Friedreich ataxia - Update on pathogenesis and possible therapies

Neurogenetics

Volumn 5, Issue 1, 2004, Pages 1-8

  Voncken, Max ^a,b   Ioannou, Panos ^b,c   Delatycki, Martin B ^b,c  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b ROYAL CHILDREN'S HOSPITAL   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Friedreich ataxia; Pathogenesis; Therapeutic strategies

Indexed keywords

2 PYRIDYLCARBOXALDEHYDE ISONICOTINOYL HYDRAZONE; ALPHA TOCOPHEROL; ANTIOXIDANT; DEFERIPRONE; DEFEROXAMINE; EBSELEN; FRATAXIN; GLUTATHIONE PEROXIDASE; IDEBENONE; IRON CHELATING AGENT; MITOQUINONE; UBIQUINONE; UNCLASSIFIED DRUG;

ADOPTIVE IMMUNOTHERAPY; ANTIOXIDANT ACTIVITY; CLINICAL GENETICS; CLINICAL TRIAL; DRUG BINDING; DRUG EFFECT; FRIEDREICH ATAXIA; GENE THERAPY; HUMAN; MOLECULAR BIOLOGY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIDE EFFECT; TREATMENT PLANNING;

ANIMALS; ANTIOXIDANTS; FRIEDREICH ATAXIA; HUMANS; IRON CHELATING AGENTS;

ANIMALIA;

EID: 1542350111     PISSN: 13646745     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10048-003-0170-z     Document Type: Review

References (99)

