Inherited cardiomyopathies

New England Journal of Medicine

Volumn 364, Issue 17, 2011, Pages 1643-1656

  Watkins, Hugh ^a,b   Ashrafian, Houman ^a   Redwood, Charles ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 2 RECEPTOR ANTAGONIST; CARDIAC MYOSIN; MYOSIN HEAVY CHAIN BETA;

ARRHYTHMOGENESIS; CARDIOMYOPATHY; CLINICAL PRACTICE; CONGESTIVE CARDIOMYOPATHY; DESMOSOME; DISEASE CLASSIFICATION; FAMILIAL DISEASE; GENE MUTATION; GENETIC HETEROGENEITY; GENOTYPE PHENOTYPE CORRELATION; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MISSENSE MUTATION; MOLECULAR GENETICS; PATHOGENESIS; PENETRANCE; PRIORITY JOURNAL; REVIEW;

EID: 79955519460     PISSN: 00284793     EISSN: 15334406     Source Type: Journal    
DOI: 10.1056/NEJMra0902923     Document Type: Review

References (98)

1. Jarcho JA, McKenna W, Pare JA, et al. Mapping a gene for familial hypertrophic cardiomyopathy to chromosome 14q1. N Engl J Med 1989;321:1372-8. (Pubitemid 19284194)
2. Geisterfer-Lowrance AA, Kass S, Tanigawa G, et al. A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation. Cell 1990;62:999-1006.
3. Thierfelder L, Watkins H, MacRae C, et al. Alpha-tropomyosin and cardiac troponin T mutations cause familial hypertrophic cardiomyopathy: a disease of the sarcomere. Cell 1994;77:701-12.
4. Dietz HC. New therapeutic approaches to mendelian disorders. N Engl J Med 2010;363:852-63.
5. Maron BJ, Towbin JA, Thiene G, et al. Contemporary definitions and classification of the cardiomyopathies: an American Heart Association Scientific Statement from the Council on Clinical Cardiology, Heart Failure and Transplantation Committee; Quality of Care and Outcomes Research and Functional Ge- nomics and Translational Biology Interdisciplinary Working Groups; and Council on Epidemiology and Prevention. Circulation 2006;113:1807-16. (Pubitemid 43958474)
6. Elliott P, Andersson B, Arbustini E, et al. Classification of the cardiomyopathies: a position statement from the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J 2008;29:270-6.
7. Kamisago M, Sharma SD, DePalma SR, et al. Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N Engl J Med 2000;343:1688-96.
8. Richard P, Charron P, Carrier L, et al. Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation 2003;107: 2227-32. [Erratum, Circulation 2004;109: 3258.] (Pubitemid 36547217)
9. Marston S, Copeland O, Jacques A, et al. Evidence from human myectomy samples that MYBPC3 mutations cause hypertrophic cardiomyopathy through haploin-sufficiency. Circ Res 2009;105:219-22.
10. van Dijk SJ, Dooijes D, dos Remedios C, et al. Cardiac myosin-binding protein C mutations and hypertrophic cardiomyopathy: haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction. Circulation 2009;119:1473-83.
11. Redwood CS, Moolman-Smook JC, Watkins H. Properties of mutant contractile proteins that cause hypertrophic cardiomyopathy. Cardiovasc Res 1999;44:20-36. (Pubitemid 29431681)
12. Seidman JG, Seidman C. The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 2001;104:557-67. (Pubitemid 32201950)
13. Knollmann BC, Kirchhof P, Sirenko SG, et al. Familial hypertrophic cardiomyopathy-linked mutant troponin T causes stress-induced ventricular tachycardia and Ca2+-dependent action potential remodeling. Circ Res 2003;92:428-36. (Pubitemid 36298203)
14. Bers DM, Guo T. Calcium signaling in cardiac ventricular myocytes. Ann N Y Acad Sci 2005;1047:86-98. (Pubitemid 41123830)
15. Huke S, Knollmann BC. Increased myofilament Ca2+-sensitivity and arrhythmia susceptibility. J Mol Cell Cardiol 2010;48:824-33.
