Animal and cellular models of Friedreich ataxia

Journal of Neurochemistry

Volumn 126, Issue SUPPL.1, 2013, Pages 65-79

  Perdomini, Morgane ^a,b,c,d,e   Hick, Aurore ^a,b,c,d,e   Puccio, Hélène ^a,b,c,d,e   Pook, Mark A ^f  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e The Collège de France   (France)

^f BRUNEL UNIVERSITY   (United Kingdom)

Author keywords

frataxin; Friedreich ataxia; GAA repeat expansion; induced pluripotent stem cells; mismatch repair; mouse model

Indexed keywords

ACONITATE HYDRATASE; ADENINE; CD71 ANTIGEN; CRE RECOMBINASE; CREATINE KINASE; DEFERIPRONE; FERRITIN; FERROPORTIN 1; FRATAXIN; GUANINE; HISTONE DEACETYLASE INHIBITOR; IDEBENONE; LIPOFUSCIN; NEURON SPECIFIC ENOLASE; PARVOVIRUS VECTOR; PRION PROTEIN; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; SIRTUIN 3; SMALL INTERFERING RNA; SUCCINATE DEHYDROGENASE;

CARDIOMYOPATHY; DISEASE MODEL; EPIGENETICS; FRIEDREICH ATAXIA; FXN GENE; GENE; GENE DELETION; GENE LOCUS; GENE SEQUENCE; GENE SILENCING; GENETIC IDENTIFICATION; HUMAN; HUMAN CELL CULTURE; INTRON; NEUROPATHOLOGY; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TRINUCLEOTIDE REPEAT; VIRAL GENE DELIVERY SYSTEM;

FRATAXIN; FRIEDREICH ATAXIA; GAA REPEAT EXPANSION; INDUCED PLURIPOTENT STEM CELLS; MISMATCH REPAIR; MOUSE MODEL;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; DNA REPEAT EXPANSION; EPIGENESIS, GENETIC; FRIEDREICH ATAXIA; GENE EXPRESSION; GENE SILENCING; HUMANS; IRON-BINDING PROTEINS; MICE; POINT MUTATION;

EID: 84880392298     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12219     Document Type: Review

References (117)

