Cardiomyopathy of Friedreich's ataxia: Use of mouse models to understand human disease and guide therapeutic development

Pediatric Cardiology

Volumn 32, Issue 3, 2011, Pages 366-378

  Payne, R Mark ^a   Pride, P Melanie ^a   Babbey, Clifford M ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiomyopathy; Friedreich's ataxia; Mitochondria; Therapy

Indexed keywords

CARDIAC IMAGING; CARDIOMYOPATHY; CAUSE OF DEATH; CONFERENCE PAPER; DISEASE MODEL; ECHOCARDIOGRAPHY; FRIEDREICH ATAXIA; GENETIC ANALYSIS; HUMAN; MORBIDITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PROGNOSIS;

ANIMALS; CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; FRIEDREICH ATAXIA; HUMANS; IRON-BINDING PROTEINS; MICE;

EID: 79953753153     PISSN: 01720643     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00246-011-9943-6     Document Type: Conference Paper

References (93)

1. Alboliras ET, Shub C, Gomez MR, Edwards WD, Hagler DJ, Reeder GS, Seward JB, Tajik AJ (1986) Spectrum of cardiac involvement in Friedreich's ataxia: clinical, electrocardiographic, and echocardiographic observations. Am J Cardiol 58:518-524 (Pubitemid 16052684)
2. Al-Mahdawi S, Pinto RM, Ismail O, Varshney D, Lymperi S, Sandi C, Trabzuni D, 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 (Pubitemid 351292262)
3. Begley DJ (1996) The blood-brain barrier: principles for targeting peptides and drugs to the central nervous system. J Pharm Pharmacol 48:136-146
4. Boddaert N, Le Quan Sang KH, Rotig A, Leroy-Willig A, Gallet S, Brunelle F, Sidi D, Thalabard JC, Munnich A, Cabantchik ZI (2007) Selective iron chelation in Friedreich ataxia: biologic and clinical implications. Blood 110:401-408 (Pubitemid 47026862)
5. Brautigam CA, Chuang JL, Tomchick DR, Machius M, Chuang DT (2005) Crystal structure of human dihydrolipoamide dehydrogenase: NAD+/NADH binding and the structural basis of disease-causing mutations. J Mol Biol 350:543-552 (Pubitemid 40828913)
6. Bunse M, Bit-Avragim N, Riefflin A, Perrot A, Schmidt O, Kreuz FR, Dietz R, Jung WI, Osterziel KJ (2003) Cardiac energetics correlates to myocardial hypertrophy in Friedreich's ataxia. Ann Neurol 53:121-123 (Pubitemid 36083837)
7. Cao G, Pei W, Ge H, Liang Q, Luo Y, Sharp FR, Lu A, Ran R, Graham SH, Chen J (2002) In vivo delivery of a bcl-xl fusion protein containing the TAT protein transduction domain protects against ischemic brain injury and neuronal apoptosis. J Neurosci 22:5423-5431
8. Casazza F, Morpurgo M (1996) The varying evolution of Friedreich's ataxia cardiomyopathy. Am J Cardiol 77:895-898 (Pubitemid 26143509)
9. Cavadini P, Adamec J, Taroni F, Gakh O, Isaya G (2000) Twostep processing of human frataxin by mitochondrial processing peptidase: precursor and intermediate forms are cleaved at different rates. J Biol Chem 275:41469-41475 (Pubitemid 32054983)
10. Chakrapani A, Vellodi A, Robinson P, Jones S, Wraith JE (2010) Treatment of infantile Pompe disease with alglucosidase alpha: the UK experience. J Inherit Metab Dis 33:747-750
11. Child JS, Perloff JK, Bach PM, Wolfe AD, Perlman S, Kark RA (1986) Cardiac involvement in Friedreich's ataxia: a clinical study of 75 patients. J Am Coll Cardiol 7:1370-1378 (Pubitemid 16100362)
12. Condo I, Ventura N, Malisan F, Rufini A, Tomassini B, Testi R (2007) In vivo maturation of human frataxin. Hum Mol Genet 16:1534-1540
13. 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 (Pubitemid 30248608)