16. Robinson P, Griffiths PJ, Watkins H, Redwood CS. Dilated and hypertrophic cardiomyopathy mutations in troponin and alpha-tropomyosin have opposing effects on the calcium affinity of cardiac thin filaments. Circ Res 2007;101:1266-73. (Pubitemid 350294643)
17. Smith GA, Dixon HB, Kirschenlohr HL, Grace AA, Metcalfe JC, Vandenberg JI. Ca2+ buffering in the heart: Ca2+ binding to and activation of cardiac myofibrils. Biochem J 2000;346:393-402. (Pubitemid 30148125)
18. Kataoka A, Hemmer C, Chase PB. Computational simulation of hypertrophic cardiomyopathy mutations in troponin I: influence of increased myofilament calcium sensitivity on isometric force, ATPase and [Ca2+]i. J Biomech 2007;40: 2044-52. (Pubitemid 46843007)
19. Ashrafian H, Redwood C, Blair E, Watkins H. Hypertrophic cardiomyopathy: a paradigm for myocardial energy depletion. Trends Genet 2003;19:263-8. (Pubitemid 36507008)
20. Belus A, Piroddi N, Scellini B, et al. The familial hypertrophic cardiomyopathy-associated myosin mutation R403Q accelerates tension generation and relaxation of human cardiac myofibrils. J Physiol 2008;586:3639-44.
21. Spindler M, Saupe KW, Christe ME, et al. Diastolic dysfunction and altered energetics in the alphaMHC403/+ mouse model of familial hypertrophic cardiomyopathy. J Clin Invest 1998;101:1775-83. (Pubitemid 28198508)
22. Crilley JG, Boehm EA, Blair E, et al. Hypertrophic cardiomyopathy due to sarcomeric gene mutations is characterized by impaired energy metabolism irrespective of the degree of hypertrophy. J Am Coll Cardiol 2003;41:1776-82. (Pubitemid 36584252)
23. Geier C, Gehmlich K, Ehler E, et al. Beyond the sarcomere: CSRP3 mutations cause hypertrophic cardiomyopathy. Hum Mol Genet 2008;17:2753-65.
24. Chiu C, Bagnall RD, Ingles J, et al. Mutations in alpha-actinin-2 cause hypertrophic cardiomyopathy: a genome-wide analysis. J Am Coll Cardiol 2010;55:1127-35.
25. Hayashi T, Arimura T, Itoh-Satoh M, et al. Tcap gene mutations in hypertrophic cardiomyopathy and dilated cardiomyopathy. J Am Coll Cardiol 2004;44:2192-201. (Pubitemid 39576040)
26. Arimura T, Bos JM, Sato A, et al. Cardiac ankyrin repeat protein gene (ANKRD1) mutations in hypertrophic cardiomyopathy. J Am Coll Cardiol 2009; 54:334-42.
27. Landstrom AP, Weisleder N, Batalden KB, et al. Mutations in JPH2-encoded junctophilin-2 associated with hypertrophic cardiomyopathy in humans. J Mol Cell Cardiol 2007;42:1026-35. (Pubitemid 46829202)
28. Osio A, Tan L, Chen SN, et al. Myozenin 2 is a novel gene for human hypertrophic cardiomyopathy. Circ Res 2007;100:766-8. (Pubitemid 46555681)
29. Blair E, Redwood C, Ashrafian H, et al. Mutations in the gamma(2) subunit of AMP-activated protein kinase cause familial hypertrophic cardiomyopathy: evidence for the central role of energy compromise in disease pathogenesis. Hum Mol Genet 2001;10:1215-20. (Pubitemid 32487544)
30. Kim AS, Miller EJ, Young LH. AMP- activated protein kinase: a core signalling pathway in the heart. Acta Physiol (Oxf) 2009;196:37-53.
