 2010. Replication-dependent instability at (CTG) × (CAG) repeat hairpins in human cells. Nat. Chem. Biol. 6:652–659.
   PubMed Web of Science ®Google Scholar
• Lin Y, Leng M, Wan M, Wilson JH. 2010. Convergent transcription through a long CAG tract destabilizes repeats and induces apoptosis. Mol. Cell. Biol. 30:4435–4451.
   PubMed Web of Science ®Google Scholar
• Lenzmeier BA, Freudenreich CH. 2003. Trinucleotide repeat instability: a hairpin curve at the crossroads of replication, recombination, and repair. Cytogenet. Genome Res. 100:7–24.
   PubMedGoogle Scholar
• Owen BA, Yang Z, Lai M, Gajec M, Badger JDII, Hayes JJ, Edelmann W, Kucherlapati R, Wilson TM, McMurray CT. 2005. (CAG)(n)-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition. Nat. Struct. Mol. Biol. 12:663–670.
   PubMed Web of Science ®Google Scholar
• Tian L, Hou C, Tian K, Holcomb NC, Gu L, Li GM. 2009. Mismatch recognition protein MutSbeta does not hijack (CAG)n hairpin repair in vitro. J. Biol. Chem. 284:20452–20456.
   PubMed Web of Science ®Google Scholar
• Liu G, Malott M, Leffak M. 2003. Multiple functional elements comprise a mammalian chromosomal replicator. Mol. Cell. Biol. 23:1832–1842.
   PubMed Web of Science ®Google Scholar
• Liu G, Bissler JJ, Sinden RR, Leffak M. 2007. 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. Mol. Cell. Biol. 27:7828–7838.
   PubMed Web of Science ®Google Scholar
• Liu G, Chen X, Gao Y, Lewis T, Barthelemy J, Leffak M. 2012. Altered replication in human cells promotes DMPK (CTG)(n) · (CAG)(n) repeat instability. Mol. Cell. Biol. 32:1618–1632.
   PubMedGoogle Scholar
• Freudenreich CH, Stavenhagen JB, Zakian VA. 1997. Stability of a CTG/CAG trinucleotide repeat in yeast is dependent on its orientation in the genome. Mol. Cell. Biol. 17:2090–2098.
   PubMed Web of Science ®Google Scholar
• Pelletier R, Krasilnikova MM, Samadashwily GM, Lahue R, Mirkin SM. 2003. Replication and expansion of trinucleotide repeats in yeast. Mol. Cell. Biol. 23:1349–1357.
   PubMed Web of Science ®Google Scholar
• Mulders SA, van den Broek WJ, Wheeler TM, Croes HJ, van Kuik-Romeijn P, de Kimpe SJ, Furling D, Platenburg GJ, Gourdon G, Thornton CA, Wieringa B, Wansink DG. 2009. Triplet-repeat oligonucleotide-mediated reversal of RNA toxicity in myotonic dystrophy. Proc. Natl. Acad. Sci. U. S. A. 106:13915–13920.
   PubMed Web of Science ®Google Scholar
• Wheeler TM, Sobczak K, Lueck JD, Osborne RJ, Lin X, Dirksen RT, Thornton CA. 2009. Reversal of RNA dominance by displacement of protein sequestered on triplet repeat RNA. Science 325:336–339.
   PubMed Web of Science ®Google Scholar
• Nakamori M, Gourdon G, Thornton CA. 2011. Stabilization of expanded (CTG)*(CAG) repeats by antisense oligonucleotides. Mol. Ther. 19:2222–2227.
   PubMedGoogle Scholar
• Avila Figueroa A, Delaney S. 2010. Mechanistic studies of hairpin to duplex conversion for trinucleotide repeat sequences. J. Biol. Chem. 285:14648–14657.
   PubMedGoogle Scholar
• Yamamoto T, Moerschell RP, Wakem LP, Komar-Panicucci S, Sherman F. 1992. Strand-specificity in the transformation of yeast with synthetic oligonucleotides. Genetics 131:811–819.
   PubMed Web of Science ®Google Scholar
• Aarts M, te Riele H. 2010. Parameters of oligonucleotide-mediated gene modification in mouse ES cells. J. Cell. Mol. Med. 14:1657–1667.