1. Cossee M, Schmitt M, Campuzano V, Reutenauer L, Moutou C, Mandel J-L, Koenig M (1997) Evolution of the Friedreich's ataxia trinucleotide repeat expansion: founder effect and premutation. Proc Natl Acad Sci U S A 94:7452-7457
2. Harding AE (1981) 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 104:589-620
3. Durr A, Cossee M, Agid Y, Campuzano V, Mignard C, Penet C, Mandel JL, Brice A, Koenig M (1996) Clinical and genetic abnormalities in patients with Friedreich's ataxia. N Engl J Med 335:1169-75
4. Delatycki M, Paris D, Gardner R, Nicholson G, Nassif N, Storey E, MacMillan J, Collins V, Williamson R, Forrest S (1999) A clinical and genetic study of Friedreich ataxia in an Australian population. Am J Med Genet 87:168-174
5. De Michele G, Perrone F, Filla A, Mirante E, Giordano M, De Placido S, Campanella G (1996) Age of onset, sex, and cardiomyopathy as predictors of disability and survival in Friedreich's disease: a retrospective study on 119 patients. Neurology 47:1260-1264
6. Hughes JT, Brownell B, Hewer RL (1968) The peripheral sensory pathway in Friedreich's ataxia. An examination by light and electron microscopy of the posterior nerve roots, posterior root ganglia, and peripheral sensory nerves in cases of Friedreich's ataxia. Brain 91:803-818
7. Lamarche JB, Lemieux B, Lieu HB (1984) The neuropathology of "typical" Friedreich's ataxia in Quebec. Can J Neurol Sci 11:592-600
8. Lamarche JB, Cote M, Lemieux B (1980) The cardiomyopathy of Friedreich's ataxia morphological observations in 3 cases. Can J Neurol Sci 7:389-396
9. Campuzano V, Montermini L, Lutz Y, Cova L, Hindelang C, Jiralerspong S, Trottier Y, Kish S, Faucheux B, Trouillas P, Authier F, Durr A, Mandel J-L, Vescovi A, Pandolfo M, Koenig M (1997) Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum Mol Genet 6:1771-1780
10. Wilson R, Roof D (1997) Respiratory deficiency due to loss of mitochondrial DNA in yeast lacking the frataxin homologue. Nat Genet 16:352-357
11. Campuzano V, Montermini L, Molto MD, Pianese L, Cossee M, Cavalcanti F, Monros E, Rodius F, Duclos F, Monticelli A, Zara F, Cañizares J, Koutnikova H, Bidichandani S, Gellere C, Brice A, Trouillas P, Michele GD, Filla A, Frutos RD, Palau F, Patel P, Donato SD, Mandel J-L, Cocozza S, Koenig M, Pandolfo M (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271:1423-1427
12. Pook MA, Al-Mahdawi SA, Thomas NH, Appleton R, Norman A, Mountford R, Chamberlain S (2000) Identification of three novel frameshift mutations in patients with Friedreich's ataxia. J Med Genet 37:E38
13. Montermini L, Andermann E, Labuda M, Richter A, Pandolfo M, Cavalcanti F, Pianese L, lodice L, Farina G, Montticelli A, Turano M, Filla A, Michele GD, Cocozza S (1997) The Friedreich ataxia GAA triplet repeat: premutation and normal alleles. Hum Mol Genet 6:1261-1266
14. Montermini L, Richter A, Morgan K, Justice CM, Julien D, Castellotti B, Mercier J, Poirier J, Capozzoli F, Bouchard JP, Lemieux B, Mathieu J, Vanasse M, Seni MH, Graham G, Andermann F, Andermann E, Melancon SB, Keats BJ, Di Donato S, Pandolfo M (1997) Phenotypic variability in Friedreich ataxia: role of the associated GAA triplet repeat expansion. Ann Neurol 41:675-682
15. 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 273:14588-14595
16. Grabczyk E, Kumari D, Usdin K (2001) Fragile X syndrome and Friedreich's ataxia: two different paradigms for repeat induced transcript insufficiency. Brain Res Bull 56:367-373
17. Bidichandani SI, Ashizawa T, Patel PI (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
18. GrabczykE, Usdin K (2000) The GAA*TTC triplet repeat expanded in Friedreich's ataxia impedes transcription elongation by T7 RNA polymerase in a length and supercoil dependent manner. Nucleic Acids Res 28:2815-2822
