Pathophysiogical and therapeutic progress in Friedreich ataxia

Revue Neurologique

Volumn 170, Issue 5, 2014, Pages 355-365

  Puccio, H ^a,b,c,d,e   Anheim, M ^a,b,c,d,f   Tranchant, C ^a,b,c,d,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 HÔPITAL DE HAUTEPIERRE   (France)

Author keywords

Frataxine; Friedreich ataxia; Mitochondria; Physiopathology; Therapeutic

Indexed keywords

ANTIOXIDANT; DEFERIPRONE; DEFEROXAMINE; FRATAXIN; HISTONE DEACETYLASE INHIBITOR; IDEBENONE; IRON CHELATING AGENT; IRON BINDING PROTEIN;

ARTICLE; CELL PROLIFERATION; FRIEDREICH ATAXIA; GENE MUTATION; GENOTYPE PHENOTYPE CORRELATION; HEART MUSCLE CELL; HUMAN; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; NUCLEOTIDE REPEAT; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; DISEASE MODEL; EXPERIMENTAL THERAPY; GENETIC PREDISPOSITION; PHYSIOLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; FRIEDREICH ATAXIA; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IRON-BINDING PROTEINS; THERAPIES, INVESTIGATIONAL;

EID: 84901044783     PISSN: 00353787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurol.2014.03.008     Document Type: Article

References (133)

1. M. Anheim, M. Fleury, B. Monga, V. Laugel, D. Chaigne, and G. Rodier et al. Epidemiological, clinical, paraclinical and molecular study of a cohort of 102 patients affected with autosomal recessive progressive cerebellar ataxia from Alsace, Eastern France: implications for clinical management Neurogenetics 11 1 2010 1 12
2. M. Anheim, C. Tranchant, and M. Koenig The autosomal recessive cerebellar ataxias N Engl J Med 366 7 2012 636 646
3. V. Campuzano, L. Montermini, M.D. Molto, L. Pianese, M. Cossee, and F. Cavalcanti et al. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion Science 271 1996 1423 1427
4. A.E. Harding Friedreich's ataxia: a clinical and genetic study of 90 families with an analysis of early diagnostic criteria and intrafamilial clustering of clinical features Brain 104 1981 589 620
5. M.B. Delatycki, D.B. Paris, R.J. Gardner, G.A. Nicholson, N. Nassif, and E. Storey et al. Clinical and genetic study of Friedreich ataxia in an Australian population Am J Med Genet 87 1999 168 174
6. A. Durr, M. Cossee, Y. Agid, V. Campuzano, C. Mignard, and C. Penet et al. Clinical and genetic abnormalities in patients with Friedreich's ataxia N Engl J Med 335 1996 1169 1175
7. A. Filla, G. DeMichele, G. Caruso, R. Marconi, and G. Campanella Genetic data and natural history of Friedreich's disease: a study of 80 Italian patients J Neurol 237 1990 345 351
8. M.H. Parkinson, S. Boesch, W. Nachbauer, C. Mariotti, and P. Giunti Clinical features of Friedreich's ataxia: classical and atypical phenotypes J Neurochem 126 Suppl. 1 2013 103 117
9. L. Schols, G. Amoiridis, H. Przuntek, G. Frank, J.T. Epplen, and C. Epplen Friedreich's ataxia. Revision of the phenotype according to molecular genetics Brain 120 1997 2131 2140
10. A.H. Koeppen, A.N. Davis, and J.A. Morral The cerebellar component of Friedreich's ataxia Acta Neuropathol 122 2011 323 330
11. A.H. Koeppen, and J.E. Mazurkiewicz Friedreich ataxia: neuropathology revised J Neuropath Exp Neurol 72 2013 78 90