1. Al-Mahdawi S., Mouro Pinto R., Ruddle P., Carroll C., Webster Z., and, Pook M., (2004) GAA repeat instability in Friedreich ataxia YAC transgenic mice. Genomics 84, 301-310.
2. Al-Mahdawi S., Mouro Pinto R., Varshney D., et al,. (2006) GAA repeat expansion mutation mouse models of Friedreich ataxia exhibit oxidative stress leading to progressive neuronal and cardiac pathology. Genomics 88, 580-590.
3. Al-Mahdawi S., Mouro Pinto R., Ismail O., Varshney D., Lymperi S., Sandi C., Trabzuni D., and, Pook M., (2008) The Friedreich ataxia GAA repeat expansion mutation induces comparable epigenetic changes in human and transgenic mouse brain and heart tissues. Hum. Mol. Genet. 17, 735-746.
4. Bayot A., Santos R., Camadro J. M., and, Rustin P., (2011) Friedreich's ataxia: the vicious circle hypothesis revisited. BMC Med. 9, 112.
5. 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.
6. Bidichandani S. I., Purandare S. M., Taylor E. E., Gumin G., Machkhas H., Harati Y., Gibbs R. A., Ashizawa T., and, Patel P. I., (1999) Somatic sequence variation at the Friedreich ataxia locus includes complete contraction of the expanded GAA triplet repeat, significant length variation in serially passaged lymphoblasts and enhanced mutagenesis in the flanking sequence. Hum. Mol. Genet. 8, 2425-2436.
7. Bourn R. L., De Biase I., Pinto R. M., Sandi C., Al-Mahdawi S., Pook M. A., and, Bidichandani S. I., (2012) Pms2 Suppresses Large Expansions of the (GAA.TTC)(n) Sequence in Neuronal Tissues. PLoS ONE 7, e47085.
8. Bradley J. L., Homayoun S., Hart P. E., Schapira A. H., and, Cooper J. M., (2004) Role of oxidative damage in Friedreich's ataxia. Neurochem. Res. 29, 561-567.
9. Busi M. V., Maliandi M. V., Valdez H., Clemente M., Zabaleta E. J., Araya A., and, Gomez-Casati D. F., (2006) Deficiency of Arabidopsis thaliana frataxin alters activity of mitochondrial Fe-S proteins and induces oxidative stress. Plant J. 48, 873-882.
10. Calmels N., Schmucker S., Wattenhofer-Donze M., Martelli A., Vaucamps N., Reutenauer L., Messaddeq N., Bouton C., Koenig M., and, Puccio H., (2009a) The first cellular models based on frataxin missense mutations that reproduce spontaneously the defects associated with Friedreich ataxia. PLoS ONE 4, e6379.
11. Calmels N., Seznec H., Villa P., Reutenauer L., Hibert M., Haiech J., Rustin P., Koenig M., and, Puccio H., (2009b) Limitations in a frataxin knockdown cell model for Friedreich ataxia in a high-throughput drug screen. BMC Neurol. 9, 46.
12. Campuzano V., Montermini L., Molto M. D., et al,. (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271, 1423-1427.
13. Carpenter L., Carr C., Yang C. T., Stuckey D. J., Clarke K., and, Watt S. M., (2012) Efficient differentiation of human induced pluripotent stem cells generates cardiac cells that provide protection following myocardial infarction in the rat. Stem Cells Dev. 21, 977-986.
14. Castaldo I., Pinelli M., Monticelli A., et al,. (2008) DNA methylation in intron 1 of the frataxin gene is related to GAA repeat length and age of onset in Friedreich ataxia patients. J. Med. Genet. 45, 808-812.
15. Cimadamore F., Fishwick K., Giusto E., Gnedeva K., Cattarossi G., Miller A., Pluchino S., Brill L. M., Bronner-Fraser M., and, Terskikh A. V., (2011) Human ESC-derived neural crest model reveals a key role for SOX2 in sensory neurogenesis. Cell Stem Cell 8, 538-551.
16. 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.
17. Coppola G., Choi S. H., Santos M. M., Miranda C. J., Tentler D., Wexler E. M., Pandolfo M., and, Geschwind D. H., (2006) Gene expression profiling in frataxin deficient mice: microarray evidence for significant expression changes without detectable neurodegeneration. Neurobiol. Dis. 22, 302-311.
18. Coppola G., Marmolino D., Lu D., Wang Q., Cnop M., Rai M., Acquaviva F., Cocozza S., Pandolfo M., and, Geschwind D. H., (2009) Functional genomic analysis of frataxin deficiency reveals tissue-specific alterations and identifies the PPARgamma pathway as a therapeutic target in Friedreich's ataxia. Hum. Mol. Genet. 18, 2452-2461.