31. Banerjee SK, McGaffin KR, Huang XN, Ahmad F. Activation of cardiac hypertrophic signaling pathways in a transgenic mouse with the human PRKAG2 Thr400Asn mutation. Biochim Biophys Acta 2010;1802:284-91.
32. Semsarian C, Ahmad I, Giewat M, et al. The L-type calcium channel inhibitor diltiazem prevents cardiomyopathy in a mouse model. J Clin Invest 2002;109:1013-20. (Pubitemid 34408576)
33. Petersen SE, Jerosch-Herold M, Hudsmith LE, et al. Evidence for microvascular dysfunction in hypertrophic cardiomyopathy: new insights from multiparametric magnetic resonance imaging. Circulation 2007;115:2418-25. (Pubitemid 46717964)
34. Ashrafian H, Frenneaux MP, Opie LH. Metabolic mechanisms in heart failure. Circulation 2007;116:434-48. (Pubitemid 47196549)
35. Abozguia K, Elliott P, McKenna WJ, et al. Metabolic modulator perhexiline corrects energy deficiency and improves exercise capacity in symptomatic hypertrophic cardiomyopathy. Circulation 2010;122:1562-9.
36. O'Hanlon R, Grasso A, Roughton M et al. Prognostic significance of myocardial fibrosis in hypertrophic cardiomyopathy. J Am Coll Cardiol 2010;56:867-74.
37. Ho CY, Lopez B, Coelho-Filho OR, et al. Myocardial fibrosis as an early manifestation of hypertrophic cardiomyopathy. N Engl J Med 2010;363:552-63.
38. Teekakirikul P, Eminaga S, Toka O, et al. Cardiac fibrosis in mice with hypertro- phic cardiomyopathy is mediated by non- myocyte proliferation and requires Tgf-beta. J Clin Invest 2010;120:3520-9.
39. Penicka M, Gregor P, Kerekes R, et al. The effects of candesartan on left ventricular hypertrophy and function in non- obstructive hypertrophic cardiomyopathy: a pilot, randomized study. J Mol Diagn 2009;11:35-41.
40. Baig MK, Goldman JH, Caforio AL, Coonar AS, Keeling PJ, McKenna WJ. Familial dilated cardiomyopathy: cardiac abnormalities are common in asymptomatic relatives and may represent early disease. J Am Coll Cardiol 1998;31:195-201. (Pubitemid 28064742)
41. DeWitt MM, MacLeod HM, Soliven B, McNally EM. Phospholamban R14 deletion results in late-onset, mild, hereditary dilated cardiomyopathy. J Am Coll Cardiol 2006;48:1396-8. (Pubitemid 44436827)
42. Jefferies JL, Towbin JA. Dilated cardiomyopathy. Lancet 2010;375:752-62.
43. Dellefave L, McNally EM. The genetics of dilated cardiomyopathy. Curr Opin Cardiol 2010 February 24 (Epub ahead of print).
44. Wolf CM, Wang L, Alcalai R, et al. Lamin A/C haploinsufficiency causes dilated cardiomyopathy and apoptosis-triggered cardiac conduction system disease. J Mol Cell Cardiol 2008;44:293-303.
45. Schönberger J, Wang L, Shin JT, et al. Mutation in the transcriptional coactivator EYA4 causes dilated cardiomyopathy and sensorineural hearing loss. Nat Genet 2005;37:418-22.
