Cardiomyopathy in Friedreich ataxia: Clinical findings and research

Journal of Child Neurology

Volumn 27, Issue 9, 2012, Pages 1179-1186

  Payne, R Mark ^a   Wagner, Gregory R ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cardiomyopathy; frataxin; Friedreich ataxia; heart; mitochondria

Indexed keywords

CREATINE KINASE MM; FRATAXIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SIRTUIN 3; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ACETYLATION; AEROBIC METABOLISM; CARDIOMYOPATHY; CELL DAMAGE; CHROMOSOME 9Q; CONFERENCE PAPER; CONFORMATIONAL TRANSITION; CYTOSOL; DEACETYLATION; DISEASE COURSE; FRIEDREICH ATAXIA; GLUCOSE BLOOD LEVEL; HEART EJECTION FRACTION; HEART FAILURE; HEART LEFT VENTRICLE HYPERTROPHY; HEART MITOCHONDRION; HEART STROKE VOLUME; HEART VENTRICLE HYPERTROPHY; HYPERTROPHIC CARDIOMYOPATHY; IRON CHELATION; LIFESTYLE; LIPID METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; T WAVE;

ADOLESCENT; CARDIOMYOPATHIES; CHILD; CHILD, PRESCHOOL; ELECTROCARDIOGRAPHY; FEMALE; FRIEDREICH ATAXIA; HUMANS; IRON-BINDING PROTEINS; MALE; MITOCHONDRIA; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84865614351     PISSN: 08830738     EISSN: 17088283     Source Type: Journal    
DOI: 10.1177/0883073812448535     Document Type: Conference Paper

References (66)