19. Babcock M, Silva D, Oaks R, Davis-Kaplan S, Jiralerspong S, Montermini L, Pandolfo M, Kaplan J (1997) Regulation of mitochondrial iron accumulation by Yfh 1p, a putative homolog of frataxin. Science 276:1709-1712
20. Cossee M, Puccio H, Gansmuller A, Koutnikova H, Dierich A, LeMeur M, Fischbeck K, Dolle P, Koenig M (2000) Inactivation of the Friedreich ataxia mouse gene leads to early embryonic lethality without iron accumulation. Hum Mol Genet 9:1219-1226
21. Puccio H, Simon D, Cossee M, Criqui-Filipe P, Tiziano F, Melki J, Hindelang C, Matyas R, Rustin P, 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
22. Foury F, Cazzalini O (1997) Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Lett 411:373-377
23. Koutnikova H, Campuzano V, Foury F, Dolle P, Cazzalini O, Koenig M (1997) Studies of human, mouse and yeast homologues indicate a mitochondrial function for frataxin. Nat Genet 16:345-351
24. Radisky DC, Babcock MC, Kaplan J (1999) The yeast frataxin homologue mediates mitochondrial iron efflux. Evidence for a mitochondrial iron cycle. J Biol Chem 274:4497-4499
25. Gakh O, Adamec J, Gacy AM, Twesten RD, Owen WG, Isaya G (2002) Physical evidence that yeast frataxin is an iron storage protein. Biochemistry 41:6798-6804
26. Park S, Gakh O, O'Neill HA, Mangravita A, Nichol H, Ferreira GC, Isaya G (2003) Yeast frataxin sequentially chaperones and stores iron by coupling protein assembly with iron oxidation. J Biol Chem 278:31340-1351
27. Park S, Gakh O, Mooney SM, Isaya G (2002) The ferroxidase activity of yeast frataxin. J Biol Chem 277:38589-38595
28. Beinert H, Holm RH, Munck E (1997) Iron-sulfur clusters: nature's modular, multipurpose structures. Science 277:653-659
29. Foury F (1999) Low iron concentration and aconitase deficiency in a yeast frataxin homologue deficient strain. FEBS Lett 456:281-284
30. Muhlenhoff U, Richhardt N, Ristow M, Kispal G, Lill R (2002) The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum Mol Genet 11:2025-2036
31. Lill R, Kispal G (2000) Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem Sci 25:352-356
32. Muhlenhoff U, Lill R (2000) Biogenesis of iron-sulfur proteins in eukaryotes: a novel task of mitochondria that is inherited from bacteria. Biochim Biophys Acta 15:2-3
33. Duby G, Foury F, Ramazzotti A, Herrmann J, Lutz T (2002) A non-essential function for yeast frataxin in iron-sulfur cluster assembly. Hum Mol Genet 11:2635-2643
34. Miranda CJ, Santos MM, Ohshima K, Smith J, Li L, Bunting M, Cossee M, Koenig M, Sequeiros J, Kaplan J, Pandolfo M (2002) Frataxin knockin mouse. FEBS Lett 512:291-297
35. Pandolfo M (1999) Molecular pathogenesis of Friedreich ataxia. Arch Neurol 56:1201-1208
36. Cavadini P, Gellera C, Patel PI, Isaya G (2000) Human frataxin maintains mitochondrial iron homeostasis in Saccharomyces cerevisiae. Hum Mol Genet 9:2523-2530
37. Pook MA, Al-Mahdawi S, Carroll CJ, Cossee M, Puccio H, Lawrence L, Clark P, Lowrie MB, Bradley JL, Cooper JM, Koenig M, Chamberlain S (2001) Rescue of the Friedreich's ataxia knockout mouse by human YAC transgenesis. Neurogenetics 3:185-193
38. Delatycki MB, Camakaris J, Brooks H, Evans-Whipp T, Thorburn DR, Williamson R, Forrest SM (1999) Direct evidence that mitochondrial iron accumulation occurs in Friedreich ataxia. Ann Neurol 45:673-675
39. Sanchez-Casis G, Cote M, Barbeau A (1977) Pathology of the heart in Friedreich's ataxia: review of the literature and report of one case. Can J Neurol Sci 3:349-354
40. Waldvogel D, Gelderen P van, Hallett M (1999) Increased iron in the dentate nucleus of patients with Friedrich's ataxia. Ann Neurol 46:123-125
