The genetic landscape of cardiomyopathy and its role in heart failure

Cell Metabolism

Volumn 21, Issue 2, 2015, Pages 174-182

  McNally, Elizabeth M ^a   Barefield, David Y ^a   Puckelwartz, Megan J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIN;

CARDIOMYOPATHY; CONGESTIVE CARDIOMYOPATHY; GENE MUTATION; GENE THERAPY; GENETIC LINKAGE; GENETIC VARIABILITY; HEART FAILURE; HEART MUSCLE CONTRACTILITY; HEART OUTPUT; HERITABILITY; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MYOFILAMENT; PHENOTYPE; PRIORITY JOURNAL; REVIEW; THIN FILAMENT; ANIMAL; GENETICS; METABOLISM; PATHOLOGY;

ANIMALS; CARDIOMYOPATHIES; HEART FAILURE; HUMANS;

EID: 84922860426     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.01.013     Document Type: Review

References (104)

1. N.R. Alpert, S.A. Mohiddin, D. Tripodi, J. Jacobson-Hatzell, K. Vaughn-Whitley, C. Brosseau, D.M. Warshaw, and L. Fananapazir Molecular and phenotypic effects of heterozygous, homozygous, and compound heterozygote myosin heavy-chain mutations Am. J. Physiol. Heart Circ. Physiol. 288 2005 H1097 H1102
2. B.R. Anderson, and H.L. Granzier Titin-based tension in the cardiac sarcomere: molecular origin and physiological adaptations Prog. Biophys. Mol. Biol. 110 2012 204 217
3. C. Andreasen, J.B. Nielsen, L. Refsgaard, A.G. Holst, A.H. Christensen, L. Andreasen, A. Sajadieh, S. Haunsø, J.H. Svendsen, and M.S. Olesen New population-based exome data are questioning the pathogenicity of previously cardiomyopathy-associated genetic variants Eur. J. Hum. Genet. 21 2013 918 928
4. M. Arad, J.G. Seidman, and C.E. Seidman Phenotypic diversity in hypertrophic cardiomyopathy Hum. Mol. Genet. 11 2002 2499 2506
5. A.K. Arndt, and C.A. MacRae Genetic testing in cardiovascular diseases Curr. Opin. Cardiol. 29 2014 235 240
6. D. Barefield, and S. Sadayappan Phosphorylation and function of cardiac myosin binding protein-C in health and disease J. Mol. Cell. Cardiol. 48 2010 866 875
7. D. Barefield, M. Kumar, P.P. de Tombe, and S. Sadayappan Contractile dysfunction in a mouse model expressing a heterozygous MYBPC3 mutation associated with hypertrophic cardiomyopathy Am. J. Physiol. Heart Circ. Physiol. 306 2014 H807 H815
8. D. Barefield, M. Kumar, J. Gorham, J.G. Seidman, C.E. Seidman, P.P. de Tombe, and S. Sadayappan Haploinsufficiency of MYBPC3 exacerbates the development of hypertrophic cardiomyopathy in heterozygous mice J. Mol. Cell. Cardiol. 79 2015 234 243
9. K.L. Bezold, J.F. Shaffer, J.K. Khosa, E.R. Hoye, and S.P. Harris A gain-of-function mutation in the M-domain of cardiac myosin-binding protein-C increases binding to actin J. Biol. Chem. 288 2013 21496 21505
10. E. Blair, C. Redwood, M. de Jesus Oliveira, J.C. Moolman-Smook, P. Brink, V.A. Corfield, I. Ostman-Smith, and H. Watkins Mutations of the light meromyosin domain of the beta-myosin heavy chain rod in hypertrophic cardiomyopathy Circ. Res. 90 2002 263 269
11. M. Bloemink, J. Deacon, S. Langer, C. Vera, A. Combs, L. Leinwand, and M.A. Geeves The hypertrophic cardiomyopathy myosin mutation R453C alters ATP binding and hydrolysis of human cardiac β-myosin J. Biol. Chem. 289 2014 5158 5167