1. Kwong JQ, Beal MF, Manfredi G. The role of mitochondria in inherited neurodegenerative diseases. J Neurochem. 2006 ; 97 (6). 1659-1675 (Pubitemid 43873659)
2. Schon EA, Manfredi G. Neuronal degeneration and mitochondrial dysfunction. J Clin Invest. 2003 ; 111 (3). 303
3. Schols L, Amoiridis G, Przuntek H, et al. Friedreich's ataxia. Revision of the phenotype according to molecular genetics. Brain. 1997 ; 120 (pt 12). 2131-2140 (Pubitemid 28014589)
4. Filla A, De Michele G, Marconi R, et al. Prevalence of hereditary ataxias and spastic paraplegias in Molise, a region of Italy. J Neurol. 1992 ; 239 (6). 351-353
5. Romeo G, Menozzi P, Ferlini A, et al. Incidence of Friedreich ataxia in Italy estimated from consanguineous marriages. Am J Hum Genet. 1983 ; 35 (3). 523-529 (Pubitemid 13095776)
6. Skre H. Friedreich's ataxia in Western Norway. Clin Genet. 1975 ; 7 (4). 287-298
7. Epplen C, Epplen JT, Frank G, et al. Differential stability of the (GAA)n tract in the Friedreich ataxia (STM7) gene. Hum Genet. 1997 ; 99 (6). 834-836 (Pubitemid 27243768)
8. Pandolfo M. Friedreich ataxia. Arch Neurol. 2008 ; 65 (10). 1296-1303
9. Patel PI, Isaya G. Friedreich ataxia: from GAA triplet-repeat expansion to frataxin deficiency. Am J Hum Genet. 2001 ; 69 (1). 15-24 (Pubitemid 32614014)
10. Montermini L, Richter A, Morgan K, et al. Phenotypic variability in Friedreich ataxia: role of the associated GAA triplet repeat expansion. Ann Neurol. 1997 ; 41 (5). 675-682 (Pubitemid 27212663)
11. Filla A, De Michele G, Cavalcanti F, et al. The relationship between trinucleotide (GAA) repeat length and clinical features in Friedreich ataxia. Am J Hum Genet. 1996 ; 59 (3). 554-560 (Pubitemid 26269033)
12. Rajagopalan B, Francis JM, Cooke F, et al. Analysis of the factors influencing the cardiac phenotype in Friedreich's ataxia. Mov Disord. 2010 ; 25 (7). 846-852
13. Evans-Galea MV, Carrodus N, Rowley SM, et al. FXN methylation predicts expression and clinical outcome in Friedreich ataxia. Ann Neurol. 2012 ; 71 (4). 487-497
14. Al-Mahdawi S, Pinto RM, Ismail O, et al. The Friedreich ataxia GAA repeat expansion mutation induces comparable epigenetic changes in human and transgenic mouse brain and heart tissues. Hum Mol Genet. 2008 ; 17 (5). 735-746 (Pubitemid 351292262)
15. Harding AE. 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. 1981 ; 104 (3). 589-620 (Pubitemid 12202197)
16. Reddy PL, Grewal RP. Friedreich's ataxia: a clinical and genetic analysis. Clin Neurol Neurosurg. 2007 ; 109 (2). 200-202 (Pubitemid 46073400)
17. De Biase I, Rasmussen A, Endres D, et al. Progressive GAA expansions in dorsal root ganglia of Friedreich's ataxia patients. Ann Neurol. 2007 ; 61 (1). 55-60 (Pubitemid 46214244)
18. Zhang Y, Lyver ER, Knight SA, et al. Mrs3p, Mrs4p, and frataxin provide iron for Fe-S cluster synthesis in mitochondria. J Biol Chem. 2006 ; 281 (32). 22493-22502
19. Huang ML, Becker EM, Whitnall M, et al. Elucidation of the mechanism of mitochondrial iron loading in Friedreich's ataxia by analysis of a mouse mutant. Proc Natl Acad Sci USA. 2009 ; 106 (38). 16381-16386
20. Yoon T, Cowan JA. Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis. J Biol Chem. 2004 ; 279 (25). 25943-25946 (Pubitemid 38798734)
21. Gakh O, Cavadini P, Isaya G. Mitochondrial processing peptidases. Biochim Biophys Acta. 2002 ; 1592 (1). 63-77 (Pubitemid 35015166)
22. Cavadini P, Adamec J, Taroni F, et al. Two-step processing of human frataxin by mitochondrial processing peptidase. Precursor and intermediate forms are cleaved at different rates. J Biol Chem. 2000 ; 275 (52). 41469-41475 (Pubitemid 32054983)
23. Condo I, Ventura N, Malisan F, et al. In vivo maturation of human frataxin. Hum Mol Genet. 2007 ; 16 (13). 1534-1540 (Pubitemid 47050667)
24. Schmucker S, Argentini M, Carelle-Calmels N, et al. The in vivo mitochondrial two-step maturation of human frataxin. Hum Mol Genet. 2008 ; 17 (22). 3521-3531
25. Correia AR, Wang T, Craig EA, Gomes CM. Iron-binding activity in yeast frataxin entails a trade off with stability in the alpha1/beta1 acidic ridge region. Biochem J. 2010 ; 426 (2). 197-203
26. Tsai CL, Barondeau DP. Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex. Biochemistry. 2010 ; 49 (43). 9132-9139
27. Stemmler TL, Lesuisse E, Pain D, Dancis A. Frataxin and mitochondrial FeS cluster biogenesis. J Biol Chem. 2010 ; 285 (35). 26737-26743
28. Schmucker S, Martelli A, Colin F, 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. 2011 ; 6 (1). e16199
29. Rotig A, de LP, Chretien D, et al. Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat Genet. 1997 ; 17 (2). 215-217
30. Lodi R, Cooper JM, Bradley JL, et al. Deficit of in vivo mitochondrial ATP production in patients with Friedreich ataxia. Proc Natl Acad Sci USA. 1999 ; 96 (20). 11492-11495 (Pubitemid 29487408)
31. Lodi R, Rajagopalan B, Blamire AM, et al. 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. 2001 ; 52 (1). 111-119 (Pubitemid 32835244)
32. Bulteau AL, O'Neill HA, Kennedy MC, et al. Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science. 2004 ; 305 (5681). 242-245 (Pubitemid 38886737)
33. Bunse M, Bit-Avragim N, Riefflin A, et al. Cardiac energetics correlates to myocardial hypertrophy in Friedreich's ataxia. Ann Neurol. 2003 ; 53 (1). 121-123 (Pubitemid 36083837)
34. Puccio H, Simon D, Cossee M, et al. Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat Genet. 2001 ; 27 (2). 181-186 (Pubitemid 32157445)