12. M.C. Fahey, P.D. Cremer, S.T. Aw, L. Millist, M.J. Todd, and O.B. White et al. Vestibular, saccadic and fixation abnormalities in genetically confirmed Friedreich ataxia Brain 131 2008 1035 1045
13. F. Fortuna, P. Barboni, R. Liguori, M.L. Valentino, G. Savini, and C. Gellera et al. Visual system involvement in patients with Friedreich's ataxia Brain 132 2009 116 123
14. A. Nieto, R. Correia, E. de Nobrega, F. Monton, and J. Barroso Cognition in late-onset Friedreich ataxia Cerebellum 12 2013 504 512
15. M. Cossee, A. Durr, M. Schmitt, N. Dahl, P. Trouillas, and P. Allinson et al. Friedreich's ataxia: point mutations and clinical presentation of compound heterozygotes Ann Neurol 45 1999 200 206
16. C. Gellera, B. Castellotti, C. Mariotti, R. Mineri, V. Seveso, and S. Didonato et al. Frataxin gene point mutations in Italian Friedreich ataxia patients Neurogenetics 8 2007 289 299
17. R. Bhidayasiri, S.L. Perlman, S.M. Pulst, and D.H. Geschwind Late-onset Friedreich ataxia: phenotypic analysis, magnetic resonance imaging findings, and review of the literature Arch Neurol 62 2005 1865 1869
18. J. Berciano, I. Mateo, C. De Pablos, J.M. Polo, and O. Combarros Friedreich ataxia with minimal GAA expansion presenting as adult-onset spastic ataxia J Neurol Sci 194 2002 75 82
19. M. Anheim, L.L. Mariani, P. Calvas, E. Cheuret, F. Zagnoli, and S. Odent et al. Exonic deletions of FXN and early-onset Friedreich ataxia Arch Neurol 69 2012 912 916
20. V. Campuzano, L. Montermini, Y. Lutz, L. Cova, C. Hindelang, and S. Jiralerspong et al. Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes Hum Mol Genet 6 1997 1771 1780
21. H. Koutnikova, V. Campuzano, F. Foury, P. Dolle, O. Cazzalini, and M. Koenig Studies of human, mouse and yeast homologues indicate a mitochondrial function for frataxin Nat Genet 16 1997 345 351
22. J.M. Gottesfeld Small molecules affecting transcription in Friedreich ataxia Pharmacol Ther 116 2007 236 248
23. A. Saveliev, C. Everett, T. Sharpe, Z. Webster, and R. Festenstein DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing Nature 422 2003 909 913
24. E.C. Deutsch, A.B. Santani, S.L. Perlman, J.M. Farmer, C.A. Stolle, and M.F. Marusich et al. A rapid, noninvasive immunoassay for frataxin: utility in assessment of Friedreich ataxia Mol Genet Metab 101 2010 238 245
25. A. Filla, G. De Michele, F. Cavalcanti, L. Pianese, A. Monticelli, and G. Campanella et al. The relationship between trinucleotide (GAA) repeat length and clinical features in Friedreich ataxia Am J Hum Genet 59 1996 554 560
26. A.R. Correia, C. Pastore, S. Adinolfi, A. Pastore, and C.M. Gomes Dynamics, stability and iron-binding activity of frataxin clinical mutants Febs J 275 2008 3680 3690
27. M.V. Busi, M.V. Maliandi, H. Valdez, M. Clemente, E.J. Zabaleta, and A. Araya et al. Deficiency of Arabidopsis thaliana frataxin alters activity of mitochondrial Fe-S proteins and induces oxidative stress Plant J 48 2006 873 882
28. M. Cossee, H. Puccio, A. Gansmuller, H. Koutnikova, A. Dierich, and M. LeMeur et al. Inactivation of the Friedreich ataxia mouse gene leads to early embryonic lethality without iron accumulation Hum Mol Genet 9 2000 1219 1226
29. H. Puccio Multicellular models of Friedreich ataxia J Neurol 256 Suppl. 1 2009 18 24