12. P. Charron, O. Dubourg, M. Desnos, R. Isnard, A. Hagege, G. Bonne, L. Carrier, F. Tesson, J.B. Bouhour, and J.C. Buzzi Genotype-phenotype correlations in familial hypertrophic cardiomyopathy. A comparison between mutations in the cardiac protein-C and the beta-myosin heavy chain genes Eur. Heart J. 19 1998 139 145
13. C.S. Chung, K.R. Hutchinson, M. Methawasin, C. Saripalli, J.E. Smith 3rd, C.G. Hidalgo, X. Luo, S. Labeit, C. Guo, and H.L. Granzier Shortening of the elastic tandem immunoglobulin segment of titin leads to diastolic dysfunction Circulation 128 2013 19 28
14. J.G. Cleland, J.R. Teerlink, R. Senior, E.M. Nifontov, J.J. Mc Murray, C.C. Lang, V.A. Tsyrlin, B.H. Greenberg, J. Mayet, and D.P. Francis The effects of the cardiac myosin activator, omecamtiv mecarbil, on cardiac function in systolic heart failure: a double-blind, placebo-controlled, crossover, dose-ranging phase 2 trial Lancet 378 2011 676 683
15. J.G. Crilley, E.A. Boehm, E. Blair, B. Rajagopalan, A.M. Blamire, P. Styles, W.J. McKenna, I. Ostman-Smith, K. Clarke, and H. Watkins Hypertrophic cardiomyopathy due to sarcomeric gene mutations is characterized by impaired energy metabolism irrespective of the degree of hypertrophy J. Am. Coll. Cardiol. 41 2003 1776 1782
16. L.M. Dellefave, P. Pytel, S. Mewborn, B. Mora, D.L. Guris, S. Fedson, D. Waggoner, I. Moskowitz, and E.M. McNally Sarcomere mutations in cardiomyopathy with left ventricular hypertrabeculation Circ Cardiovasc Genet 2 2009 442 449
17. M.M. DeWitt, H.M. MacLeod, B. Soliven, and E.M. McNally Phospholamban R14 deletion results in late-onset, mild, hereditary dilated cardiomyopathy J. Am. Coll. Cardiol. 48 2006 1396 1398
18. P.S. Dhandapany, S. Sadayappan, Y. Xue, G.T. Powell, D.S. Rani, P. Nallari, T.S. Rai, M. Khullar, P. Soares, and A. Bahl A common MYBPC3 (cardiac myosin binding protein C) variant associated with cardiomyopathies in South Asia Nat. Genet. 41 2009 187 191
19. S.M. Dunlay, N.D. Shah, Q. Shi, B. Morlan, H. VanHouten, K.H. Long, and V.L. Roger Lifetime costs of medical care after heart failure diagnosis Circ Cardiovasc Qual Outcomes 4 2011 68 75
20. A. Freiburg, and M. Gautel A molecular map of the interactions between titin and myosin-binding protein C. Implications for sarcomeric assembly in familial hypertrophic cardiomyopathy Eur. J. Biochem. 235 1996 317 323
21. A. Freiburg, K. Trombitas, W. Hell, O. Cazorla, F. Fougerousse, T. Centner, B. Kolmerer, C. Witt, J.S. Beckmann, and C.C. Gregorio Series of exon-skipping events in the elastic spring region of titin as the structural basis for myofibrillar elastic diversity Circ. Res. 86 2000 1114 1121
22. D.O. Fürst, M. Osborn, R. Nave, and K. Weber The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line J. Cell Biol. 106 1988 1563 1572
23. M. Gautel Cytoskeletal protein kinases: titin and its relations in mechanosensing Pflugers Archiv. Eur. J. Physiol. 462 2011 119 134
24. K. Gehmlich, M.S. Dodd, J. William Allwood, M. Kelly, M. Bellahcene, H.V. Lad, A. Stockenhuber, C. Hooper, H. Ashrafian, and C.S. Redwood Changes in the cardiac metabolome caused by perhexiline treatment in a mouse model of hypertrophic cardiomyopathy Mol. Biosyst. 11 2015 564 573
25. A.A. Geisterfer-Lowrance, M. Christe, D.A. Conner, J.S. Ingwall, F.J. Schoen, C.E. Seidman, and J.G. Seidman A mouse model of familial hypertrophic cardiomyopathy Science 272 1996 731 734