19. Correia A. R., Pastore C., Adinolfi S., Pastore A., and, Gomes C. M., (2008) Dynamics, stability and iron-binding activity of frataxin clinical mutants. FEBS J. 275, 3680-3690.
20. Cossee M., Schmitt M., Campuzano V., Reutenauer L., Moutou C., Mandel J. L., and, Koenig M., (1997) Evolution of the Friedreich's ataxia trinucleotide repeat expansion: founder effect and premutations. Proc. Natl Acad. Sci. USA 94, 7452-7457.
21. Cossee M., Durr A., Schmitt M., et al,. (1999) Friedreich's ataxia: point mutations and clinical presentation of compound heterozygotes. Ann. Neurol. 45, 200-206.
22. Cossee M., Puccio H., Gansmuller A., Koutnikova H., Dierich A., LeMeur M., Fischbeck K., Dolle P., and, Koenig M., (2000) Inactivation of the Friedreich ataxia mouse gene leads to early embryonic lethality without iron accumulation. Hum. Mol. Genet. 9, 1219-1226.
23. De Biase I., Rasmussen A., Endres D., Al-Mahdawi S., Monticelli A., Cocozza S., Pook M., and, Bidichandani S. I., (2007a) Progressive GAA expansions in dorsal root ganglia of Friedreich's ataxia patients. Ann. Neurol. 61, 55-60.
24. De Biase I., Rasmussen A., Monticelli A., Al-Mahdawi S., Pook M., Cocozza S., and, Bidichandani S. I., (2007b) Somatic instability of the expanded GAA triplet-repeat sequence in Friedreich ataxia progresses throughout life. Genomics 90, 1-5.
25. De Biase I., Chutake Y. K., Rindler P. M., and, Bidichandani S. I., (2009) Epigenetic silencing in Friedreich ataxia is associated with depletion of CTCF (CCCTC-binding factor) and antisense transcription. PLoS ONE 4, e7914.
26. De Michele G., Cavalcanti F., Criscuolo C., Pianese L., Monticelli A., Filla A., and, Cocozza S., (1998) Parental gender, age at birth and expansion length influence GAA repeat intergenerational instability in the X25 gene: pedigree studies and analysis of sperm from patients with Friedreich's ataxia. Hum. Mol. Genet. 7, 1901-1906.
27. Delatycki M. B., Paris D., Gardner R. J., Forshaw K., Nicholson G. A., Nassif N., Williamson R., and, Forrest S. M., (1998) Sperm DNA analysis in a Friedreich ataxia premutation carrier suggests both meiotic and mitotic expansion in the FRDA gene. J. Med. Genet. 35, 713-716.
28. Delatycki M. B., Knight M., Koenig M., Cossee M., Williamson R., and, Forrest S. M., (1999) G130V, a common FRDA point mutation, appears to have arisen from a common founder. Hum. Genet. 105, 343-346.
29. Denham M., Parish C. L., Leaw B., Wright J., Reid C. A., Petrou S., Dottori M., and, Thompson L. H., (2012) Neurons derived from human embryonic stem cells extend long-distance axonal projections through growth along host white matter tracts after intra-cerebral transplantation. Front. Cell. Neurosci. 6, 11.
30. Deutsch E. C., Santani A. B., Perlman S. L., Farmer J. M., Stolle C. A., Marusich M. F., and, Lynch D. R., (2010) A rapid, noninvasive immunoassay for frataxin: utility in assessment of Friedreich ataxia. Mol. Genet. Metab. 101, 238-245.
31. Ditch S., Sammarco M. C., Banerjee A., and, Grabczyk E., (2009) Progressive GAA.TTC repeat expansion in human cell lines. PLoS Genet. 5, e1000704.
32. Dow L. E., and, Lowe S. W., (2012) Life in the fast lane: mammalian disease models in the genomics era. Cell 148, 1099-1109.
33. Du J., Campau E., Soragni E., Ku S., Puckett J. W., Dervan P. B., and, Gottesfeld J. M., (2012) Role of mismatch repair enzymes in GAA.TTC triplet-repeat expansion in Friedreich ataxia induced pluripotent stem cells. J. Biol. Chem. 287, 29861-29872.
34. Durr A., Cossee M., Agid Y., Campuzano V., Mignard C., Penet C., Mandel J. L., Brice A., and, Koenig M., (1996) Clinical and genetic abnormalities in patients with Friedreich's ataxia. N. Engl. J. Med. 335, 1169-1175.
35. Emond M., Lepage G., Vanasse M., and, Pandolfo M., (2000) Increased levels of plasma malondialdehyde in Friedreich ataxia. Neurology 55, 1752-1753.
36. Evans-Galea M. V., Carrodus N., Rowley S. M., et al,. (2012) FXN methylation predicts expression and clinical outcome in Friedreich ataxia. Ann. Neurol. 71, 487-497.