   PubMedGoogle Scholar
• Olsen PA, Randol M, Krauss S. 2005. Implications of cell cycle progression on functional sequence correction by short single-stranded DNA oligonucleotides. Gene Ther. 12:546–551.
   PubMed Web of Science ®Google Scholar
• Aarts M, te Riele H. 2011. Progress and prospects: oligonucleotide-directed gene modification in mouse embryonic stem cells: a route to therapeutic application. Gene Ther. 18:213–219.
   PubMed Web of Science ®Google Scholar
• Radecke S, Radecke F, Peter I, Schwarz K. 2006. Physical incorporation of a single-stranded oligodeoxynucleotide during targeted repair of a human chromosomal locus. J. Gene Med. 8:217–228.
   PubMed Web of Science ®Google Scholar
• Olsen PA, Solhaug A, Booth JA, Gelazauskaite M, Krauss S. 2009. Cellular responses to targeted genomic sequence modification using single-stranded oligonucleotides and zinc-finger nucleases. DNA Repair (Amst.) 8:298–308.
   PubMedGoogle Scholar
• Lahiri M, Gustafson TL, Majors ER, Freudenreich CH. 2004. Expanded CAG repeats activate the DNA damage checkpoint pathway. Mol. Cell 15:287–293.
   PubMed Web of Science ®Google Scholar
• McMurray CT. 1999. DNA secondary structure: a common and causative factor for expansion in human disease. Proc. Natl. Acad. Sci. U. S. A. 96:1823–1825.
   PubMed Web of Science ®Google Scholar
• Malott M, Leffak M. 1999. Activity of the c-myc replicator at an ectopic chromosomal location. Mol. Cell. Biol. 19:5685–5695.
   PubMedGoogle Scholar
• Kamath S, Leffak M. 2001. Multiple sites of replication initiation in the human beta-globin gene locus. Nucleic Acids Res. 29:809–817.
   PubMedGoogle Scholar
• Gacy AM, Goellner G, Juranic N, Macura S, McMurray CT. 1995. Trinucleotide repeats that expand in human disease form hairpin structures in vitro. Cell 81:533–540.
   PubMed Web of Science ®Google Scholar
• Avila-Figueroa A, Cattie D, Delaney S. 2011. A small unstructured nucleic acid disrupts a trinucleotide repeat hairpin. Biochem. Biophys. Res. Commun. 413:532–536.
   PubMedGoogle Scholar
• Mirkin EV, Mirkin SM. 2007. Replication fork stalling at natural impediments. Microbiol. Mol. Biol. Rev. 71:13–35.
   PubMed Web of Science ®Google Scholar
• Mani M, Smith J, Kandavelou K, Berg JM, Chandrasegaran S. 2005. Binding of two zinc finger nuclease monomers to two specific sites is required for effective double-strand DNA cleavage. Biochem. Biophys. Res. Commun. 334:1191–1197.
   PubMed Web of Science ®Google Scholar
• Sander JD, Maeder ML, Reyon D, Voytas DF, Joung JK, Dobbs D. 2010. ZiFiT (zinc finger targeter): an updated zinc finger engineering tool. Nucleic Acids Res. 38:W462–W468. doi:10.1093/nar/gkq319.
   PubMed Web of Science ®Google Scholar
• Voineagu I, Freudenreich CH, Mirkin SM. 2009. Checkpoint responses to unusual structures formed by DNA repeats. Mol. Carcinog. 48:309–318.
   PubMed Web of Science ®Google Scholar
• Andreoni F, Darmon E, Poon WC, Leach DR. 2010. Overexpression of the single-stranded DNA-binding protein (SSB) stabilises CAG*CTG triplet repeats in an orientation dependent manner. FEBS Lett. 584:153–158.
   PubMedGoogle Scholar
• Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA. 2005. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 19:1040–1052.
   PubMed Web of Science ®Google Scholar
• Sogo JM, Lopes M, Foiani M. 2002. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297:599–602.
   PubMed Web of Science ®Google Scholar
• Van C, Yan S, Michael WM, Waga S, Cimprich KA. 2010. Continued primer synthesis at stalled replication forks contributes to checkpoint activation. J. Cell Biol. 189:233–246.