26. R. Gilbert, M.G. Kelly, T. Mikawa, and D.A. Fischman The carboxyl terminus of myosin binding protein C (MyBP-C, C-protein) specifies incorporation into the A-band of striated muscle J. Cell Sci. 109 1996 101 111
27. F. Girolami, C.Y. Ho, C. Semsarian, M. Baldi, M.L. Will, K. Baldini, F. Torricelli, L. Yeates, F. Cecchi, M.J. Ackerman, and I. Olivotto Clinical features and outcome of hypertrophic cardiomyopathy associated with triple sarcomere protein gene mutations J. Am. Coll. Cardiol. 55 2010 1444 1453
28. J.R. Golbus, M.J. Puckelwartz, J.P. Fahrenbach, L.M. Dellefave-Castillo, D. Wolfgeher, and E.M. McNally Population-based variation in cardiomyopathy genes Circ Cardiovasc Genet 5 2012 391 399
29. J.R. Golbus, M.J. Puckelwartz, L. Dellefave-Castillo, J.P. Fahrenbach, V. Nelakuditi, L.L. Pesce, P. Pytel, and E.M. McNally Targeted analysis of whole genome sequence data to diagnose genetic cardiomyopathy Circ Cardiovasc Genet 7 2014 751 759
30. H.L. Granzier, M.H. Radke, J. Peng, D. Westermann, O.L. Nelson, K. Rost, N.M. King, Q. Yu, C. Tschöpe, and M. McNabb Truncation of titin's elastic PEVK region leads to cardiomyopathy with diastolic dysfunction Circ. Res. 105 2009 557 564
31. H.L. Granzier, K.R. Hutchinson, P. Tonino, M. Methawasin, F.W. Li, R.E. Slater, M.M. Bull, C. Saripalli, C.T. Pappas, C.C. Gregorio, and J.E. Smith 3rd Deleting titin's I-band/A-band junction reveals critical roles for titin in biomechanical sensing and cardiac function Proc. Natl. Acad. Sci. USA 111 2014 14589 14594
32. K. Haghighi, F. Kolokathis, A.O. Gramolini, J.R. Waggoner, L. Pater, R.A. Lynch, G.C. Fan, D. Tsiapras, R.R. Parekh, and G.W. Dorn II A mutation in the human phospholamban gene, deleting arginine 14, results in lethal, hereditary cardiomyopathy Proc. Natl. Acad. Sci. USA 103 2006 1388 1393
33. S.P. Harris, C.R. Bartley, T.A. Hacker, K.S. McDonald, P.S. Douglas, M.L. Greaser, P.A. Powers, and R.L. Moss Hypertrophic cardiomyopathy in cardiac myosin binding protein-C knockout mice Circ. Res. 90 2002 594 601
34. P.A. Heidenreich, N.M. Albert, L.A. Allen, D.A. Bluemke, J. Butler, G.C. Fonarow, J.S. Ikonomidis, O. Khavjou, M.A. Konstam, T.M. Maddox American Heart Association Advocacy Coordinating Committee Council on Arteriosclerosis, Thrombosis and Vascular Biology Council on Cardiovascular Radiology and Intervention Council on Clinical Cardiology Council on Epidemiology and Prevention Stroke Council Forecasting the impact of heart failure in the United States: a policy statement from the American Heart Association Circ Heart Fail 6 2013 606 619
35. A.S. Helms, F.M. Davis, D. Coleman, S.N. Bartolone, A.A. Glazier, F. Pagani, J.M. Yob, S. Sadayappan, E. Pedersen, and R. Lyons Sarcomere mutation-specific expression patterns in human hypertrophic cardiomyopathy Circ Cardiovasc Genet 7 2014 434 443
36. D.S. Herman, L. Lam, M.R. Taylor, L. Wang, P. Teekakirikul, D. Christodoulou, L. Conner, S.R. DePalma, B. McDonough, and E. Sparks Truncations of titin causing dilated cardiomyopathy N. Engl. J. Med. 366 2012 619 628
37. R.E. Hershberger, D.J. Hedges, and A. Morales Dilated cardiomyopathy: the complexity of a diverse genetic architecture Nat. Rev. Cardiol. 10 2013 531 547