37. 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.
38. Filla A., De Michele G., Cavalcanti F., Pianese L, Monticelli A., Campanella G., and, Cocozza S., (1996) The relationship between trinucleotide (GAA) repeat length and clinical features in Friedreich ataxia. Am. J. Hum. Genet. 59: 554-560.
39. Frugier T., Tiziano F. D., Cifuentes-Diaz C., Miniou P., Roblot N., Dierich A., Le Meur M., and, Melki J., (2000) Nuclear targeting defect of SMN lacking the C-terminus in a mouse model of spinal muscular atrophy. Hum. Mol. Genet. 9, 849-858.
40. Garcia-Gimenez J. L., Gimeno A., Gonzalez-Cabo P., Dasi F., Bolinches-Amoros A., Molla B., Palau F., and, Pallardo F. V., (2011) Differential expression of PGC-1alpha and metabolic sensors suggest age-dependent induction of mitochondrial biogenesis in Friedreich ataxia fibroblasts. PLoS ONE 6, e20666.
41. Gellera C., Castellotti B., Mariotti C., Mineri R., Seveso V., Didonato S., and, Taroni F., (2007) Frataxin gene point mutations in Italian Friedreich ataxia patients. Neurogenetics 8, 289-299.
42. Gottesfeld J. M., (2007) Small molecules affecting transcription in Friedreich ataxia. Pharmacol. Ther. 116, 236-248.
43. Grabczyk E., Mancuso M., and, Sammarco M. C., (2007) A persistent RNA.DNA hybrid formed by transcription of the Friedreich ataxia triplet repeat in live bacteria, and by T7 RNAP in vitro. Nucleic Acids Res. 35, 5351-5359.
44. Greene E., Mahishi L., Entezam A., Kumari D., and, Usdin K., (2007) Repeat-induced epigenetic changes in intron 1 of the frataxin gene and its consequences in Friedreich ataxia. Nucleic Acids Res. 35, 3383-3390.
45. Halabi A., Ditch S., Wang J., and, Grabczyk E., (2012) DNA mismatch repair complex MutSbeta promotes GAA.TTC repeat expansion in human cells. J. Biol. Chem. 287, 29958-29967.
46. Herman D., Jenssen K., Burnett R., Soragni E., Perlman S. L., and, Gottesfeld J. M., (2006) Histone deacetylase inhibitors reverse gene silencing in Friedreich's ataxia. Nat. Chem. Biol. 2, 551-558.
47. Hick A., Wattenhofer-Donze M., Chintawar S., et al,. (2012) Induced pluripotent stem cell derived neurons and cardiomyocytes as a model for mitochondrial defects in Friedreich's ataxia. Dis. Model. Mech. 6, Advanced Online Article. doi: 10.1242/dmm.010900.
48. Huang M. L., Becker E. M., Whitnall M., Suryo Rahmanto Y., Ponka P., and, Richardson D. R., (2009) Elucidation of the mechanism of mitochondrial iron loading in Friedreich's ataxia by analysis of a mouse mutant. Proc. Natl Acad. Sci. USA 106, 16381-16386.
49. Jauslin M. L., Wirth T., Meier T., and, Schoumacher F., (2002) A cellular model for Friedreich Ataxia reveals small-molecule glutathione peroxidase mimetics as novel treatment strategy. Hum. Mol. Genet. 11, 3055-3063.
50. Jauslin M. L., Meier T., Smith R. A., and, Murphy M. P., (2003) Mitochondria-targeted antioxidants protect Friedreich Ataxia fibroblasts from endogenous oxidative stress more effectively than untargeted antioxidants. FASEB J. 17, 1972-1974.
51. Jauslin M. L., Vertuani S., Durini E., Buzzoni L., Ciliberti N., Verdecchia S., Palozza P., Meier T., and, Manfredini S., (2007) Protective effects of Fe-Aox29, a novel antioxidant derived from a molecular combination of Idebenone and vitamin E, in immortalized fibroblasts and fibroblasts from patients with Friedreich Ataxia. Mol. Cell. Biochem. 302, 79-85.
52. Kattman S. J., Witty A. D., Gagliardi M., Dubois N. C., Niapour M., Hotta A., Ellis J., and, Keller G., (2011) Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 8, 228-240.
53. Kim E., Napierala M., and, Dent S. Y., (2011) Hyperexpansion of GAA repeats affects post-initiation steps of FXN transcription in Friedreich's ataxia. Nucleic Acids Res. 39, 8366-8377.
54. Koeppen A. H., (2011) Friedreich's ataxia: pathology, pathogenesis, and molecular genetics. J. Neurol. Sci. 303, 1-12.