46. Schmitt JP, Debold EP, Ahmad F, et al. Cardiac myosin missense mutations cause dilated cardiomyopathy in mouse models and depress molecular motor function. Proc Natl Acad Sci U S A 2006;103:14525-30. (Pubitemid 44484783)
47. Debold EP, Schmitt JP, Patlak JB, et al. Hypertrophic and dilated cardiomyopathy mutations differentially affect the molecular force generation of mouse alpha- cardiac myosin in the laser trap assay. Am J Physiol Heart Circ Physiol 2007;293:H284-H291. (Pubitemid 47105083)
48. Mirza M, Marston S, Willott R, et al. Dilated cardiomyopathy mutations in three thin filament regulatory proteins result in a common functional phenotype. J Biol Chem 2005;280:28498-506. (Pubitemid 41105750)
49. Vatta M, Mohapatra B, Jimenez S, et al. Mutations in Cypher/ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. J Am Coll Cardiol 2003;42:2014-27. (Pubitemid 37485581)
50. Tsubata S, Bowles KR, Vatta M, et al. Mutations in the human delta-sarcoglycan gene in familial and sporadic dilated cardiomyopathy. J Clin Invest 2000;106:655-62.
51. Bowles NE, Bowles KR, Towbin JA. The "final common pathway" hypothesis and inherited cardiovascular disease: the role of cytoskeletal proteins in dilated cardiomyopathy. Herz 2000;25:168-75. (Pubitemid 30422160)
52. Miller MK, Granzier H, Ehler E, Gregorio CC. The sensitive giant: the role of titin-based stretch sensing complexes in the heart. Trends Cell Biol 2004;14:119-26. (Pubitemid 38293454)
53. Haghighi K, Kolokathis F, Gramolini AO, et al. A mutation in the human phos-pholamban gene, deleting arginine 14, results in lethal, hereditary cardiomyopathy. Proc Natl Acad Sci U S A 2006;103: 1388-93. (Pubitemid 43191175)
54. Malhotra R, Mason PK. Lamin A/C deficiency as a cause of familial dilated cardiomyopathy. Curr Opin Cardiol 2009; 24:203-8.
55. Mudd JO, Kass DA. Tackling heart failure in the twenty-first century. Nature 2008;451:919-28. (Pubitemid 351301747)
56. Foo RS, Mani K, Kitsis RN. Death begets failure in the heart. J Clin Invest 2005;115:565-71. (Pubitemid 40322226)
57. Sen-Chowdhry S, Morgan RD, Chambers JC, McKenna WJ. Arrhythmogenic cardiomyopathy: etiology, diagnosis, and treatment. Annu Rev Med 2010;61:233-53.
58. Asimaki A, Tandri H, Huang H, et al. A new diagnostic test for arrhythmogenic right ventricular cardiomyopathy. N Engl J Med 2009;360:1075-84.
59. Beffagna G, Occhi G, Nava A, et al. Regulatory mutations in transforming growth factor-beta3 gene cause arrhythmogenic right ventricular cardiomyopathy type 1. Cardiovasc Res 2005;65:366-73. (Pubitemid 40082478)
60. Merner ND, Hodgkinson KA, Haywood AF, et al. Arrhythmogenic right ventricular cardiomyopathy type 5 is a fully penetrant, lethal arrhythmic disorder caused by a missense mutation in the TMEM43 gene. Am J Hum Genet 2008; 82:809-21.
61. Matolweni LO, Bardien S, Rebello G, et al. Arrhythmogenic right ventricular cardiomyopathy type 6 (ARVC6): support for the locus assignment, narrowing of the critical region and mutation screening of three candidate genes. BMC Med Genet 2006;7:29.
62. Kirchhof P, Fabritz L, Zwiener M, et al. Age- and training-dependent development of arrhythmogenic right ventricular cardiomyopathy in heterozygous plakoglobin-deficient mice. Circulation 2006;114:1799-806. (Pubitemid 44673354)
63. Kaplan SR, Gard JJ, Protonotarios N, et al. Remodeling of myocyte gap junctions in arrhythmogenic right ventricular cardiomyopathy due to a deletion in plakoglobin (Naxos disease). Heart Rhythm 2004;1:3-11. (Pubitemid 38647241)
64. Garcia-Gras E, Lombardi R, Giocondo MJ, et al. Suppression of canonical Wnt/beta-catenin signaling by nuclear plakoglobin recapitulates phenotype of arrhythmogenic right ventricular cardio-myopathy. J Clin Invest 2006;116:2012-21. (Pubitemid 44033325)
65. Lombardi R, Dong J, Rodriguez G, et al. Genetic fate mapping identifies second heart field progenitor cells as a source of adipocytes in arrhythmogenic right ventricular cardiomyopathy. Circ Res 2009;104:1076-84.