38. J. Ingles, A. Doolan, C. Chiu, J. Seidman, C. Seidman, and C. Semsarian Compound and double mutations in patients with hypertrophic cardiomyopathy: implications for genetic testing and counselling J. Med. Genet. 42 2005 e59
39. J.S. Ingwall The energetic cost of contraction is higher in the myocardium of patients with hypertrophic cardiomyopathy Cardiovasc. Res. 103 2014 192 193
40. E.M. Jeong, M.M. Monasky, L. Gu, D.M. Taglieri, B.G. Patel, H. Liu, Q. Wang, I. Greener, S.C. Dudley Jr., and R.J. Solaro Tetrahydrobiopterin improves diastolic dysfunction by reversing changes in myofilament properties J. Mol. Cell. Cardiol. 56 2013 44 54
41. J. Jiang, H. Wakimoto, J.G. Seidman, and C.E. Seidman Allele-specific silencing of mutant Myh6 transcripts in mice suppresses hypertrophic cardiomyopathy Science 342 2013 111 114
42. A.M. Katz Ernest Henry Starling, his predecessors, and the "Law of the Heart" Circulation 106 2002 2986 2992
43. R.W. Kensler, J.F. Shaffer, and S.P. Harris Binding of the N-terminal fragment C0-C2 of cardiac MyBP-C to cardiac F-actin J. Struct. Biol. 174 2011 44 51
44. F.S. Korte, T.J. Herron, M.J. Rovetto, and K.S. McDonald Power output is linearly related to MyHC content in rat skinned myocytes and isolated working hearts Am. J. Physiol. Heart Circ. Physiol. 289 2005 H801 H812
45. G. Kunst, K.R. Kress, M. Gruen, D. Uttenweiler, M. Gautel, and R.H. Fink Myosin binding protein C, a phosphorylation-dependent force regulator in muscle that controls the attachment of myosin heads by its interaction with myosin S2 Circ. Res. 86 2000 51 58
46. S. Labeit, M. Gautel, A. Lakey, and J. Trinick Towards a molecular understanding of titin EMBO J. 11 1992 1711 1716
47. E.J. Lee, J. Peng, M. Radke, M. Gotthardt, and H.L. Granzier Calcium sensitivity and the Frank-Starling mechanism of the heart are increased in titin N2B region-deficient mice J. Mol. Cell. Cardiol. 49 2010 449 458
48. W. Lehman, V. Hatch, V. Korman, M. Rosol, L. Thomas, R. Maytum, M.A. Geeves, J.E. Van Eyk, L.S. Tobacman, and R. Craig Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments J. Mol. Biol. 302 2000 593 606
49. R.H. Lekanne Deprez, J.J. Muurling-Vlietman, J. Hruda, M.J. Baars, L.C. Wijnaendts, I. Stolte-Dijkstra, M. Alders, and J.M. van Hagen Two cases of severe neonatal hypertrophic cardiomyopathy caused by compound heterozygous mutations in the MYBPC3 gene J. Med. Genet. 43 2006 829 832
50. H.L. Li, N. Fujimoto, N. Sasakawa, S. Shirai, T. Ohkame, T. Sakuma, M. Tanaka, N. Amano, A. Watanabe, and H. Sakurai Precise correction of the dystrophin gene in Duchenne muscular dystrophy patient induced pluripotent stem cells by TALEN and CRISPR-Cas9 Stem Cell Rep. 4 2014 143 154
51. C. Long, J.R. McAnally, J.M. Shelton, A.A. Mireault, R. Bassel-Duby, and E.N. Olson Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA Science 345 2014 1184 1188
52. S. Lowey, L.M. Lesko, A.S. Rovner, A.R. Hodges, S.L. White, R.B. Low, M. Rincon, J. Gulick, and J. Robbins Functional effects of the hypertrophic cardiomyopathy R403Q mutation are different in an alpha- or beta-myosin heavy chain backbone J. Biol. Chem. 283 2008 20579 20589