41. Rotig A, Lonlay P de, Chretien D, Foury F, Koenig M, Sidi D, Munnich A, Rustin P (1997) Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat Genet 17:215-217
42. Tan G, Napoli E, Taroni F, Cortopassi G (2003) Decreased expression of genes involved in sulfur amino acid metabolism in frataxin-deficient cells. Hum Mol Genet 12:1699-1711
43. Jiralerspong S, Ge B, Hudson TJ, Pandolfo M (2001) Manganese superoxide dismutase induction by iron is impaired in Friedreich ataxia cells. FEBS Lett 509:101-105
44. Chantrel-Groussard K, Geromel V, Puccio H, Koenig M, Munnich A, Rotig A, Rustin P (2001) Disabled early recruitment of antioxidant defenses in Friedreich's ataxia. Hum Mol Genet 10:2061-2067
45. Tozzi G, Nuccetelli M, Lo Bello M, Bernardini S, Bellincampi L, Ballerini S, Gaeta LM, Casali C, Pastore A, Federici G, Bertini E, Piemonte F (2002) Antioxidant enzymes in blood of patients with Friedreich's ataxia. Arch Dis Child 86:376-379
46. Pastore A, Tozzi G, Gaeta LM, Bertini E, Serafini V, Di Cesare S, Bonetto V, Casoni F, Carrozzo R, Federici G, Piemonte F (2003) Actin glutathionylation increases in fibroblasts of patients with Friedreich's ataxia: a potential role in the pathogenesis of the disease. J Biol Chem 274:26683-26690
47. Lenaz G, Bovina C, D'Aurelio M, Fato R, Formiggini G, Genova ML, Giuliano G, Pich MM, Paolucci U, Castelli GP, Ventura B (2002) Role of mitochondria in oxidative stress and aging. Ann N Y Acad Sci 959:199-213
48. Hamai D, Bondy SC, Becaria A, Campbell A (2001) The chemistry of transition metals in relation to their potential role in neurodegenerative processes. Curr Top Med Chem 1:541-51
49. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97-112
50. Moosmann B, Behl C (2002) Antioxidants as treatment for neurodegenerative disorders. Expert Opin Investig Drugs 11:1407-1435
51. Suno M, Nagaoka A (1984) Inhibition of lipid peroxidation by a novel compound (CV-2619) in brain mitochondria and mode of action of the inhibition. Biochem Biophys Res Commun 125:1046-1052
52. Nagaoka A, Suno M, Shibota M, Kakihana M (1984) Effects of idebenone (CV-2619) on neurological deficits, local cerebral blood flow, and energy metabolism in rats with experimental cerebral ischemia. Nippon Yakurigaku Zasshi 84:303-309
53. Yamazaki N, Take Y, Nagaoka A, Nagawa Y (1984) Beneficial effect of idebenone (CV-2619) on cerebral ischemia-induced amnesia in rats. Jpn J Pharmacol 36:349-356
54. Suno M, Nagaoka A (1988) Effect of idebenone and various nootropic drugs on lipid peroxidation in rat brain homogenate in the presence of succinate. Nippon Yakurigaku Zasshi 91:295-299
55. Suno M, Nagaoka A (1989) Inhibition of lipid peroxidation by idebenone in brain mitochondria in the presence of succinate. Arch Geront Geriatr 8:291-297
56. Koyama T, Zhu MY, Kinjo M, Araiso T (1991) Protective effects of idebenone against alterations in dynamic microstructure induced by lipid peroxidation in rat cardiac mitochondria. Jpn Heart J 32:91-100
57. Sugiyama Y, Fujita T (1985) Stimulation of the respiratory and phosphorylating activities in rat brain mitochondria by idebenone (CV-2619), a new agent improving cerebral metabolism. FEBS Lett 184:48-51
58. Shimamoto N, Tanabe M, Imamoto T, Hirata M (1982) Effects of 2,3-dimethoxy-5-methyl-6-(10′-hydroxydecyl)-1,4-benzoquinone (CV-2619) on myocardial energy metabolism in the hypertrophied heart of spontaneously hypertensive rats. Nippon Yakurigaku Zasshi 80:299-306
59. Rustin P, Kleist-Retzow J-C, Chantrel-Groussard K, Sidi D, Munnich A, Rotig A (1999) Effect of idebenone on cardiomyopathy in Friedreich's ataxia, Lancet 354:477-479
60. Hausse AO, Aggoun Y, Bonnet D, Sidi D, Munnich A, Rotig A, Rustin P (2002) Idebenone and reduced cardiac hypertrophy in Friedreich's ataxia. Heart 87:346-349