30. N. Ventura, S.L. Rea, and R. Testi Long-lived C. elegans mitochondrial mutants as a model for human mitochondrial-associated diseases Exp Gerontol 41 2006 974 991
31. S. Adinolfi, M. Trifuoggi, A.S. Politou, S. Martin, and A. Pastore A structural approach to understanding the iron-binding properties of phylogenetically different frataxins Hum Mol Genet 11 2002 1865 1877
32. T.J. Gibson, E.V. Koonin, G. Musco, A. Pastore, and P. Bork Friedreich's ataxiaprotein: phylogenetic evidence for mitochondrial dysfunction Trends Neurosci 19 1996 465 468
33. I. Condo, N. Ventura, F. Malisan, A. Rufini, B. Tomassini, and R. Testi In vivo maturation of human frataxin Hum Mol Genet 16 2007 1534 1540
34. H. Koutnikova, V. Campuzano, and M. Koenig Maturation of wild-type and mutated frataxin by the mitochondrial processing peptidase Hum Mol Genet 7 1998 1485 1489
35. S. Schmucker, M. Argentini, N. Carelle-Calmels, A. Martelli, and H. Puccio The in vivo mitochondrial two-step maturation of human frataxin Hum Mol Genet 17 2008 3521 3531
36. S. Schmucker, A. Martelli, F. Colin, A. Page, M. Wattenhofer-Donze, and L. Reutenauer et al. Mammalian frataxin: an essential function for cellular viability through an interaction with a preformed ISCU/NFS1/ISD11 iron-sulfur assembly complex PLoS ONE 6 2011 e16199
37. S.J. Cho, M.G. Lee, J.K. Yang, J.Y. Lee, H.K. Song, and S.W. Suh Crystal structure of Escherichia coli CyaY protein reveals a previously unidentified fold for the evolutionarily conserved frataxin family Proc Natl Acad Sci 7 2000 8932 8937
38. S. Dhe-Paganon, R. Shigeta, Y.I. Chi, M. Ristow, and S.E. Shoelson Crystal structure of human frataxin J Biol Chem 275 2000 30753 30756
39. T. Karlberg, U. Schagerlof, O. Gakh, S. Park, U. Ryde, and M. Lindahl et al. The structures of frataxin oligomers reveal the mechanism for the delivery and detoxification of iron Structure 14 2006 1535 1546
40. G. Musco, G. Stier, B. Kolmerer, S. Adinolfi, S. Martin, and T. Frenkiel et al. Towards a structural understanding of Friedreich's ataxia: the solution structure of frataxin Structure 8 2000 695 707
41. M. Nair, S. Adinolfi, C. Pastore, G. Kelly, P. Temussi, and A. Pastore Solution structure of the bacterial frataxin ortholog, CyaY: mapping the iron binding sites Structure 12 2004 2037 2048
42. F. Prischi, P.V. Konarev, C. Iannuzzi, C. Pastore, S. Adinolfi, and S.R. Martin et al. Structural bases for the interaction of frataxin with the central components of iron-sulphur cluster assembly Nat Commun 1 2010 95
43. A.R. Correia, S. Adinolfi, A. Pastore, and C.M. Gomes Conformational stability of human frataxin and effect of Friedreich's ataxia-related mutations on protein folding Biochem J 398 2006 605 611
44. S. Adinolfi, C. Iannuzzi, F. Prischi, C. Pastore, S. Iametti, and S. Martin et al. Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS Nat Struct Mol Biol 16 2009 390 396
45. F. Colin, A. Martelli, Clemancey, J.M. Latour, S. Gambarelli, and L. Zeppieri et al. Mammalian frataxin controls sulfur production and iron entry during de novo Fe4S4 cluster assembly J Am Chem Soc 135 2013 733 740
46. M.A. Huynen, B. Snel, P. Bork, and T.J. Gibson The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly Hum Mol Genet 10 2001 2463 2468