53. D.G. MacArthur, T.A. Manolio, D.P. Dimmock, H.L. Rehm, J. Shendure, G.R. Abecasis, D.R. Adams, R.B. Altman, S.E. Antonarakis, and E.A. Ashley Guidelines for investigating causality of sequence variants in human disease Nature 508 2014 469 476
54. H. Mahrholdt, A. Wagner, R.M. Judd, U. Sechtem, and R.J. Kim Delayed enhancement cardiovascular magnetic resonance assessment of non-ischaemic cardiomyopathies Eur. Heart J. 26 2005 1461 1474
55. F.I. Malik, J.J. Hartman, K.A. Elias, B.P. Morgan, H. Rodriguez, K. Brejc, R.L. Anderson, S.H. Sueoka, K.H. Lee, and J.T. Finer Cardiac myosin activation: a potential therapeutic approach for systolic heart failure Science 331 2011 1439 1443
56. A.J. Marian Pathogenesis of diverse clinical and pathological phenotypes in hypertrophic cardiomyopathy Lancet 355 2000 58 60
57. B.J. Maron, J.M. Gardin, J.M. Flack, S.S. Gidding, T.T. Kurosaki, and D.E. Bild Prevalence of hypertrophic cardiomyopathy in a general population of young adults. Echocardiographic analysis of 4111 subjects in the CARDIA Study. Coronary Artery Risk Development in (Young) Adults Circulation 92 1995 785 789
58. B.J. Maron, H. Niimura, S.A. Casey, M.K. Soper, G.B. Wright, J.G. Seidman, and C.E. Seidman Development of left ventricular hypertrophy in adults in hypertrophic cardiomyopathy caused by cardiac myosin-binding protein C gene mutations J. Am. Coll. Cardiol. 38 2001 315 321
59. B.J. Maron, J.A. Towbin, G. Thiene, C. Antzelevitch, D. Corrado, D. Arnett, A.J. Moss, C.E. Seidman, J.B. Young American Heart Association Council on Clinical Cardiology, Heart Failure and Transplantation Committee Quality of Care and Outcomes Research and Functional Genomics and Translational Biology Interdisciplinary Working Groups Council on Epidemiology and Prevention 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 Genomics and Translational Biology Interdisciplinary Working Groups; and Council on Epidemiology and Prevention Circulation 113 2006 1807 1816
60. S. Marston, O. Copeland, A. Jacques, K. Livesey, V. Tsang, W.J. McKenna, S. Jalilzadeh, S. Carballo, C. Redwood, and H. Watkins Evidence from human myectomy samples that MYBPC3 mutations cause hypertrophic cardiomyopathy through haploinsufficiency Circ. Res. 105 2009 219 222
61. D.F. McKillop, and M.A. Geeves Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament Biophys. J. 65 1993 693 701
62. E.M. McNally, J.R. Golbus, and M.J. Puckelwartz Genetic mutations and mechanisms in dilated cardiomyopathy J. Clin. Invest. 123 2013 19 26
63. G. Mearini, D. Stimpel, B. Geertz, F. Weinberger, E. Krämer, S. Schlossarek, J. Mourot-Filiatre, A. Stoehr, A. Dutsch, and P.J. Wijnker Mybpc3 gene therapy for neonatal cardiomyopathy enables long-term disease prevention in mice Nat. Commun. 5 2014 5515
64. J.R. Moore, L. Leinwand, and D.M. Warshaw Understanding cardiomyopathy phenotypes based on the functional impact of mutations in the myosin motor Circ. Res. 111 2012 375 385
65. R.K. Moore, S. Abdullah, and J.C. Tardiff Allosteric effects of cardiac troponin TNT1 mutations on actomyosin binding: a novel pathogenic mechanism for hypertrophic cardiomyopathy Arch. Biochem. Biophys. 552-553 2014 21 28