14. De Biase I, Rasmussen A, Endres D, Al-Mahdawi S, Monticelli A, Cocozza S, Pook M, Bidichandani SI (2007) Progressive GAA expansions in dorsal root ganglia of Friedreich's ataxia patients. Ann Neurol 61:55-60 (Pubitemid 46214244)
15. Del Gaizo Moore V, Payne RM (2004) Transactivator of transcription fusion protein transduction causes membrane inversion. J Biol Chem 279:32541-32544
16. Del Gaizo V, Payne RM (2003) A novel TAT-mitochondrial signal sequence fusion protein is processed, stays in mitochondria, and crosses the placenta. Mol Ther 7:720-730 (Pubitemid 36790248)
17. Del Gaizo-Moore V, MacKenzie JA, Payne RM (2003) Targeting proteins to mitochondria using TAT. Mol Genet Metab 80:170-180 (Pubitemid 37272243)
18. Drin G, Cottin S, Blanc E, Rees AR, Temsamani J (2003) Studies on the internalization mechanism of cationic cell-penetrating peptides. J Biol Chem 278:31192-31201 (Pubitemid 36994635)
19. Dutka DP, Donnelly JE, Palka P, Lange A, Nunez DJ, Nihoyannopoulos P (2000) Echocardiographic characterization of cardiomyopathy in Friedreich's ataxia with tissue Doppler echocardiographically derived myocardial velocity gradients. Circulation 102:1276-1282
20. Epplen C, Epplen JT, Frank G, Miterski B, Santos EJ, Schols L (1997) Differential stability of the (GAA)n tract in the Friedreich ataxia (STM7) gene. Hum Genet 99:834-836 (Pubitemid 27243768)
21. Filla A, De Michele G, Marconi R, Bucci L, Carillo C, Castellano AE, Iorio L, Kniahynicki C, Rossi F, Campanella G (1992) Prevalence of hereditary ataxias and spastic paraplegias in Molise, a region of Italy. J Neurol 239:351-353
22. Filla A, De Michele G, Cavalcanti F, Pianese L, Monticelli A, Campanella G, Cocozza S (1996) The relationship between trinucleotide (GAA) repeat length and clinical features in Friedreich ataxia. Am J Hum Genet 59:554-560 (Pubitemid 26269033)
23. Gacy AM, Goellner GM, Spiro C, Chen X, Gupta G, Bradbury EM, Dyer RB, Mikesell MJ, Yao JZ, Johnson AJ, Richter A, Melancon SB, McMurray CT (1998) GAA instability in Friedreich's ataxia shares a common DNA-directed and intraallelic mechanism with other trinucleotide diseases. Mol Cell 1:583-593 (Pubitemid 128374694)
24. Gaume B, Klaus C, Ungermann C, Guiard B, Neupert W, Brunner M (1998) Unfolding of preproteins upon import into mitochondria. EMBO J 17:6497-6507 (Pubitemid 28521785)
25. Gillingham MB, Scott B, Elliott D, Harding CO (2006) Metabolic control during exercise with and without medium-chain triglycerides (MCT) in children with long-chain 3-hydroxy acyl-CoA dehydrogenase (LCHAD) or trifunctional protein (TFP) deficiency. Mol Genet Metab 89:58-63 (Pubitemid 44205484)
26. Goker-Alpan O (2010) Optimal therapy in Gaucher disease. Ther Clin Risk Manag 6:315-323
27. Gustafsson AB, Sayen MR, Williams SD, Crow MT, Gottlieb RA (2002) TAT protein transduction into isolated perfused hearts: TAT-apoptosis repressor with caspase recruitment domain is cardioprotective. Circulation 106:735-739 (Pubitemid 34851935)
28. Gustafsson AB, Gottlieb RA, Granville DJ (2005) TAT-mediated protein transduction: delivering biologically active proteins to the heart. Methods Mol Med 112:81-90
29. Haas RH (2007) The evidence basis for coenzyme Q therapy in oxidative phosphorylation disease. Mitochondrion 7(Suppl): S136-S145
30. Hanley A, Corrigan R, Mohammad S, MacMahon B (2010) Friedreich's ataxia cardiomyopathy: case based discussion and management issues. Ir Med J 103:117-118
31. 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