66. Djouadi F, Lecarpentier Y, Hébert JL, Charron P, Bastin J, Coirault C. A potential link between peroxisome proliferator-activated receptor signalling and the pathogenesis of arrhythmogenic right ventricular cardiomyopathy. Cardiovasc Res 2009;84:83-90.
67. Lakdawala NK, Dellefave L, Redwood CS, et al. Familial dilated cardiomyopathy caused by an alpha-tropomyosin mutation: the distinctive natural history of sarcomeric dilated cardiomyopathy. J Am Coll Cardiol 2010;55:320-9.
68. Fatkin D, MacRae C, Sasaki T, et al. Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease. N Engl J Med 1999;341:1715-24.
69. Marcus FI, McKenna WJ, Sherrill D, et al. Diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia: proposed modification of the task force criteria. Circulation 2010;121:1533-41.
70. Oechslin EN, Attenhofer Jost CH, Rojas JR, Kaufmann PA, Jenni R et al. Long-term follow-up of 34 adults with isolated left ventricular noncompaction: a distinct cardiomyopathy with poor prognosis. J Am Coll Cardiol 2000;36:493-500.
71. Lofiego C, Biagini E, Pasquale F, et al. Wide spectrum of presentation and variable outcomes of isolated left ventricular non-compaction. Heart 2007;93:65-71. (Pubitemid 46094056)
72. Wordsworth S, Leal J, Blair E, et al. DNA testing for hypertrophic cardiomyopathy: a cost-effectiveness model. Eur Heart J 2010;31:926-35.
73. Arad M, Penas-Lado M, Monserrat L, et al. Gene mutations in apical hypertrophic cardiomyopathy. Circulation 2005;112:2805-11. (Pubitemid 41641675)
74. Kubo T, Gimeno JR, Bahl A, et al. Prevalence, clinical significance, and genetic basis of hypertrophic cardiomyopathy with restrictive phenotype. J Am Coll Cardiol 2007;49:2419-26. (Pubitemid 46962256)
75. Klaassen S, Probst S, Oechslin E, et al. Mutations in sarcomere protein genes in left ventricular noncompaction. Circulation 2008;117:2893-901. (Pubitemid 351787074)
76. Maron BJ, Roberts WC, Arad M, et al. Clinical outcome and phenotypic expression in LAMP2 cardiomyopathy. JAMA 2009;301:1253-9.
77. Monserrat L, Gimeno-Blanes JR, Marin F, et al. Prevalence of Fabry disease in a cohort of 508 unrelated patients with hypertrophic cardiomyopathy. J Am Coll Cardiol 2007;50:2399-403. (Pubitemid 50011583)
78. Watkins H, Ashrafian H, McKenna WJ. The genetics of hypertrophic cardio-myopathy: Teare redux. Heart 2008;94:1264-8.
79. Pasotti M, Klersy C, Pilotto A, et al. Long-term outcome and risk stratification in dilated cardiolaminopathies. J Am Coll Cardiol 2008;52:1250-60.
80. Meune C, Van Berlo JH, Anselme F, Bonne G, Pinto YM, Duboc D. Primary prevention of sudden death in patients with lamin A/C gene mutations. N Engl J Med 2006;354:209-10. (Pubitemid 43076737)
81. Watkins H, McKenna WJ, Thierfelder L, et al. Mutations in the genes for cardiac troponin T and alpha-tropomyosin in hypertrophic cardiomyopathy. N Engl J Med 1995;332:1058-64.