66. J.Y. Mun, M.J. Previs, H.Y. Yu, J. Gulick, L.S. Tobacman, S. Beck Previs, J. Robbins, D.M. Warshaw, and R. Craig Myosin-binding protein C displaces tropomyosin to activate cardiac thin filaments and governs their speed by an independent mechanism Proc. Natl. Acad. Sci. USA 111 2014 2170 2175
67. J.L. Myhre, J.A. Hills, K. Prill, S.L. Wohlgemuth, and D.B. Pilgrim The titin A-band rod domain is dispensable for initial thick filament assembly in zebrafish Dev. Biol. 387 2014 93 108
68. I. Olivotto, F. Girolami, M.J. Ackerman, S. Nistri, J.M. Bos, E. Zachara, S.R. Ommen, J.L. Theis, R.A. Vaubel, and F. Re Myofilament protein gene mutation screening and outcome of patients with hypertrophic cardiomyopathy Mayo Clin. Proc. 83 2008 630 638
69. I. Olivotto, F. Girolami, R. Sciagrà, M.J. Ackerman, B. Sotgia, J.M. Bos, S. Nistri, A. Sgalambro, C. Grifoni, and F. Torricelli Microvascular function is selectively impaired in patients with hypertrophic cardiomyopathy and sarcomere myofilament gene mutations J. Am. Coll. Cardiol. 58 2011 839 848
70. S. Pan, C.A. Caleshu, K.E. Dunn, M.J. Foti, M.K. Moran, O. Soyinka, and E.A. Ashley Cardiac structural and sarcomere genes associated with cardiomyopathy exhibit marked intolerance of genetic variation Circ Cardiovasc Genet 5 2012 602 610
71. B.G. Patel, T. Wilder, and R.J. Solaro Novel control of cardiac myofilament response to calcium by S-glutathionylation at specific sites of myosin binding protein C Front. Physiol. 4 2013 336
72. M.J. Previs, S. Beck Previs, J. Gulick, J. Robbins, and D.M. Warshaw Molecular mechanics of cardiac myosin-binding protein C in native thick filaments Science 337 2012 1215 1218
73. P. Richard, R. Isnard, L. Carrier, O. Dubourg, Y. Donatien, B. Mathieu, G. Bonne, F. Gary, P. Charron, and M. Hagege Double heterozygosity for mutations in the beta-myosin heavy chain and in the cardiac myosin binding protein C genes in a family with hypertrophic cardiomyopathy J. Med. Genet. 36 1999 542 545
74. C. Rickers, N.M. Wilke, M. Jerosch-Herold, S.A. Casey, P. Panse, N. Panse, J. Weil, A.G. Zenovich, and B.J. Maron Utility of cardiac magnetic resonance imaging in the diagnosis of hypertrophic cardiomyopathy Circulation 112 2005 855 861
75. G.R. Ritchie, and P. Flicek Computational approaches to interpreting genomic sequence variation Genome Med. 6 2014 87
76. A.M. Roberts, J.S. Ware, D.S. Herman, S. Schafer, J. Baksi, A.G. Bick, R.J. Buchan, R. Walsh, S. John, and S. Wilkinson Integrated allelic, transcriptional, and phenomic dissection of the cardiac effects of titin truncations in health and disease Sci. Transl. Med. 7 2015 270ra276
77. S. Sadayappan, J. Gulick, H. Osinska, L.A. Martin, H.S. Hahn, G.W. Dorn II, R. Klevitsky, C.E. Seidman, J.G. Seidman, and J. Robbins Cardiac myosin-binding protein-C phosphorylation and cardiac function Circ. Res. 97 2005 1156 1163
78. S. Sadayappan, H. Osinska, R. Klevitsky, J.N. Lorenz, M. Sargent, J.D. Molkentin, C.E. Seidman, J.G. Seidman, and J. Robbins Cardiac myosin binding protein C phosphorylation is cardioprotective Proc. Natl. Acad. Sci. USA 103 2006 16918 16923
79. E. Schaefer, P. Helms, L. Marcellin, P. Desprez, P. Billaud, V. Chanavat, R. Rousson, and G. Millat Next-generation sequencing (NGS) as a fast molecular diagnosis tool for left ventricular noncompaction in an infant with compound mutations in the MYBPC3 gene Eur. J. Med. Genet. 57 2014 129 132