32. Hart PE, Lodi R, Rajagopalan B, Bradley JL, Crilley JG, Turner C, Blamire AM, Manners D, Styles P, Schapira AH, Cooper JM (2005) Antioxidant treatment of patients with Friedreich ataxia: four-year follow-up. Arch Neurol 62:621-626 (Pubitemid 40489896)
33. Hawley RJ, Gottdiener JS (1986) Five-year follow-up of Friedreich's ataxia cardiomyopathy. Arch Intern Med 146:483-488 (Pubitemid 16067893)
34. Herman D, Jenssen K, Burnett R, Soragni E, Perlman SL, Gottesfeld JM (2006) Histone deacetylase inhibitors reverse gene silencing in Friedreich's ataxia. Nat Chem Biol 2:551-558 (Pubitemid 44413238)
35. Hewer R (1969) The heart in Friedreich's ataxia. Br Heart J 31:5-14
36. Huang ML, Becker EM, Whitnall M, Rahmanto YS, Ponka P, Richardson DR (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
37. Isaya G (2007) Ironing out a therapy for Friedreich ataxia. Blood 110:1-2
38. 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 17:1972-1974
39. Jensen KD, Nori A, Tijerina M, Kopeckova P, Kopecek J (2003) Cytoplasmic delivery and nuclear targeting of synthetic macromolecules. J Control Release 87:89-105 (Pubitemid 36258389)
40. Kearney M, Orrell RW, Fahey M, Pandolfo M (2009) Antioxidants and other pharmacological treatments for Friedreich ataxia. Cochrane Database Syst Rev: CD007791
41. Kipps A, Alexander M, Colan SD, Gauvreau K, Smoot L, Crawford L, Darras BT, Blume ED (2009) The longitudinal course of cardiomyopathy in Friedreich's ataxia during childhood. Pediatr Cardiol 30:306-310
42. Kosutic J, Zamurovic D (2005) High-dose beta-blocker hypertrophic cardiomyopathy therapy in a patient with Friedreich ataxia. Pediatr Cardiol 26:727-730 (Pubitemid 43015828)
43. Leonard H, Forsyth R (2001) Friedreich's ataxia presenting after cardiac transplantation. Arch Dis Child 84:167-168 (Pubitemid 32150337)
44. Levin VA (1980) Relationship of octanol/water partition coefficient and molecular weight to rat brain capillary permeability. J Med Chem 23:682-684
45. Li K, Besse EK, Ha D, Kovtunovych G, Rouault TA (2008) Iron-dependent regulation of frataxin expression: implications for treatment of Friedreich ataxia. Hum Mol Genet 17:2265-2273
46. Lim F, Palomo GM, Mauritz C, Gimenez-Cassina A, Illana B, Wandosell F, 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 (Pubitemid 46813609)
47. Lodi R, Cooper JM, Bradley JL, Manners D, Styles P, Taylor DJ, Schapira AH (1999) Deficit of in vivo mitochondrial ATP production in patients with Friedreich ataxia. Proc Natl Acad Sci USA 96:11492-11495 (Pubitemid 29487408)
48. Lodi R, Rajagopalan B, Blamire AM, Cooper JM, Davies CH, Bradley JL, Styles P, Schapira AH (2001) Cardiac energetics are abnormal in Friedreich ataxia patients in the absence of cardiac dysfunction and hypertrophy: an in vivo 31P magnetic resonance spectroscopy study. Cardiovasc Res 52:111-119 (Pubitemid 32835244)
49. Lynch DR, Perlman SL, Meier T (2010) A phase 3, double-blind, placebo-controlled trial of idebenone in Friedreich ataxia. Arch Neurol 67:941-947
50. Malo S, Latour Y, Cote M, Geoffroy G, Lemieux B, Barbeau A (1976) Electrocardiographic and vectocardiographic findings in Friedreich's ataxia: the Canadian journal of neurological sciences. J Can Sci Neurol 3:323-328 (Pubitemid 8067185)
51. Mariotti C, Solari A, Torta D, Marano L, Fiorentini C, Di DS (2003) Idebenone treatment in Friedreich patients: one-year-long randomized placebo-controlled trial. Neurology 60:1676-1679 (Pubitemid 36618100)
52. Michael S, Petrocine SV, Qian J, Lamarche JB, Knutson MD, Garrick MD, Koeppen AH (2006) Iron and iron-responsive proteins in the cardiomyopathy of Friedreich's ataxia. Cerebellum 5:257-267 (Pubitemid 44875782)