82. Niimura H, Bachinski LL, Sangwatanaroj S, et al. Mutations in the gene for cardiac myosin-binding protein C and late- onset familial hypertrophic cardiomyopathy. N Engl J Med 1998;338:1248-57. (Pubitemid 28216578)
83. Van Driest SL, Ellsworth EG, Ommen SR, Tajik AJ, Gersh BJ, Ackerman MJ. Prevalence and spectrum of thin filament mutations in an outpatient referral population with hypertrophic cardiomyopathy. Circulation 2003;108:445-51. (Pubitemid 36935538)
84. Blair E, Redwood C, Watkins H. Ascertainment strategies and genotype: phenotype correlations in hypertrophic cardiomyopathy. Circulation 2003;108(4):e24-e25.
85. Blair E, Price SJ, Baty CJ, Ostman-Smith I, Watkins H. Mutations in cis can confound genotype-phenotype correlations in hypertrophic cardiomyopathy. J Med Genet 2001;38:385-8.
86. Ingles J, Doolan A, Chiu C, Seidman J, Seidman C, Semsarian C. Compound and double mutations in patients with hyper- trophic cardiomyopathy: implications for genetic testing and counselling. J Med Genet 2005;42(10):e59.
87. Girolami F, Ho CY, Semsarian C, et al. Clinical features and outcome of hyper-trophic cardiomyopathy associated with triple sarcomere protein gene mutations. J Am Coll Cardiol 2010;55:1444-53.
88. Xu T, Yang Z, Vatta M, et al. Compound and digenic heterozygosity contributes to arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol 2010;55:587-97.
89. Dhandapany PS, Sadayappan S, Xue Y, et al. A common MYBPC3 (cardiac myosin binding protein C) variant associated with cardiomyopathies in South Asia. Nat Genet 2009;41:187-91.
90. Andersen PS, Havndrup O, Hougs L, et al. Diagnostic yield, interpretation, and clinical utility of mutation screening of sarcomere encoding genes in Danish hypertrophic cardiomyopathy patients and relatives. Hum Mutat 2009;30:363-70.
91. Olivotto I, Girolami F, Ackerman MJ, et al. Myofilament protein gene mutation screening and outcome of patients with hypertrophic cardiomyopathy. Mayo Clin Proc 2008;83:630-8. (Pubitemid 351810562)
92. Matkovich SJ, Van Booven DJ, Hindes A, et al. Cardiac signaling genes exhibit unexpected sequence diversity in sporadic cardiomyopathy, revealing HSPB7 polymorphisms associated with disease. J Clin Invest 2010;120:280-9.
93. Cinquetti R, Badi I, Campione M, et al. Transcriptional deregulation and a missense mutation define ANKRD1 as a candidate gene for total anomalous pulmonary venous return. Hum Mutat 2008;29:468-74. (Pubitemid 351536985)
94. Duboscq-Bidot L, Charron P, Ruppert V, et al. Mutations in the ANKRD1 gene encoding CARP are responsible for human dilated cardiomyopathy. Eur Heart J 2009;30:2128-36.
95. Maron BJ, Niimura H, Casey SA, et al. Development of left ventricular hypertrophy in adults in hypertrophic cardiomyopathy caused by cardiac myosin-binding protein C gene mutations. J Am Coll Cardiol 2001;38:315-21. (Pubitemid 32721755)
96. van Spaendonck-Zwarts KY, van Tintelen JP, van Veldhuisen DJ, et al. Peripartum cardiomyopathy as a part of familial dilated cardiomyopathy. Circulation 2010;121:2169-75.
97. Noutsias M, Fechner H, de Jonge H, et al. Human coxsackie-adenovirus receptor is colocalized with integrins alpha(v) beta(3) and alpha(v)beta(5) on the cardiomyocyte sarcolemma and upregulated in dilated cardiomyopathy: implications for cardiotropic viral infections. Circulation 2001;104:275-80. (Pubitemid 32666947)
98. Xiong D, Lee GH, Badorff C, et al. Dystrophin deficiency markedly increases enterovirus-induced cardiomyopathy: a genetic predisposition to viral heart disease. Nat Med 2002;8:872-7.