47. U. Muhlenhoff, N. Richhardt, M. Ristow, G. Kispal, and R. Lill The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins Hum Mol Genet 11 2002 2025 2036
48. C.L. Tsai, and D.P. Barondeau Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex Biochemistry 49 2010 9132 9139
49. J.D. Cook, K.Z. Bencze, and A.D. Jankovic et al. Monomeric yeast frataxin is an iron-binding protein Biochemistry 45 2006 7767 7777
50. T. Yoon, and J.A. Cowan Iron-sulfur cluster biosynthesis. Characterization of frataxin as an iron donor for assembly of [2Fe-2S] clusters in ISU-type proteins J Am Chem Soc 125 2003 6078 6084
51. J. Gerber, U. Muhlenhoff, and R. Lill An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1 EMBO Rep 4 2003 906 911
52. J. Adamec, F. Rusnak, W.G. Owen, S. Naylor, L.M. Benson, and A.M. Gacy et al. Iron-dependent self-assembly of recombinant yeast frataxin: implications for Friedreich ataxia Am J Hum Genet 67 2000 549 562
53. G. Layer, S. Ollagnier-de Choudens, Y. Sanakis, and M. Fontecave Iron-sulfur cluster biosynthesis: characterization of Escherichia coli CYaY as an iron donor for the assembly of [2Fe-2S] clusters in the scaffold IscU J Biol Chem 281 2006 16256 16263
54. O. Gakh, S. Park, G. Liu, L. Macomber, J.A. Imlay, and G.C. Ferreira et al. Mitochondrial iron detoxification is a primary function of frataxin that limits oxidative damage and preserves cell longevity Hum Mol Genet 15 2006 467 479
55. K. Aloria, B. Schilke, A. Andrew, and E.A. Craig Iron-induced oligomerization of yeast frataxin homologue Yfh1 is dispensable in vivo EMBO Rep 5 2004 1096 1101
56. O. Gakh, T. Bedekovics, S.F. Duncan, D.Y.T. Smith, D.S. Berkholz, and G. Isaya Normal and Friedreich ataxia cells express different isoforms of frataxin with complementary roles in iron-sulfur cluster assembly J Biol Chem 285 2010 38486 38501
57. R. Lill Function and biogenesis of iron-sulphur proteins Nature 460 2009 831 838
58. H. Li, O. Gakh, D.Y.T. Smith, and G. Isaya Oligomeric yeast frataxin drives assembly of core machinery for mitochondrial iron-sulfur cluster synthesis J Biol Chem 284 2009 21971 21980
59. Y. Shan, E. Napoli, and G. Cortopassi Mitochondrial frataxin interacts with ISD11 of the NFS1/ISCU complex and multiple mitochondrial chaperones Hum Mol Genet 16 2007 929 941
60. H. Yoon, R. Golla, E. Lesuisse, J. Pain, J.E. Donald, and E.R. Lyver et al. Mutation in the Fe-S scaffold protein Isu bypasses frataxin deletion Bioch J 441 2012 473 480
61. A. Pandey, D.M. Gordon, J. Pain, T.L. Stemmler, A. Dancis, and D. Pain Frataxin directly stimulates mitochondrial cysteine desulfurase by exposing substrate-binding sites and a mutant Fe-S cluster scaffold protein with frataxin-bypassing ability acts similarly J Biol Chem 288 52 2013 36773 36786
62. A. Rotig, P. de Lonlay, D. Chretien, F. Foury, M. Koenig, and D. Sidi et al. Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia Nat Genet 17 1997 215 217
63. J.L. Bradley, S. Homayoun, P.E. Hart, A.H. Schapira, and J.M. Cooper Role of oxidative damage in Friedreich's ataxia Neurochem Res 29 2004 561 567
64. M. Emond, G. Lepage, M. Vanasse, and M. Pandolfo Increased levels of plasma malondialdehyde in Friedreich ataxia Neurology 55 2000 1752 1753