80. J.P. Schmitt, E.P. Debold, F. Ahmad, A. Armstrong, A. Frederico, D.A. Conner, U. Mende, M.J. Lohse, D. Warshaw, C.E. Seidman, and J.G. Seidman Cardiac myosin missense mutations cause dilated cardiomyopathy in mouse models and depress molecular motor function Proc. Natl. Acad. Sci. USA 103 2006 14525 14530
81. C. Semsarian, M.J. Healey, D. Fatkin, M. Giewat, C. Duffy, C.E. Seidman, and J.G. Seidman A polymorphic modifier gene alters the hypertrophic response in a murine model of familial hypertrophic cardiomyopathy J. Mol. Cell. Cardiol. 33 2001 2055 2060
82. T.S. Simonson, Y. Zhang, C.D. Huff, J. Xing, W.S. Watkins, D.J. Witherspoon, S.R. Woodward, and L.B. Jorde Limited distribution of a cardiomyopathy-associated variant in India Ann. Hum. Genet. 74 2010 184 188
83. R.F. Sommese, J. Sung, S. Nag, S. Sutton, J.C. Deacon, E. Choe, L.A. Leinwand, K. Ruppel, and J.A. Spudich Molecular consequences of the R453C hypertrophic cardiomyopathy mutation on human β-cardiac myosin motor function Proc. Natl. Acad. Sci. USA 110 2013 12607 12612
84. M. Spindler, K.W. Saupe, M.E. Christe, H.L. Sweeney, C.E. Seidman, J.G. Seidman, and J.S. Ingwall Diastolic dysfunction and altered energetics in the alphaMHC403/+ mouse model of familial hypertrophic cardiomyopathy J. Clin. Invest. 101 1998 1775 1783
85. A. Srivastava, N. Garg, T. Mittal, R. Khanna, S. Gupta, P.K. Seth, and B. Mittal Association of 25 bp deletion in MYBPC3 gene with left ventricle dysfunction in coronary artery disease patients PLoS ONE 6 2011 e24123
86. K.A. Strauss, L. DuBiner, M. Simon, M. Zaragoza, P.P. Sengupta, P. Li, N. Narula, S. Dreike, J. Platt, and V. Procaccio Severity of cardiomyopathy associated with adenine nucleotide translocator-1 deficiency correlates with mtDNA haplogroup Proc. Natl. Acad. Sci. USA 110 2013 3453 3458
87. M. Suzuki, K.M. Carlson, D.A. Marchuk, and H.A. Rockman Genetic modifier loci affecting survival and cardiac function in murine dilated cardiomyopathy Circulation 105 2002 1824 1829
88. J.C. Tardiff Thin filament mutations: developing an integrative approach to a complex disorder Circ. Res. 108 2011 765 782
89. P. Teekakirikul, M.A. Kelly, H.L. Rehm, N.K. Lakdawala, and B.H. Funke Inherited cardiomyopathies: molecular genetics and clinical genetic testing in the postgenomic era J. Mol. Diagn. 15 2013 158 170
90. M.J. Tyska, E. Hayes, M. Giewat, C.E. Seidman, J.G. Seidman, and D.M. Warshaw Single-molecule mechanics of R403Q cardiac myosin isolated from the mouse model of familial hypertrophic cardiomyopathy Circ. Res. 86 2000 737 744
91. P.A. van der Zwaag, I.A. van Rijsingen, A. Asimaki, J.D. Jongbloed, D.J. van Veldhuisen, A.C. Wiesfeld, M.G. Cox, L.T. van Lochem, R.A. de Boer, and R.M. Hofstra Phospholamban R14del mutation in patients diagnosed with dilated cardiomyopathy or arrhythmogenic right ventricular cardiomyopathy: evidence supporting the concept of arrhythmogenic cardiomyopathy Eur. J. Heart Fail. 14 2012 1199 1207
92. S.J. van Dijk, D. Dooijes, C. dos Remedios, M. Michels, J.M. Lamers, S. Winegrad, S. Schlossarek, L. Carrier, F.J. ten Cate, G.J. Stienen, and J. van der Velden Cardiac myosin-binding protein C mutations and hypertrophic cardiomyopathy: haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction Circulation 119 2009 1473 1483