   PubMed Web of Science ®Google Scholar
• Walter J, Newport J. 2000. Initiation of eukaryotic DNA replication: origin unwinding and sequential chromatin association of Cdc45, RPA, and DNA polymerase alpha. Mol. Cell 5:617–627.
   PubMed Web of Science ®Google Scholar
• Liu G, Myers S, Chen X, Bissler J, Sinden R, Leffak M. 2012. Replication fork stalling and checkpoint activation by a PKD1 locus mirror repeat homopurine-homopyrimidine (Pu-Py) tract. J. Biol. Chem. 287:33412–33423.
   PubMed Web of Science ®Google Scholar
• Cheng CH, Kuchta RD. 1993. DNA polymerase epsilon: aphidicolin inhibition and the relationship between polymerase and exonuclease activity. Biochemistry 32:8568–8574.
   PubMedGoogle Scholar
• Lambert S, Froget B, Carr AM. 2007. Arrested replication fork processing: interplay between checkpoints and recombination. DNA Repair (Amst.) 6:1042–1061.
   PubMed Web of Science ®Google Scholar
• Hamdan SM, Richardson CC. 2009. Motors, switches, and contacts in the replisome. Annu. Rev. Biochem. 78:205–243.
   PubMed Web of Science ®Google Scholar
• Anand RP, Shah KA, Niu H, Sung P, Mirkin SM, Freudenreich CH. 2012. Overcoming natural replication barriers: differential helicase requirements. Nucleic Acids Res. 40:1091–1105.
   PubMed Web of Science ®Google Scholar
• Burhans WC, Vassilev LT, Wu J, Sogo JM, Nallaseth FS, DePamphilis ML. 1991. Emetine allows identification of origins of mammalian DNA replication by imbalanced DNA synthesis, not through conservative nucleosome segregation. EMBO J. 10:4351–4360.
   PubMedGoogle Scholar
• Lin Y, Wilson JH. 2011. Transcription-induced DNA toxicity at trinucleotide repeats: double bubble is trouble. Cell Cycle 10:611–618.
   PubMed Web of Science ®Google Scholar
• Brosh RMJr, Li JL, Kenny MK, Karow JK, Cooper MP, Kureekattil RP, Hickson ID, Bohr VA. 2000. Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J. Biol. Chem. 275:23500–23508.
   PubMed Web of Science ®Google Scholar
• Hyun M, Park S, Kim E, Kim DH, Lee SJ, Koo HS, Seo YS, Ahn B. 2012. Physical and functional interactions of Caenorhabditis elegans WRN-1 helicase with RPA-1. Biochemistry 51:1336–1345.
   PubMedGoogle Scholar
• Machwe A, Lozada E, Wold MS, Li GM, Orren DK. 2011. Molecular cooperation between the Werner syndrome protein and replication protein A in relation to replication fork blockage. J. Biol. Chem. 286:3497–3508.
   PubMedGoogle Scholar
• Sowd G, Wang H, Pretto D, Chazin WJ, Opresko PL. 2009. Replication protein A stimulates the Werner syndrome protein branch migration activity. J. Biol. Chem. 284:34682–34691.
   PubMedGoogle Scholar
• Kim C, Paulus BF, Wold MS. 1994. Interactions of human replication protein A with oligonucleotides. Biochemistry 33:14197–14206.
   PubMed Web of Science ®Google Scholar
• Prakash A, Kieken F, Marky LA, Borgstahl GE. 2011. Stabilization of a G-quadruplex from unfolding by replication protein a using potassium and the porphyrin TMPyP4. J. Nucleic Acids 2011:529828. doi:10.4061/2011/529828.
   PubMedGoogle Scholar
• Bacolla A, Larson JE, Collins JR, Li J, Milosavljevic A, Stenson PD, Cooper DN, Wells RD. 2008. Abundance and length of simple repeats in vertebrate genomes are determined by their structural properties. Genome Res. 18:1545–1553.
   PubMed Web of Science ®Google Scholar
• Dhar SK, Yoshida K, Machida Y, Khaira P, Chaudhuri B, Wohlschlegel JA, Leffak M, Yates J, Dutta A. 2001. Replication from oriP of Epstein-Barr virus requires human ORC and is inhibited by geminin. Cell 106:287–296.
   PubMed Web of Science ®Google Scholar