65. J.B. Schulz, T. Dehmer, and L. Schols et al. Oxidative stress in patients with Friedreich ataxia Neurology 55 2000 1719 1721
66. A. Bayot, R. Santos, J.M. Camadro, and P. Rustin Friedreich's ataxia: the vicious circle hypothesis revisited BMC Med 9 2011 112
67. I. De Biase, A. Rasmussen, A. Monticelli, S. Al-Mahdawi, M. Pook, and S. Cocozza et al. Somatic instability of the expanded GAA triplet-repeat sequence in Friedreich ataxia progresses throughout life Genomics 90 2007 1 5
68. E. Monros, M.D. Molto, F. Martinez, J. Canizares, J. Blanca, and J.J. Vilchez et al. Phenotype correlation and intergenerational dynamics of the Friedreich ataxia GAA trinucleotide repeat Am J Hum Genet 61 1997 101 110
69. R.M. Clark, I. De Biase, A.P. Malykhina, S. Al-Mahdawi, M. Pook, and S.I. Bidichandani 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 2007 633 640
70. D. Kumari, and K. Usdin Is Friedreich ataxia an epigenetic disorder? Clin Epigenet 4 2012 2
71. H. Puccio, D. Simon, M. Cossee, P. Criqui-Filipe, F. Tiziano, and J. Melki et al. Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits Nat Genet 27 2001 181 186
72. H. Seznec, D. Simon, C. Bouton, L. Reutenauer, A. Hertzog, and P. Golik et al. Friedreich ataxia: the oxidative stress paradox Hum Mol Genet 14 2005 463 474
73. A. Martelli, M. Wattenhofer-Donze, S. Schmucker, S. Bouvet, L. Reutenauer, and H. Puccio Frataxin is essential for extramitochondrial Fe-S cluster proteins in mammalian tissues Hum Mol Genet 16 2007 2651 2658
74. K. Chantrel-Groussard, V. Geromel, H. Puccio, M. Koenig, A. Munnich, and A. Rotig et al. Disabled early recruitment of antioxidant defenses in Friedreich's ataxia Hum Mol Genet 10 2001 2061 2067
75. S. Jiralerspong, B. Ge, T.J. Hudson, and M. Pandolfo Manganese superoxide dismutase induction by iron is impaired in Friedreich ataxia cells FEBS Lett 509 2001 101 105
76. G. Tozzi, M. Nuccetelli, M. Lo Bello, S. Bernardini, L. Bellincampi, and S. Ballerini et al. Antioxidant enzymes in blood of patients with Friedreich's ataxia Arch Dis Child 86 2002 376 379
77. N. Calmels, S. Schmucker, Wattenhofer-Donze, A. Martelli, N. Vaucamps, and L. Reutenauer et al. The first cellular models based on frataxin missense mutations that reproduce spontaneously the defects associated with Friedreich ataxia PLoS ONE 4 2009 e6379
78. J.V. Llorens, J.A. Navarro, M.J. Martinez-Sebastian, M.K. Baylies, S. Schneuwly, and J.A. Botella et al. Causative role of oxidative stress in a Drosophila model of Friedreich ataxia Faseb J 21 2007 333 344
79. A. Wong, J. Yang, P. Cavadini, C. Gellera, B. Lonnerdal, and F. Taroni et al. 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 1999 425 430
80. V. Paupe, E.P. Dassa, S. Goncalves, F. Auchere, M. Lonn, and A. Holmgren et al. Impaired nuclear Nrf2 translocation undermines the oxidative stress response in Friedreich ataxia PLoS ONE 4 2009 e4253
81. N.A. Di Prospero, A. Baker, N. Jeffries, and K.H. Fischbeck Neurological effects of high-dose idebenone in patients with Friedreich's ataxia: a randomised, placebo-controlled trial Lancet Neurol 6 2007 878 886
82. N.A. Di Prospero, C.J. Sumner, S.R. Penzak, B. Ravina, K.H. Fischbeck, and J.P. Taylor Safety, tolerability, and pharmacokinetics of high-dose idebenone in patients with Friedreich ataxia Arch Neurol 64 2007 803 808