53. 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 (Pubitemid 34164497)
54. Mitchell DJ, Kim DT, Steinman L, Fathman CG, Rothbard JB (2000) Polyarginine enters cells more efficiently than other polycationic homopolymers. J Pept Res 56:318-325
55. 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 (Pubitemid 27212663)
56. Palagi B, Picozzi R, Casazza F, Possa M, Magri G, Zoccarato O, Graziano E, Ferrari F, Morpurgo M (1988) Biventricular function in Friedreich's ataxia: a radionuclide angiographic study. Br Heart J 59:692-695
57. Pandolfo M (2008) Friedreich ataxia. Arch Neurol 65:1296-1303
58. Patel PI, Isaya G (2001) Friedreich ataxia: from GAA tripletrepeat expansion to frataxin deficiency. Am J Hum Genet 69:15-24 (Pubitemid 32614014)
59. Pineda M, Arpa J, Montero R, Aracil A, Dominguez F, Galvan M, Mas A, Martorell L, Sierra C, Brandi N, Garcia-Arumi E, Rissech M, Velasco D, Costa JA, Artuch R (2008) Idebenone treatment in paediatric and adult patients with Friedreich ataxia: long-term follow-up. Eur J Paediatr Neurol 12:470-475
60. 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 (Pubitemid 33738404)
61. Puccio H, Koenig M (2000) Recent advances in the molecular pathogenesis of Friedreich ataxia. Hum Mol Genet 9:887-892 (Pubitemid 30216099)
62. 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 (Pubitemid 32157445)
63. Rai M, Soragni E, Jenssen K, Burnett R, Herman D, Coppola G, Geschwind DH, Gottesfeld JM, Pandolfo M (2008) HDAC inhibitors correct frataxin deficiency in a Friedreich ataxia mouse model. PLoS One 3:e1958
64. Rajagopalan B, Francis JM, Cooke F, Korlipara LV, Blamire AM, Schapira AH, Madan J, Neubauer S, Cooper JM (2010) Analysis of the factors influencing the cardiac phenotype in Friedreich's ataxia. Mov Disord 25:846-852
65. Raman SV, Phatak K, Hoyle JC, Pennell ML, McCarthy B, Tran T, Prior TW, Olesik JW, Lutton A, Rankin C, Kissel JT, Al-Dahhak R (2010) Impaired myocardial perfusion reserve and fibrosis in Friedreich ataxia: a mitochondrial cardiomyopathy with metabolic syndrome. Eur Heart J (in press)
66. Rapoport M, Lorberboum-Galski H (2009) TAT-based drug delivery system: new directions in protein delivery for new hopes? Expert Opin Drug Deliv 6:453-463
67. Rapoport M, Saada A, Elpeleg O, Lorberboum-Galski H (2008) TAT-mediated delivery of LAD restores pyruvate dehydrogenase complex activity in the mitochondria of patients with LAD deficiency. Mol Ther 16:691-697 (Pubitemid 351426170)
68. Rayapureddi JP, Tomamichel WJ, Walton ST, Payne RM (2010) TAT fusion protein transduction into isolated mitochondria is accelerated by sodium channel inhibitors. Biochemistry (in press)
69. Reddy PL, Grewal RP (2007) Friedreich's ataxia: a clinical and genetic analysis. Clin Neurol Neurosurg 109:200-202 (Pubitemid 46073400)
70. Richardson DR (2003) Friedreich's ataxia: iron chelators that target the mitochondrion as a therapeutic strategy? Expert Opin Investig Drugs 12:235-245
71. Richardson DR, Huang ML, Whitnall M, Becker EM, Ponka P, Rahmanto YS (2010) The ins and outs of mitochondrial ironloading: the metabolic defect in Friedreich's ataxia. J Mol Med 88:323-329
72. Romeo G, Menozzi P, Ferlini A, Fadda S, Di Donato S, Uziel G, Lucci B, Capodaglio L, Filla A, Campanella G (1983) Incidence of Friedreich ataxia in Italy estimated from consanguineous marriages. Am J Hum Genet 35:523-529 (Pubitemid 13095776)
73. Rotig A, de LP, 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