35. Thierbach R, Schulz TJ, Isken F, et al. Targeted disruption of hepatic frataxin expression causes impaired mitochondrial function, decreased life span and tumor growth in mice. Hum Mol Genet. 2005 ; 14 (24). 3857-3864 (Pubitemid 43020087)
36. Whitnall M, Rahmanto YS, Sutak R, et al. 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. 2008 ; 105 (28). 9757-9762 (Pubitemid 352031373)
37. Vyas PM, Tomamichel WJ, Pride PM, et al. A TAT-Frataxin fusion protein increases lifespan and cardiac function in a conditional Friedreich's ataxia mouse model. Hum Mol Genet. 2012 ; 21 (6). 1230-1247
38. Michael S, Petrocine SV, Qian J, et al. Iron and iron-responsive proteins in the cardiomyopathy of Friedreich's ataxia. Cerebellum. 2006 ; 5 (4). 257-267 (Pubitemid 44875782)
39. Kakhlon O, Manning H, Breuer W, et al. Cell functions impaired by frataxin deficiency are restored by drug-mediated iron relocation. Blood. 2008 ; 112 (13). 5219-5227
40. Wong A, Yang J, Cavadini P, 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. 1999 ; 8 (3). 425-430 (Pubitemid 29097330)
41. Chantrel-Groussard K, Geromel V, Puccio H, et al. Disabled early recruitment of antioxidant defenses in Friedreich's ataxia. Hum Mol Genet. 2001 ; 10 (19). 2061
42. Bulteau AL, Planamente S, Jornea L, et al. Changes in mitochondrial glutathione levels and protein thiol oxidation in yfh1 yeast cells and the lymphoblasts of patients with Friedreich's ataxia. Biochimica et Biophysica Acta. 2012 ; 1822 (2). 212-225
43. Seznec H, Simon D, Bouton C, et al. Friedreich ataxia: the oxidative stress paradox. Hum Mol Genet. 2005 ; 14 (4). 463-474 (Pubitemid 40277462)
44. Navarro JA, Ohmann E, Sanchez D, et al. Altered lipid metabolism in a Drosophila model of Friedreich's ataxia. Hum Mol Genet. 2010 ; 19 (14). 2828-2840
45. Coppola G, Burnett R, Perlman S, et al. A gene expression phenotype in lymphocytes from Friedreich ataxia patients. Ann Neurol. 2011 ; 70 (5). 790-804
46. Ventura-Clapier R, Garnier A, Veksler V. Energy metabolism in heart failure. J Physiol. 2004 ; 555 (pt 1). 1-13 (Pubitemid 38313058)
47. Lopaschuk GD, Ussher JR, Folmes CD, et al. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010 ; 90 (1). 207-258
48. Neubauer S. The failing heart-an engine out of fuel. New Engl J Med. 2007 ; 356 (11). 1140-1151 (Pubitemid 46425598)
49. Wagner GR, Pride PM, Babbey CM, Payne RM. Friedreich's Ataxia reveals a mechanism for coordinate regulation of oxidative metabolism via feedback inhibition of the SIRT3 deacetylase. Hum Mol Genet. 2012 ; 21 (12). 2688-97
50. Hirschey MD, Shimazu T, Goetzman E, et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature. 2010 ; 464 (7285). 121-125
51. Tsou AY, Paulsen EK, Lagedrost SJ, et al. Mortality in Friedreich ataxia. J Neurol Sci. 2011 ; 307 (1-2). 46-49
52. Kipps A, Alexander M, Colan SD, et al. The longitudinal course of cardiomyopathy in Friedreich's ataxia during childhood. Pediatr Cardiol. 2009 ; 30 (3). 306-310
53. Sherrid MV, Barac I, McKenna WJ, et al. Multicenter study of the efficacy and safety of disopyramide in obstructive hypertrophic cardiomyopathy. J Am Coll Cardiol. 2005 ; 45 (8). 1251-1258 (Pubitemid 40523146)
54. Raman SV, Phatak K, Hoyle JC, et al. Impaired myocardial perfusion reserve and fibrosis in Friedreich ataxia: a mitochondrial cardiomyopathy with metabolic syndrome. Eur Heart J. 2011 ; 32 (5). 561-567
55. Raman SV, Dickerson JA, Al-Dahhak R. Myocardial ischemia in the absence of epicardial coronary artery disease in Friedreich's ataxia. J Cardiovasc Magn Reson. 2008 ; 10: 15
56. Mottram PM, Delatycki MB, Donelan L, et al. Early changes in left ventricular long-axis function in Friedreich ataxia: relation with the FXN gene mutation and cardiac structural change. J Am Soc Echocardiogr. 2011 ; 24 (7). 782-789
57. Regner SR, Lagedrost SJ, Plappert T, et al. Analysis of echocardiograms in a large heterogeneous cohort of patients with Friedreich ataxia. Am J Cardiol. 2012 ; 109 (3). 401-405
58. Hanley A, Corrigan R, Mohammad S, MacMahon B. Friedreich's ataxia cardiomyopathy: case based discussion and management issues. Ir Med J. 2010 ; 103 (4). 117-118
59. Cook JD, Lynch SR. The liabilities of iron deficiency. Blood. 1986 ; 68 (4). 803-809 (Pubitemid 17183836)
60. Malo S, Latour Y, Cote M, et al. Electrocardiographic and vectocardiographic findings in Friedreich's ataxia. Can J Neurol Sci. 1976 ; 3 (4). 323-328 (Pubitemid 8067185)
61. Child JS, Perloff JK, Bach PM, et al. Cardiac involvement in Friedreich's ataxia: a clinical study of 75 patients. J Am Coll Cardiol. 1986 ; 7 (6). 1370-1378 (Pubitemid 16100362)
62. Isnard R, Kalotka H, Durr A, et al. Correlation between left ventricular hypertrophy and GAA trinucleotide repeat length in Friedreich's ataxia. Circulation. 1997 ; 95 (9). 2247
63. Koeppen AH. Friedreich's ataxia: pathology, pathogenesis, and molecular genetics. J Neurol Sci. 2011 ; 303 (1-2). 1-12
64. Delatycki MB, Williamson R, Forrest SM. Friedreich ataxia: an overview. J Med Genet. 2000 ; 37 (1). 1-8 (Pubitemid 30245868)
65. Cossee M, Puccio H, Gansmuller A, et al. Inactivation of the Friedreich ataxia mouse gene leads to early embryonic lethality without iron accumulation. Hum Mol Genet. 2000 ; 9 (8). 1219-1226 (Pubitemid 30248608)
66. Quercia N, Somers GR, Halliday W, et al. Friedreich ataxia presenting as sudden cardiac death in childhood: clinical, genetic and pathological correlation, with implications for genetic testing and counselling. Neuromuscul Disord. 2010 ; 20 (5). 340-342