Role of mismatch repair enzymes in GAA·TTC triplet-repeat expansion in friedreich ataxia induced pluripotent stem cells

Journal of Biological Chemistry

Volumn 287, Issue 35, 2012, Pages 29861-29872

  Du, Jintang ^a   Campau, Erica ^a   Soragni, Elisabetta ^a   Ku, Sherman ^a   Puckett, James W ^b   Dervan, Peter B ^b   Gottesfeld, Joel M ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MODEL; CONSTRUCT MODELS; EMBRYONIC CELLS; GENETIC MUTATIONS; HUMAN GENOMES; IN-VITRO; MISMATCH REPAIR; MISMATCH REPAIR SYSTEMS; NEUROSPHERES; PLURIPOTENT STEM CELLS; PYRROLE-IMIDAZOLE POLYAMIDES;

CELL CULTURE; ENZYMES; EXPANSION; FIBROBLASTS; GENES; NEURODEGENERATIVE DISEASES; NEURONS; REPAIR; STEM CELLS; TRANSCRIPTION FACTORS;

GALLIUM ALLOYS;

ALANINE; CYSTEINE; GLYCINE; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN MSH2; PROTEIN MSH3; PROTEIN MSH6; PROTEIN MUTS; PROTEIN MUTS ALPHA; PROTEIN MUTS BETA; PROTEIN PRECURSOR; SHORT HAIRPIN RNA; THREONINE; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL DIVISION; CELL STRUCTURE; EMBRYO; EMBRYO CELL; ENZYME ACTIVITY; ENZYME INHIBITION; FIBROBLAST; FRIEDREICH ATAXIA; FXN GENE; GENE; GENE SILENCING; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRON; MISMATCH REPAIR; MOLECULAR LIBRARY; MOUSE; NEURAL STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRINUCLEOTIDE REPEAT;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; DNA MISMATCH REPAIR; FIBROBLASTS; FRIEDREICH ATAXIA; GENOME, HUMAN; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INTRONS; IRON-BINDING PROTEINS; MICE; MODELS, BIOLOGICAL; MUTS HOMOLOG 2 PROTEIN; NEURAL STEM CELLS; SPHEROIDS, CELLULAR; TRANSCRIPTION FACTORS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84865490878     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.391961     Document Type: Article

References (46)