83. L. Myers, J.M. Farmer, R.B. Wilson, L. Friedman, A. Tsou, and S.L. Perlman et al. Antioxidant use in Friedreich ataxia J Neurol Sci 267 2008 174 176
84. L.M. Myers, D.R. Lynch, J.M. Farmer, L.S. Friedman, J.A. Lawson, and R.B. Wilson Urinary isoprostanes in Friedreich ataxia: lack of correlation with disease features Mov Disord 23 2008 1920 1922
85. A.C. Haugen, N.A. Di Prospero, J.S. Parker, R.D. Fannin, J. Chou, and J.N. Meyer et al. Altered gene expression and DNA damage in peripheral blood cells from Friedreich's ataxia patients: cellular model of pathology PLoS Genet 6 2010 e1000812
86. J. Rudolf, V. Makrantoni, W.J. Ingledew, M.J. Stark, and M.F. White The DNA repair helicases XPD and FancJ have essential iron-sulfur domains Mol Cell 23 2006 801 808
87. M. Babcock, D. de Silva, R. Oaks, S. Davis-Kaplan, S. Jiralerspong, and L. Montermini et al. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin Science 276 1997 1709 1712
88. F. Foury, and O. Cazzalini Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria FEBS Lett 411 1997 373 377
89. R.P. Vazquez-Manrique, P. Gonzalez-Cabo, S. Ros, H. Aziz, H.A. Baylis, and F. Palau Reduction of Caenorhabditis elegans frataxin increases sensitivity to oxidative stress, reduces lifespan, and causes lethality in a mitochondrial complex II mutant FASEB J 20 2006 172 174
90. K. Zarse, T.J. Schulz, M. Birringer, and M. Ristow Impaired respiration is positively correlated with decreased life span in Caenorhabditis elegans models of Friedreich Ataxia FASEB J 21 2007 1271 1275
91. P.R. Anderson, K. Kirby, A.J. Hilliker, and J.P. Phillips RNAi-mediated suppression of the mitochondrial iron chaperone, frataxin, in Drosophila Hum Mol Genet 14 522 2005 3397 3405
92. S. Al-Mahdawi, R.M. Pinto, D. Varshney, L. Lawrence, M.B. Lowrie, and S. Hughes et al. GAA repeat expansion mutation mouse models of Friedreich ataxia exhibit oxidative stress leading to progressive neuronal and cardiac pathology Genomics 88 2006 580 590
93. C.J. Miranda, M.M. Santos, K. Ohshima, J. Smith, L. Li, and M. Bunting et al. Frataxin knockin mouse FEBS Lett 512 2002 291 297
94. M.A. Pook, S. Al-Mahdawi, C.J. Carroll, M. Cossee, H. Puccio, and L. Lawrence et al. Rescue of the Friedreich's ataxia knockout mouse by human YAC transgenesis Neurogenetics 3 2001 185 193
95. T.A. Rouault Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease Dis Models Mech 5 2012 155 164
96. M.L. Huang, E.M. Becker, M. Whitnall, Y. Suryo Rahmanto, P. Ponka, and D.R. Richardson Elucidation of the mechanism of mitochondrial iron loading in Friedreich's ataxia by analysis of a mouse mutant PNAS 106 2009 16381 16386
97. G.R. Wagner, P.M. Pride, C.M. Babbey, and R.M. Payne Friedreich's ataxia reveals a mechanism for coordinate regulation of oxidative metabolism via feedback inhibition of the SIRT3 deacetylase Hum Mol Genet 21 2012 2688 2697
98. D. Simon, H. Seznec, A. Gansmuller, N. Carelle, P. Weber, and D. Metzger et al. Friedreich ataxia mouse models with progressive cerebellar and sensory ataxia reveal autophagic neurodegeneration in dorsal root ganglia J Neurosci 24 2004 1987 1995