55. Koeppen A. H., Michael S. C., Knutson M. D., Haile D. J., Qian J., Levi S., Santambrogio P., Garrick M. D., and, Lamarche J. B., (2007) The dentate nucleus in Friedreich's ataxia: the role of iron-responsive proteins. Acta Neuropathol. 114, 163-173.
56. Koutnikova H., Campuzano V., Foury F., Dolle P., Cazzalini O., and, Koenig M., (1997) Studies of human, mouse and yeast homologues indicate a mitochondrial function for frataxin. Nat. Genet. 16, 345-351.
57. 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's ataxia induced pluripotent stem cells model intergenerational GAATTC triplet repeat instability. Cell Stem Cell 7, 631-637.
58. Kumari D., and, Usdin K., (2012) Is Friedreich ataxia an epigenetic disorder? Clin. Epigenetics 4, 2.
59. Kumari D., Biacsi R. E., and, Usdin K., (2011) Repeat expansion affects both transcription initiation and elongation in friedreich ataxia cells. J. Biol. Chem. 286, 4209-4215.
60. Lamarche J. B., Cote M., and, Lemieux B., (1980) The cardiomyopathy of Friedreich's ataxia morphological observations in 3 cases. Can. J. Neurol. Sci. 7, 389-396.
61. Lee G., Chambers S. M., Tomishima M. J., and, Studer L., (2010) Derivation of neural crest cells from human pluripotent stem cells. Nat. Protoc. 5, 688-701.
62. Lian X., Hsiao C., Wilson G., Zhu K., Hazeltine L. B., Azarin S. M., Raval K. K., Zhang J., Kamp T. J., and, Palecek S. P., (2012) Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc. Natl Acad. Sci. USA 109, E1848-E1857.
63. Lill R., (2009) Function and biogenesis of iron-sulphur proteins. Nature 460, 831-838.
64. Lim F., Palomo G. M., Mauritz C., Gimenez-Cassina A., Illana B., Wandosell F., and, Diaz-Nido J., (2007) Functional recovery in a Friedreich's ataxia mouse model by frataxin gene transfer using an HSV-1 amplicon vector. Mol. Ther. 15, 1072-1078.
65. Liu J., Verma P. J., Evans-Galea M. V., et al,. (2011) Generation of induced pluripotent stem cell lines from Friedreich ataxia patients. Stem Cell Rev. 7, 703-713.
66. Lopez Castel A., Cleary J. D., and, Pearson C. E., (2010) Repeat instability as the basis for human diseases and as a potential target for therapy. Nat. Rev. Mol. Cell Biol. 11, 165-170.
67. Lu C., and, Cortopassi G., (2007) Frataxin knockdown causes loss of cytoplasmic iron-sulfur cluster functions, redox alterations and induction of heme transcripts. Arch. Biochem. Biophys. 457, 111-122.
68. Marmolino D., Manto M., Acquaviva F., Vergara P., Ravella A., Monticelli A., and, Pandolfo M., (2010) PGC-1alpha down-regulation affects the antioxidant response in Friedreich's ataxia. PLoS ONE 5, e10025.
69. Martelli A., Wattenhofer-Donze M., Schmucker S., Bouvet S., Reutenauer L., and, Puccio H., (2007) Frataxin is essential for extramitochondrial Fe-S cluster proteins in mammalian tissues. Hum. Mol. Genet. 16, 2651-2658.
70. Martelli A., Friedman L. S., Reutenauer L., Messaddeq N., Perlman S. L., Lynch D. R., Fedosov K., Schulz J. B., Pandolfo M., and, Puccio H., (2012) Clinical data and characterization of the liver conditional mouse model exclude neoplasia as a non-neurological manifestation associated with Friedreich's ataxia. Dis. Model. Mech. 5, 860-869.
71. Miranda C. J., Santos M. M., Ohshima K., et al,. (2002) Frataxin knockin mouse. FEBS Lett. 512, 291-297.
72. Monros E., Molto M. D., Martinez F., Canizares J., Blanca J., Vilchez J. J., Prieto F., de Frutos R., and, Palau F., (1997) Phenotype correlation and intergenerational dynamics of the Friedreich ataxia GAA trinucleotide repeat. Am. J. Hum. Genet. 61, 101-110.
73. Montermini L., Andermann E., Labuda M., et al,. (1997a) The Friedreich ataxia GAA triplet repeat: premutation and normal alleles. Hum. Mol. Genet. 6, 1261-1266.
74. Montermini L., Kish S. J., Jiralerspong S., Lamarche J. B., and, Pandolfo M., (1997b) Somatic mosaicism for Friedreich's ataxia GAA triplet repeat expansions in the central nervous system. Neurology 49, 606-610.
75. Napoli E., Morin D., Bernhardt R., Buckpitt A., and, Cortopassi G., (2007) Hemin rescues adrenodoxin, heme a and cytochrome oxidase activity in frataxin-deficient oligodendroglioma cells. Biochim. Biophys. Acta 1772, 773-780.