93. S.J. van Dijk, N.M. Boontje, M.W. Heymans, F.J. Ten Cate, M. Michels, C. Dos Remedios, D. Dooijes, M.A. van Slegtenhorst, J. van der Velden, and G.J. Stienen Preserved cross-bridge kinetics in human hypertrophic cardiomyopathy patients with MYBPC3 mutations Pflugers Archiv. Eur. J. Physiol. 466 2014 1619 1633
94. I.A. van Rijsingen, P.A. van der Zwaag, J.A. Groeneweg, E.A. Nannenberg, J.D. Jongbloed, A.H. Zwinderman, Y.M. Pinto, R.H. Dit Deprez, J.G. Post, and H.L. Tan Outcome in phospholamban R14del carriers: results of a large multicentre cohort study Circ Cardiovasc Genet 7 2014 455 465
95. M. Veltrop, and A. Aartsma-Rus Antisense-mediated exon skipping: taking advantage of a trick from Mother Nature to treat rare genetic diseases Exp. Cell Res. 325 2014 50 55
96. K.L. Vikstrom, S.M. Factor, and L.A. Leinwand Mice expressing mutant myosin heavy chains are a model for familial hypertrophic cardiomyopathy Mol. Med. 2 1996 556 567
97. R. Walsh, C. Rutland, R. Thomas, and S. Loughna Cardiomyopathy: a systematic review of disease-causing mutations in myosin heavy chain 7 and their phenotypic manifestations Cardiology 115 2010 49 60
98. A. Weith, S. Sadayappan, J. Gulick, M.J. Previs, P. Vanburen, J. Robbins, and D.M. Warshaw Unique single molecule binding of cardiac myosin binding protein-C to actin and phosphorylation-dependent inhibition of actomyosin motility requires 17 amino acids of the motif domain J. Mol. Cell. Cardiol. 52 2012 219 227
99. A.E. Weith, M.J. Previs, G.J. Hoeprich, S.B. Previs, J. Gulick, J. Robbins, and D.M. Warshaw The extent of cardiac myosin binding protein-C phosphorylation modulates actomyosin function in a graded manner J. Muscle Res. Cell Motil. 33 2012 449 459
100. M.W. Wessels, J.C. Herkert, I.M. Frohn-Mulder, M. Dalinghaus, A. van den Wijngaard, R.R. de Krijger, M. Michels, I.F. de Coo, Y.M. Hoedemaekers, and D. Dooijes Compound heterozygous or homozygous truncating MYBPC3 mutations cause lethal cardiomyopathy with features of noncompaction and septal defects Eur. J. Hum. Genet. 2014 10.1038/ejhg.2014.211
101. F.C. Wheeler, H. Tang, O.A. Marks, T.N. Hadnott, P.L. Chu, L. Mao, H.A. Rockman, and D.A. Marchuk Tnni3k modifies disease progression in murine models of cardiomyopathy PLoS Genet. 5 2009 e1000647
102. E.R. Witjas-Paalberends, C. Ferrara, B. Scellini, N. Piroddi, J. Montag, C. Tesi, G.J. Stienen, M. Michels, C.Y. Ho, and T. Kraft Faster cross-bridge detachment and increased tension cost in human hypertrophic cardiomyopathy with the R403Q MYH7 mutation J. Physiol. 592 2014 3257 3272
103. E.R. Witjas-Paalberends, A. Güçlü, T. Germans, P. Knaapen, H.J. Harms, A.M. Vermeer, I. Christiaans, A.A. Wilde, C. Dos Remedios, and A.A. Lammertsma Gene-specific increase in the energetic cost of contraction in hypertrophic cardiomyopathy caused by thick filament mutations Cardiovasc. Res. 103 2014 248 257
104. F. Xie, L. Ye, J.C. Chang, A.I. Beyer, J. Wang, M.O. Muench, and Y.W. Kan Seamless gene correction of β-thalassemia mutations in patient-specific iPSCs using CRISPR/Cas9 and piggyBac Genome Res. 24 2014 1526 1533