61. Rustin P, Rotig A, Munnich A, Sidi D (2002) Heart hypertrophy and function are improved by idebenone in Friedreich's ataxia. Free Radic Res 36:467-469
62. Schols L, Vorgerd M, Schillings M, Skipka G, Zange J (2001) Idebenone in patients with Friedreich ataxia. Neurosci Lett 306:169-172
63. Mariotti C, Solari A, Torta D, Marano L, Fiorentini C, Di Donato S (2003) Idebenone treatment in Friedreich patients: one-year-long randomized placebo-controlled trial. Neurology 60:1676-1679
64. Buyse G, Mertens L, Di Salvo G, Matthijs I, Weidemann F, Eyskens B, Goossens W, Goemans N, Sutherland GR, Van Hove JL (2003) Idebenone treatment in Friedreich's ataxia: neurological, cardiac, and biochemical monitoring. Neurology 60:1679-1681
65. Filla A, Moss AJ (2003) Idebenone for treatment of Friedreich's ataxia? Neurology 60:1569-1570
66. Schulz JB, Dehmer T, Schols L, Mende H, Hardt C, Vorgerd M, Burk K, Matson W, Dichgans J, Beal MF, Bogdanov MB (2000) Oxidative stress in patients with Friedreich ataxia. Neurology 55:1719-1721
67. Lodi R, Hart PE, Rajagopalan B, Taylor DJ, Crilley JG, Bradley JL, Blamire AM, Manners D, Styles P, Schapira AH, Cooper JM (2001) Antioxidant treatment improves in vivo cardiac and skeletal muscle bioenergetics in patients with Friedreich's ataxia. Ann Neurol. 49:590-596
68. Kelso GF, Porteous CM, Coulter CV, Hughes G, Porteous WK, Ledgerwood EC, Smith RA, Murphy MP (2001) Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties. J Biol Chem 276:4588-4596
69. Chen LB (1988) Mitochondrial membrane potential in living cells. Annu Rev Cell Biol 4:155-181
70. Murphy MP (1997) Selective targeting of bioactive compounds to mitochondria. Trends Biotechnol 15:326-330
71. Murphy MP, Smith RA (2000) Drug delivery to mitochondria: the key to mitochondrial medicine. Adv Drug Deliv Rev 41:235-250
72. Ingold KU, Bowry VW, Stocker R, Walling C (1993) Autoxidation of lipids and antioxidation by alpha-tocopherol and ubiquinol in homogeneous solution and in aqueous dispersions of lipids: unrecognized consequences of lipid particle size as exemplified by oxidation of human low density lipoprotein. Proc Natl Acad Sci U S A 90:45-49
73. Kagan VE, Serbinova EA, Stoyanovsky DA, Khwaja S, Packer L (1994) Assay of ubiquinones and ubiquinols as antioxidants. Methods Enzymol 234:343-354
74. Maguire JJ, Wilson DS, Packer L (1989) Mitochondrial electron transport-linked tocopheroxyl radical reduction. J Biol Chem 264:21462-21465
75. Jauslin ML, Meier T, Smith RA, Murphy MP (2003) Mitochondria-targeted antioxidants protect Friedreich ataxia fibroblasts from endogenous oxidative stress more effectively than untargeted antioxidants. FASEB J (in press)
76. Smith JC, Kushner JP, Bromberg M, Hammond E, Barry WH, Pandolfo M, Kaplan J (1999) Proceedings of the Friedreich's Research Conference. National Institutes of Health, Bethesda, Md., USA
77. Ponka P, Borova J, Neuwirt J, Fuchs O (1979) Mobilization of iron from reticulocytes. Identification of pyridoxal isonicotinoyl hydrazone as a new iron chelating agent. FEBS Lett 97:317-321
78. Ponka P, Grady RW, Wilczynska A, Schulman HM (1984) The effect of various chelating agents on the mobilization of iron from reticulocytes in the presence and absence of pyridoxal isonicotinoyl hydrazone. Biochim Biophys Acta 802:477-489
79. Liu ZD, Hider RC (2002) Design of clinically useful iron(III)-selective chelators. Med Res Rev 22:26-64
80. Sephton-Smith R (1962) Iron excretion in thalassaemia major after administration of chelating agents. BMJ 2:1577
81. Bannerman R, Callender S, Williams D (1962) Effect of desferrioxamine and DTPA in iron overload. BMJ 2:1573