76. Ohshima K., Montermini L., Wells R. D., and, 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, 14588-14595.
77. Pandolfo M., (2009) Friedreich ataxia: the clinical picture. J. Neurol. 256 (Suppl 1), 3-8.
78. Payne R. M., Pride P. M., and, Babbey C. M., (2011) Cardiomyopathy of Friedreich's ataxia: use of mouse models to understand human disease and guide therapeutic development. Pediatr. Cardiol. 32, 366-378.
79. Pianese L., Cavalcanti F., De Michele G., Filla A., Campanella G., Calabrese O., Castaldo I., Monticelli A., and, Cocozza S., (1997) The effect of parental gender on the GAA dynamic mutation in the FRDA gene. Am. J. Hum. Genet. 60, 460-463.
80. Pook M. A., Al-Mahdawi S., Carroll C. J., et al,. (2001) Rescue of the Friedreich's ataxia knockout mouse by human YAC transgenesis. Neurogenetics 3, 185-193.
81. Puccio H., (2009) Multicellular models of Friedreich ataxia. J. Neurol. 256 (Suppl 1), 18-24.
82. Puccio H., Simon D., Cossee M., Criqui-Filipe P., Tiziano F., Melki J., Hindelang C., Matyas R., Rustin P., and, Koenig M., (2001) Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet. 27, 181-186.
83. Punga T., and, Buhler M., (2010) Long intronic GAA repeats causing Friedreich ataxia impede transcription elongation. EMBO. Mol. Med. 2, 120-129.
84. Rai M., Soragni E., Jenssen K., Burnett R., Herman D., Coppola G., Geschwind D. H., Gottesfeld J. M., and, Pandolfo M., (2008) HDAC inhibitors correct frataxin deficiency in a Friedreich ataxia mouse model. PLoS ONE 3, e1958.
85. Rai M., Soragni E., Chou C. J., Barnes G., Jones S., Rusche J. R., Gottesfeld J. M., and, Pandolfo M., (2010) Two new pimelic diphenylamide HDAC inhibitors induce sustained frataxin upregulation in cells from Friedreich's ataxia patients and in a mouse model. PLoS ONE 5, e8825.
86. Ristow M., Mulder H., Pomplun D., et al,. (2003) Frataxin deficiency in pancreatic islets causes diabetes due to loss of beta cell mass. J. Clin. Invest. 112, 527-534.
87. Rotig A., de Lonlay P., Chretien D., Foury F., Koenig M., Sidi D., Munnich A., and, Rustin P., (1997) Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet. 17, 215-217.
88. Rouault T. A., (2012) Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease. Dis. Model. Mech. 5, 155-164.
89. Sakamoto N., Ohshima K., Montermini L., Pandolfo M., and, Wells R. D., (2001) Sticky DNA, a self-associated complex formed at long GAA*TTC repeats in intron 1 of the frataxin gene, inhibits transcription. J. Biol. Chem. 276, 27171-27177.
90. Sandi C., Pinto R. M., Al-Mahdawi S., Ezzatizadeh V., Barnes G., Jones S., Rusche J. R., Gottesfeld J. M., and, Pook M. A., (2011) Prolonged treatment with pimelic o-aminobenzamide HDAC inhibitors ameliorates the disease phenotype of a Friedreich ataxia mouse model. Neurobiol. Dis. 42, 496-505.
91. Santos M. M., Ohshima K., and, Pandolfo M., (2001) Frataxin deficiency enhances apoptosis in cells differentiating into neuroectoderm. Hum. Mol. Genet. 10, 1935-1944.
92. Saveliev A., Everett C., Sharpe T., Webster Z., and, Festenstein R., (2003) DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing. Nature 422, 909-913.
93. Schmucker S., Martelli A., Colin F., Page A., Wattenhofer-Donze M., Reutenauer L., and, Puccio H., (2011) Mammalian frataxin: an essential function for cellular viability through an interaction with a preformed ISCU/NFS1/ISD11 iron-sulfur assembly complex. PLoS ONE 6, e16199.
94. Schulz J. B., Dehmer T., Schols L., et al,. (2000) Oxidative stress in patients with Friedreich ataxia. Neurology 55, 1719-1721.
95. Seznec H., Simon D., Monassier L., Criqui-Filipe P., Gansmuller A., Rustin P., Koenig M., and, Puccio H., (2004) Idebenone delays the onset of cardiac functional alteration without correction of Fe-S enzymes deficit in a mouse model for Friedreich ataxia. Hum. Mol. Genet. 13, 1017-1024.
96. Seznec H., Simon D., Bouton C., et al,. (2005) Friedreich ataxia: the oxidative stress paradox. Hum. Mol. Genet. 14, 463-474.