1. Mirkin, S. M. (2007) Expandable DNA repeats and human disease. Nature 447, 932-940
2. Kovtun, I. V., and McMurray, C. T. (2008) Features of trinucleotide repeat instability in vivo. Cell Res. 18, 198-213
3. McMurray, C. T. (2010) Mechanisms of trinucleotide repeat instability during human development. Nat. Rev. Genet. 11, 786-799
4. Herman, D., Jenssen, K., Burnett, R., Soragni, E., Perlman, S. L., and Gottesfeld, J. M. (2006) Histone deacetylase inhibitors reverse gene silencing in Friedreich ataxia. Nat. Chem. Biol. 2, 551-558
5. Campuzano, V., Montermini, L., Moltò, M. D., Pianese, L., Cossée, M., Cavalcanti, F., Monros, E., Rodius, F., Duclos, F., Monticelli, A., Zara, F., Cañizares, J., Koutnikova, H., Bidichandani, S. I., Gellera, C., Brice, A., Trouillas, P., De Michele, G., Filla, A., De Frutos, R., Palau, F., Patel, P. I., Di Donato, S., Mandel, J. L., Cocozza, S., Koenig, M., and Pandolfo, M. (1996) Friedreich ataxia: autosomal recessive disease caused by an intronic GAA triplet-repeat expansion. Science 271, 1423-1427
6. Bidichandani, S. I., Ashizawa, T., and Patel, P. I. (1998) 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, 111-121
7. n sequence results in frequent deletion of the triplet-repeat sequence. Nucleic Acids Res. 36, 489-500
8. Kim, H. M., Narayanan, V., Mieczkowski, P. A., Petes, T. D., Krasilnikova, M. M., Mirkin, S. M., and Lobachev, K. S. (2008) Chromosome fragility at GAA tracts in yeast depends on repeat orientation and requires mismatch repair. EMBO J. 27, 2896-2906
9. Shishkin, A. A., Voineagu, I., Matera, R., Cherng, N., Chernet, B. T., Krasilnikova, M. M., Narayanan, V., Lobachev, K. S., and Mirkin, S. M. (2009) Large-scale expansions of Friedreich ataxia GAA repeats in yeast. Mol. Cell 35, 82-92
10. Rindler, P. M., and Bidichandani, S. I. (2011) Role of transcript and interplay between transcription and replication in triplet-repeat instability in mammalian cells. Nucleic Acids Res. 39, 526-535
11. Ditch, S., Sammarco, M. C., Banerjee, A., and Grabczyk, E. (2009) Progressive GAA·TTC repeat expansion in human cell lines. PLoS Genet. 5, e1000704
12. Rindler, P. M., Clark, R. M., Pollard, L. M., De Biase, I., and Bidichandani, S. I. (2006) Replication in mammalian cells recapitulates the locus-specific differences in somatic instability of genomic GAA triplet repeats. Nucleic Acids Res. 34, 6352-6361
13. Clark, R. M., De Biase, I., Malykhina, A. P., Al-Mahdawi, S., Pook, M., and Bidichandani, S. I. (2007) The GAA triplet repeat is unstable in the context of the human FXN locus and displays age-dependent expansions in cerebellum and DRG in a transgenic mouse model. Hum. Genet. 120, 633-640
14. Al-Mahdawi, S., Pinto, R. M., Ruddle, P., Carroll, C., Webster, Z., and Pook, M. (2004) GAA repeat instability in Friedreich ataxia YAC transgenic mice. Genomics 84, 301-310
15. Ezzatizadeh, V., Pinto, R. M., Sandi, C., Sandi, M., Al-Mahdawi, S., Te Riele, H., and Pook, M. A. (2012) The mismatch repair system protects against intergenerational GAA repeat instability in a Friedreich ataxia mouse model. Neurobiol. Dis. 46, 165-171
16. Ku, S., Soragni, E., Campau, E., Thomas, E. A., Altun, G., Laurent, L. C., Loring, J. F., Napierala, M., and Gottesfeld, J. M. (2010) Friedreich ataxia induced pluripotent stem cells model intergenerational GAA·TTC triplet-repeat instability. Cell Stem Cell 7, 631-637
17. Liu, J., Verma, P. J., Evans-Galea, M. V., Delatycki, M. B., Michalska, A., Leung, J., Crombie, D., Sarsero, J. P., Williamson, R., Dottori, M., and Pébay, A. (2011) Generation of induced pluripotent stem cell lines from Friedreich ataxia patients. Stem Cell Rev. 7, 703-713
18. Park, I. H., Zhao, R., West, J. A., Yabuuchi, A., Huo, H., Ince, T. A., Lerou, P. H., Lensch, M. W., and Daley, G. Q. (2008) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451, 141-146
19. Dottori, M., and Pera, M. F. (2008) Neural differentiation of human embryonic stem cells. Methods Mol. Biol. 438, 19-30
20. Zhou, J., Su, P., Li, D., Tsang, S., Duan, E., and Wang, F. (2010) High-efficiency induction of neural conversion in human ESCs and human induced pluripotent stem cells with a single chemical inhibitor of transforming growth factor β superfamily receptors. Stem Cells 28, 1741-1750
21. Chambers, S. M., Fasano, C. A., Papapetrou, E. P., Tomishima, M., Sadelain, M., and Studer, L. (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27, 275-280
22. Kim, D. S., Lee, J. S., Leem, J. W., Huh, Y. J., Kim, J. Y., Kim, H. S., Park, I. H., Daley, G. Q., Hwang, D. Y., and Kim, D. W. (2010) Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev. 6, 270-281
23. Laird, P. W., Zijderveld, A., Linders, K., Rudnicki, M. A., Jaenisch, R., and Berns, A. (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19, 4293
24. Abramoff, M. D., Magalhaes, P. J., and Ram, S. J. (2004) Image Processing with ImageJ. Biophotonics Int. 11, 36-42