99. M. Ristow, H. Mulder, D. Pomplun, T.J. Schulz, K. Muller-Schmehl, and A. Krause et al. Frataxin deficiency in pancreatic islets causes diabetes due to loss of {beta} cell mass J Clin Invest 112 2003 527 534
100. S. Al-Mahdawi, R.M. Pinto, P. Ruddle, C. Carroll, Z. Webster, and M. Pook GAA repeat instability in Friedreich ataxia YAC transgenic mice Genomics 84 2004 301 310
101. B. Sturm, U. Bistrich, M. Schranzhofer, J.P. Sarsero, U. Rauen, and B. Scheiber-Mojdehkar et al. Friedreich's ataxia, no changes in mitochondrial labile iron in human lymphoblasts and fibroblasts: a decrease in antioxidative capacity? J Biol Chem 280 2005 6701 6708
102. M.L. Jauslin, T. Wirth, T. Meier, and F. Schoumacher A cellular model for Friedreich ataxia reveals small-molecule glutathione peroxidase mimetics as novel treatment strategy Hum Mol Genet 11 2002 3055 3063
103. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676
104. A. Eigentler, S. Boesch, R. Schneider, G. Dechant, and R. Nat Induced pluripotent stem cells from Friedreich ataxia patients fail to upregulate frataxin during in vitro differentiation to peripheral sensory neurons Stem cells Devt 22 24 2013 3271 3282
105. A. Hick, M. Wattenhofer-Donze, S. Chintawar, P. Tropel, J.P. Simard, and N. Vaucamps et al. Neurons and cardiomyocytes derived from induced pluripotent stem cells as a model for mitochondrial defects in Friedreich's ataxia Dis Model Mech 6 2013 608 621
106. S. Ku, E. Soragni, E. Campau, E.A. Thomas, G. Altun, and L.C. Laurent et al. Friedreich's ataxia induced pluripotent stem cells model intergenerational GAATTC triplet repeat instability Cell Stem Cell 7 2010 631 637
107. J. Liu, P.J. Verma, M.V. Evans-Galea, M.B. Delatycki, A. Michalska, and J. Leung et al. Generation of induced pluripotent stem cell lines from Friedreich ataxia patients Stem Cell Rev 7 2011 703 713
108. R.A. Vaubel, and G. Isaya Iron-sulfur cluster synthesis, iron homeostasis and oxidative stress in Friedreich ataxia Mol Cell Neurosci 55 2013 50 61
109. N. Boddaert, K.H. Le Quan Sang, and A. Rotig Selective iron chelation in Friedreich ataxia: biologic and clinical implications Blood 110 2007 401 408
110. O. Kakhlon, H. Manning, W. Breuer, N. Melamed-Book, C. Lu, and G. Cortopassi et al. Cell functions impaired by frataxin deficiency are restored by drug-mediated iron relocation Blood 112 2008 5219 5227
111. M. Pandolfo, and L. Hausmann Deferiprone for the treatment of Friedreich's ataxia J Neurochem 126 Suppl. 1 2013 142 146
112. D.R. Richardson Friedreich's ataxia: iron chelators that target the mitochondrion as a therapeutic strategy? Expert Opin Investig Drugs 12 2003 235 245
113. D.R. Richardson, C. Mouralian, P. Ponka, and E. Becker Development of potential iron chelators for the treatment of Friedreich's ataxia: ligands that mobilize mitochondrial iron Biochim Biophys Acta 1536 2001 133 140
114. D. Velasco-Sanchez, A. Aracil, R. Montero, A. Mas, L. Jimenez, and M. O'Callaghan et al. Combined therapy with idebenone and deferiprone in patients with Friedreich's ataxia Cerebellum 10 2011 1 8
115. K. Li, E.K. Besse, D. Ha, G. Kovtunovych, and T.A. Rouault Iron-dependent regulation of frataxin expression: implications for treatment of Friedreich ataxia Hum Mol Genet 17 2008 2265 2273