97. 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.
98. Shi F., Corrales C. E., Liberman M. C., and, Edge A. S., (2007) BMP4 induction of sensory neurons from human embryonic stem cells and reinnervation of sensory epithelium. Eur. J. Neurosci. 26, 3016-3023.
99. Simon D., Seznec H., Gansmuller A., Carelle N., Weber P., Metzger D., Rustin P., Koenig M., and, Puccio H., (2004) Friedreich ataxia mouse models with progressive cerebellar and sensory ataxia reveal autophagic neurodegeneration in dorsal root ganglia. J. Neurosci. 24, 1987-1995.
100. Stehling O., Elsasser H. P., Bruckel B., Muhlenhoff U., and, Lill R., (2004) Iron-sulfur protein maturation in human cells: evidence for a function of frataxin. Hum. Mol. Genet. 13, 3007-3015.
101. Sturm B., Bistrich U., Schranzhofer M., Sarsero J. P., Rauen U., Scheiber-Mojdehkar B., de Groot H., Ioannou P., and, Petrat F., (2005) Friedreich's ataxia, no changes in mitochondrial labile iron in human lymphoblasts and fibroblasts: a decrease in antioxidative capacity? J. Biol. Chem. 280, 6701-6708.
102. Takahashi K., and, Yamanaka S., (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
103. Takahashi T., Lord B., Schulze P. C., Fryer R. M., Sarang S. S., Gullans S. R., and, Lee R. T., (2003) Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 107, 1912-1916.
104. Thierbach R., Schulz T. J., Isken F., et al,. (2005) Targeted disruption of hepatic frataxin expression causes impaired mitochondrial function, decreased life span and tumor growth in mice. Hum. Mol. Genet. 14, 3857-3864.
105. Tsai C. L., and, Barondeau D. P., (2010) Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex. Biochemistry 49, 9132-9139.
106. Tsou A. Y., Paulsen E. K., Lagedrost S. J., Perlman S. L., Mathews K. D., Wilmot G. R., Ravina B., Koeppen A. H., and, Lynch D. R., (2011) Mortality in Friedreich ataxia. J. Neurol. Sci. 307, 46-49.
107. Ventura N., Rea S. L., and, Testi R., (2006) Long-lived C. elegans mitochondrial mutants as a model for human mitochondrial-associated diseases. Exp. Gerontol. 41, 974-991.
108. Vyas P. M., Tomamichel W. J., Pride P. M., Babbey C. M., Wang Q., Mercier J., Martin E. M., and, Payne R. M., (2012) A TAT-frataxin fusion protein increases lifespan and cardiac function in a conditional Friedreich's ataxia mouse model. Hum. Mol. Genet. 21, 1230-1247.
109. Wagner G. R., Pride P. M., Babbey C. M., and, Payne R. M., (2012) Friedreich's ataxia reveals a mechanism for coordinate regulation of oxidative metabolism via feedback inhibition of the SIRT3 deacetylase. Hum. Mol. Genet. 21, 2688-2697.
110. Wang Y., Chen G., Song T., Mao G., and, Bai H., (2010) Enhancement of cardiomyocyte differentiation from human embryonic stem cells. Sci. China Life Sci. 53, 581-589.
111. Wells R. D., (2008) DNA triplexes and Friedreich ataxia. FASEB J. 22, 1625-1634.
112. Wong A., Yang J., Cavadini P., Gellera C., Lonnerdal B., Taroni F., and, Cortopassi G., (1999) The Friedreich's ataxia mutation confers cellular sensitivity to oxidant stress which is rescued by chelators of iron and calcium and inhibitors of apoptosis. Hum. Mol. Genet. 8, 425-430.
113. Yang L., Soonpaa M. H., Adler E. D., et al,. (2008) Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 453, 524-528.
114. Yu J., Vodyanik M. A., Smuga-Otto K., et al,. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920.
115. Zanella I., Derosas M., Corrado M., Cocco E., Cavadini P., Biasiotto G., Poli M., Verardi R., and, Arosio P., (2008) The effects of frataxin silencing in HeLa cells are rescued by the expression of human mitochondrial ferritin. Biochim. Biophys. Acta 1782, 90-98.
116. Zhang H., Yang B., Mu X., et al,. (2011a) Several rAAV vectors efficiently cross the blood-brain barrier and transduce neurons and astrocytes in the neonatal mouse central nervous system. Mol. Ther. 19, 1440-1448.
117. Zhang Q., Jiang J., Han P., et al,. (2011b) Direct differentiation of atrial and ventricular myocytes from human embryonic stem cells by alternating retinoid signals. Cell Res. 21, 579-587.