82. Sephton-Smith R (1964) Chelating agents in the diagnosis and treatment of iron overload in thalassemia. Ann NY Acad Sci 119:776
83. Olivieri NF, Brittenham GM, McLaren CE, Templeton DM, Cameron RG, McClelland RA, Burt AD, Fleming KA (1998) Long-term safety and effectiveness of iron-chelation therapy with deferiprone for thalassemia major. N Engl J Med 339:417-423
84. Stella M, Pinzello G, Maggio A (1998) Iron chelation with oral deferiprone in patients with thalassemia. N Engl J Med 339:1713-1714
85. Wanless IR, Sweeney G, Dhillon AP, Guido M, Piga A, Galanello R, Gamberini MR, Schwartz E, Cohen AR (2002) Lack of progressive hepatic fibrosis during long-term therapy with deferiprone in subjects with transfusion-dependent beta-thalassemia. Blood 100:1566-1569
86. Berdoukas V, Bohane T, Eagle C, Lindeman R, DeSilva K, Tobias V, Painter D, Fraser I (2000) The Sydney Children's Hospital experience with the oral iron chelator deferiprone (LI). Transfus Sci 23:239-240
87. Tondury P, Zimmermann A, Nielsen P, Hirt A (1998) Liver iron and fibrosis during long-term treatment with deferiprone in Swiss thalassaemic patients. Br J Haematol 101:413-415
88. Anderson LJ, Wonke B, Prescott E, Holden S, Walker JM, Pennell DJ (2002) Comparison of effects of oral deferiprone and subcutaneous desferrioxamine on myocardial iron concentrations and ventricular function in beta-thalassaemia. Lancet 360:516-520
89. Stobie S, Tyberg J, Matsui D, Fernandes D, Klein J, Olivieri N, Bentur Y, Koren G (1993) Comparison of the pharmacokinetics of 1,2-dimethyl-3-hydroxypyrid-4-one (L1) in healthy volunteers, with and without co-administration of ferrous sulfate, to thalassemia patients. Int J Clin Pharmacol Ther Tox 31:602-605
90. Liu ZD, Kayyali R, Hider RC, Porter JB, Theobald AE (2002) Design, synthesis, and evaluation of novel 2-substituted 3-hydroxypyridin-4-ones: structure-activity investigation of metalloenzyme inhibition by iron chelators. J Med Chem 45:631-639
91. Richardson DR, Mouralian C, Ponka P, Becker E (2001) Development of potential iron chelators for the treatment of Friedreich's ataxia: ligands that mobilize mitochondrial iron. Biochim Biophys Acta 1536:133-140
92. Jauslin ML, Wirth T, Meier T, 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
93. Karthikeyan G, Lewis LK, Resnick MA (2002) The mitochondrial protein frataxin prevents nuclear damage. Hum Mol Genet 11:1351-1362
94. Shoichet SA, Baumer AT, Stamenkovic D, Sauer H, Pfeiffer AF, Kahn CR, Muller-Wieland D, Richter C, Ristow M (2002) Frataxin promotes antioxidant defense in a thiol-dependent manner resulting in diminished malignant transformation in vitro. Hum Mol Genet 11:815-821
95. Sarsero JP, Li L, Wardan H, Sitte K, Williamson R, Ioannou PA (2003) Upregulation of expression from the FRDA genomic locus for the therapy of Friedreich ataxia. J Gene Med 5:72-81
96. Ghazizadeh M (2003) Cisplatin may induce frataxin expression. J Nippon Med Sch 70:367-371
97. Turano M, Tammaro A, De Biase I, Lo Casale MS, Ruggiero G, Monticelli A, Cocozza S, Pianese L (2003) 3-Nitropropionic acid increases frataxin expression in human lymphoblasts and in transgenic rat PC12 cells. Neurosci Lett 350:184-186
98. Grabczyk E, Usdin K (2000) Alleviating transcript insufficiency caused by Friedreich's ataxia triplet repeats. Nucleic Acids Res 28:4930-4937
99. Johnson P, Walker R, Jones S, Stephens K, Meurer J, Zajchowski D, Luke M, Eeckman F, Tan Y, Wong L, Parry G, Morgan TJ, McCarrick M, Monforte J (2002) Multiplex gene expression analysis for high-throughput drug discovery: screening and analysis of compounds affecting genes overexpressed in cancer cells. Mol Cancer Ther 1:1293-1304