74. 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 (Pubitemid 35154096)
75. Ryser HJ, Drummond I, Shen WC (1982) The cellular uptake of horseradish peroxidase and its poly(lysine) conjugate by cultured fibroblasts is qualitatively similar despite a 900-fold difference in rate. J Cell Physiol 113:167-178 (Pubitemid 12035326)
76. Sakamoto N, Ohshima K, Montermini L, Pandolfo M, Wells RD (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
77. Schmucker S, Argentini M, Carelle-Calmels N, Martelli A, Puccio H (2008) The in vivo mitochondrial two-step maturation of human frataxin. Hum Mol Genet 17:3521-3531
78. Schols L, Amoiridis G, Przuntek H, Frank G, Epplen JT, Epplen C (1997) Friedreich's ataxia: revision of the phenotype according to molecular genetics. Brain 120:2131-2140 (Pubitemid 28014589)
79. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285:1569-1572
80. Sedlak TL, Chandavimol M, Straatman L (2004) Cardiac transplantation: a temporary solution for Friedreich's ataxia-induced dilated cardiomyopathy. J Heart Lung Transplant 23:1304-1306 (Pubitemid 39472911)
81. Segovia J, Alonso-Pulpon L, Burgos R, Silva L, Serrano S, Castedo E, Jimenez J, Fuentes R, Canas A, Ugarte J (2001) Heart transplantation in Friedreich's ataxia and other neuromuscular diseases. J Heart Lung Transplant 20:169
82. Shaddy RE, Boucek MM, Hsu DT, Boucek RJ, Canter CE, Mahony L, Ross RD, Pahl E, Blume ED, Dodd DA, Rosenthal DN, Burr J, LaSalle B, Holubkov R, Lukas MA, Tani LY (2007) Carvedilol for children and adolescents with heart failure: a randomized controlled trial. JAMA 298:1171-1179 (Pubitemid 47403103)
83. Shan Y, Napoli E, Cortopassi G (2007) Mitochondrial frataxin interacts with ISD11 of the NFS1/ISCU complex and multiple mitochondrial chaperones. Hum Mol Genet 16:929-941 (Pubitemid 47062737)
84. Skre H (1975) Friedreich's ataxia in Western Norway. Clin Genet 7:287-298
85. Stemmler TL, Lesuisse E, Pain D, Dancis A (2010) Frataxin and mitochondrial FeS cluster biogenesis. J Biol Chem 285: 26737-26743
86. Toro A, Grunebaum E (2006) TAT-mediated intracellular delivery of purine nucleoside phosphorylase corrects its deficiency in mice. J Clin Invest 116:2717-2726 (Pubitemid 44511635)
87. Velasco-Sanchez D, Aracil A, Montero R, Mas A, Jimenez L, O'Callaghan M, Tondo M, Capdevila A, Blanch J, Artuch R, Pineda M (2010) Combined therapy with idebenone and deferiprone in patients with Friedreich's ataxia. Cerebellum 10:1-8
88. Vyas PM, Payne RM (2008) TAT opens the door. Mol Ther 16:647-648 (Pubitemid 351426164)
89. Watson MS, Mann MY, Lloyd-Puryear MA, Rinaldo P (2006) Newborn screening: toward a uniform screening panel and system. Genet Med 8:1S-11S
90. Whitnall M, Rahmanto YS, Sutak R, Xu X, Becker EM, Mikhael MR, Ponka P, Richardson DR (2008) The MCK mouse heart model of Friedreich's ataxia: alterations in iron-regulated proteins and cardiac hypertrophy are limited by iron chelation. Proc Natl Acad Sci USA 105:9757-9762 (Pubitemid 352031373)
91. Yoon T, Cowan JA (2004) Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis. J Biol Chem 279:25943-25946 (Pubitemid 38798734)
92. Zhang Y, Lyver ER, Knight SA, Pain D, Lesuisse E, Dancis A (2006) Mrs3p, Mrs4p, and frataxin provide iron for Fe-S cluster synthesis in mitochondria. J Biol Chem 281:22493-22502
93. Zhang XY, Dinh A, Cronin J, Li SC, Reiser J (2008) Cellular uptake and lysosomal delivery of galactocerebrosidase tagged with the HIV TAT protein transduction domain. J Neurochem 104:1055-1064 (Pubitemid 351143640)