116. Y.S. Sohn, W. Breuer, A. Munnich, and Z.I. Cabantchik Redistribution of accumulated cell iron: a modality of chelation with therapeutic implications Blood 111 2008 1690 1699
117. J.M. Cooper, and A.H. Schapira Friedreich's ataxia: disease mechanisms, antioxidant and coenzyme Q10 therapy Biofactors 18 2003 163 171
118. J.M. Cooper, and A.H. Schapira Friedreich's ataxia: coenzyme Q10 and vitamin E therapy Mitochondrion 7 2007 S127 S135
119. M.H. Parkinson, J.B. Schulz, and P. Giunti Co-enzyme Q10 and idebenone use in Friedreich's ataxia J Neurochem 126 Suppl. 1 2013 125 141
120. P. Rustin, A. Rotig, A. Munnich, and D. Sidi Heart hypertrophy and function are improved by idebenone in Friedreich's ataxia Free Radic Res 36 2002 467 469
121. H. Seznec, R.B. Wilson, and H. Puccio 2003 International Friedreich's Ataxia Research Conference, 14-16 February 2003, Bethesda, MD, USA Neuromuscul Disord 14 2004 70 82
122. J.C. Gillis, P. Benefield, and D. McTavish Idebenone. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic use in age-related cognitive disorders Drugs Aging 5 1994 133 152
123. H. Seznec, D. Simon, L. Monassier, P. Criqui-Filipe, A. Gansmuller, and P. Rustin et al. 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 2004 1017 1024
124. P. Rustin, J.C. von Kleist-Retzow, K. Chantrel-Groussard, D. Sidi, A. Munnich, and A. Rotig Effect of idebenone on cardiomyopathy in Friedreich's ataxia: a preliminary study Lancet 354 1999 477 479
125. S.J. Lagedrost, M.S. Sutton, M.S. Cohen, G.M. Satou, B.D. Kaufman, and S.L. Perlman et al. Idebenone in Friedreich ataxia cardiomyopathy-results from a 6-month phase III study (IONIA) Am Heart J 161 2011 639 645
126. D.R. Lynch, S.L. Perlman, and T. Meier A phase 3, double-blind, placebo-controlled trial of idebenone in friedreich ataxia Arch Neurol 67 2010 941 947
127. P.M. Vyas, W.J. Tomamichel, Pride, C.M. Babbey, Q. Wang, and J. Mercier et al. A TAT-frataxin fusion protein increases lifespan and cardiac function in a conditional Friedreich's ataxia mouse model Hum Mol Genet 21 2012 1230 1247
128. B. Langley, J.M. Gensert, M.F. Beal, and R.R. Ratan Remodeling chromatin and stress resistance in the central nervous system: histone deacetylase inhibitors as novel and broadly effective neuroprotective agents Curr Drug Targets CNS Neurol Disord 4 2005 41 50
129. D. Herman, K. Jenssen, R. Burnett, E. Soragni, S.L. Perlman, and J.M. Gottesfeld Histone deacetylase inhibitors reverse gene silencing in Friedreich's ataxia Nat Chem Biol 2 2006 551 558
130. M. Rai, E. Soragni, C.J. Chou, G. Barnes, S. Jones, and J.R. Rusche et al. 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 2010 e8825
131. M. Rai, E. Soragni, K. Jenssen, R. Burnett, D. Herman, and G. Coppola et al. HDAC inhibitors correct frataxin deficiency in a Friedreich ataxia mouse model PLoS ONE 3 2008 e1958
132. C. Sandi, R.M. Pinto, S. Al-Mahdawi, V. Ezzatizadeh, G. Barnes, and S. Jones et al. Prolonged treatment with pimelic o-aminobenzamide HDAC inhibitors ameliorates the disease phenotype of a Friedreich ataxia mouse model Neurobiol Disease 42 2011 496 505
133. B. Sturm, D. Stupphann, C. Kaun, S. Boesch, M. Schranzhofer, and J. Wojta et al. Recombinant human erythropoietin: effects on frataxin expression in vitro Eur J Clin Invest 35 2005 711 717