25. Monckton, D. G., Wong, L. J., Ashizawa, T., and Caskey, C. T. (1995) Somatic mosaicism, germ-line expansions, germ-line reversions, and intergenerational reductions in myotonic dystrophy males: small-pool PCR analyses. Hum. Mol. Genet. 4, 1-8
26. ΔΔCT method. Methods 25, 402-408
27. Burnett, R., Melander, C., Puckett, J. W., Son, L. S., Wells, R. D., Dervan, P. B., and Gottesfeld, J. M. (2006) DNA sequence-specific polyamides alleviate transcription inhibition associated with long GAA·TTC repeats in Friedreich ataxia. Proc. Natl. Acad. Sci. U.S.A. 103, 11497-11502
28. Dickinson, L. A., Gulizia, R. J., Trauger, J. W., Baird, E. E., Mosier, D. E., Gottesfeld, J. M., and Dervan, P. B. (1998) Inhibition of RNA polymerase II transcription in human cells by synthetic DNA-binding ligands. Proc. Natl. Acad. Sci. U.S.A. 95, 12890-12895
29. Fujimoto, J., Bando, T., Minoshima, M., Uchida, S., Iwasaki, M., Shinohara, K., and Sugiyama, H. (2008) Detection of triplet repeat sequences in the double-stranded DNA using pyrene-functionalized pyrrole-imidazole polyamides with rigid linkers. Bioorg. Med. Chem. 16, 5899-5907
30. Sharma, R., Bhatti, S., Gomez, M., Clark, R. M., Murray, C., Ashizawa, T., and Bidichandani, S. I. (2002) The GAA triplet-repeat sequence in Friedreich ataxia shows a high level of somatic instability in vivo, with a significant predilection for large contractions. Hum. Mol. Genet. 11, 2175-2187
31. Gomes-Pereira, M., Bidichandani, S. I., and Monckton, D. G. (2004) Analysis of unstable triplet repeats using small-pool polymerase chain reaction. Methods Mol. Biol. 277, 61-76
32. Ding, V. M., Ling, L., Natarajan, S., Yap, M. G., Cool, S. M., and Choo, A. B. (2010) FGF-2 modulates Wnt signaling in undifferentiated hESC and iPS cells through activated PI3K/GSK3β signaling. J. Cell. Physiol. 225, 417-428
33. Sheridan, S. D., Theriault, K. M., Reis, S. A., Zhou, F., Madison, J. M., Daheron, L., Loring, J. F., and Haggarty, S. J. (2011) Epigenetic characterization of the FMR1 gene and aberrant neurodevelopment in human induced pluripotent stem cell models of fragile X syndrome. PLoS ONE 6, e26203
34. Foiry, L., Dong, L., Savouret, C., Hubert, L., te Riele, H., Junien, C., and Gourdon, G. (2006) Msh3 is a limiting factor in the formation of intergenerational CTG expansions in DM1 transgenic mice. Hum. Genet. 119, 520-526
35. Li, G. M. (2008) Mechanisms and functions of DNA mismatch repair. Cell Res. 18, 85-98
36. Jiricny, J. (2006) The multifaceted mismatch repair system. Nat. Rev. Mol. Cell Biol. 7, 335-346
37. Seriola, A., Spits, C., Simard, J. P., Hilven, P., Haentjens, P., Pearson, C. E., and Sermon, K. (2011) Huntington and myotonic dystrophy hESCs: down-regulated trinucleotide repeat instability and mismatch repair machinery expression upon differentiation. Hum. Mol. Genet. 20, 176-185
38. Marra, G., Iaccarino, I., Lettieri, T., Roscilli, G., Delmastro, P., and Jiricny, J. (1998) Mismatch repair deficiency associated with overexpression of the MSH3 gene. Proc. Natl. Acad. Sci. U.S.A. 95, 8568-8573
39. Dragileva, E., Hendricks, A., Teed, A., Gillis, T., Lopez, E. T., Friedberg, E. C., Kucherlapati, R., Edelmann, W., Lunetta, K. L., MacDonald, M. E., and Wheeler, V. C. (2009) Intergenerational and striatal CAG repeat instability in Huntington disease knock-in mice involves different DNA repair genes. Neurobiol. Dis. 33, 37-47
40. Sakamoto, N., Chastain, P. D., Parniewski, P., Ohshima, K., Pandolfo, M., Griffith, J. D., and Wells, R. D. (1999) Sticky DNA: self-association properties of long GAA·TTC repeats in R·R·Y triplex structures from Friedreich ataxia. Mol. Cell 3, 465-475
41. Napierala, M., Dere, R., Vetcher, A., and Wells, R. D. (2004) Structure-dependent recombination hot spot activity of GAA·TTC sequences from intron 1 of the Friedreich ataxia gene. J. Biol. Chem. 279, 6444-6454
42. Urbach, A. R., Love, J. J., Ross, S. A., and Dervan, P. B. (2002) Structure of a β-alanine-linked polyamide bound to a full helical turn of purine tract DNA in the 1:1 motif. J. Mol. Biol. 320, 55-71
43. Urbach, A. R., and Dervan, P. B. (2001) Toward rules for 1:1 polyamide: DNA recognition. Proc. Natl. Acad. Sci. U.S.A. 98, 4343-4348
44. Dudouet, B., Burnett, R., Dickinson, L. A., Wood, M. R., Melander, C., Belitsky, J. M., Edelson, B., Wurtz, N., Briehn, C., Dervan, P. B., and Gottesfeld, J. M. (2003) Accessibility of nuclear chromatin by DNA-binding polyamides. Chem. Biol. 10, 859-867
45. Gomes-Pereira, M., Fortune, M. T., Ingram, L., McAbney, J. P., and Monckton, D. G. (2004) Pms2 is a genetic enhancer of trinucleotide CAG·CTG repeat somatic mosaicism: implications for the mechanism of triplet-repeat expansion. Hum. Mol. Genet. 13, 1815-1825
46. Lin, Y., Dent, S. Y., Wilson, J. H., Wells, R. D., and Napierala, M. (2010) R loops stimulate genetic instability of CTG·CAG repeats. Proc. Natl. Acad. Sci. U.S.A. 107, 692-697