Rescue of familial cardiomyopathies by modifications at the level of sarcomere and Ca2+ fluxes

Journal of Molecular and Cellular Cardiology

Volumn 48, Issue 5, 2010, Pages 834-842

  Alves, Marco L ^a   Gaffin, Robert D ^a   Wolska, Beata M ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Ca2+ homeostasis; Dilated cardiomyopathy; Hypertrophic cardiomyopathy; Myofilament Ca2+ sensitivity; Phospholamban; SERCA2a

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALDOSTERONE ANTAGONIST; ANGIOTENSIN RECEPTOR ANTAGONIST; ATORVASTATIN; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCIUM ION; CANDESARTAN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DISOPYRAMIDE; DIURETIC AGENT; ENALAPRIL; LOSARTAN; PHOSPHOLAMBAN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2A; SIMVASTATIN; SPIRONOLACTONE; UNCLASSIFIED DRUG; VERAPAMIL;

CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CONGESTIVE CARDIOMYOPATHY; DIASTOLIC DYSFUNCTION; DISEASE MODEL; DISEASE SEVERITY; FAMILIAL HYPERTROPHIC CARDIOMYOPATHY; GENE MUTATION; GENETIC ANALYSIS; HEART DISEASE; HEART HYPERTROPHY; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HUMAN; MYOFILAMENT; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SARCOMERE; SARCOPLASMIC RETICULUM; SYSTOLIC DYSFUNCTION;

ANIMALS; CALCIUM; CARDIOMYOPATHY, DILATED; CARDIOMYOPATHY, HYPERTROPHIC, FAMILIAL; HUMANS; SARCOMERES; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

ANIMALIA;

EID: 77951621386     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2010.01.003     Document Type: Review

References (172)

1. Maron B.J., Towbin J.A., Thiene G., Antzelevitch C., Corrado D., Arnett D., 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 Genomics and Translational Biology Interdisciplinary Working Groups; and Council on Epidemiology and Prevention. Circulation 2006, 113:1807-1816.
2. Elliott P., Andersson B., Arbustini E., Bilinska Z., Cecchi F., Charron P., 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, 29:270-276.
3. Elliott P., McKenna W.J. Hypertrophic cardiomyopathy. Lancet 2004, 363:1881-1891.
4. Bos J.M., Towbin J.A., Ackerman M.J. Diagnostic, prognostic, and therapeutic implications of genetic testing for hypertrophic cardiomyopathy. J. Am. Coll. Cardiol. 2009, 54:201-211.
5. Hughes S.E. The pathology of hypertrophic cardiomyopathy. Histopathology 2004, 44:412-427.
6. Tardiff J.C. Sarcomeric proteins and familial hypertrophic cardiomyopathy: linking mutations in structural proteins to complex cardiovascular phenotypes. Heart Fail. Rev. 2005, 10:237-248.
7. Marian A.J. Modifier genes for hypertrophic cardiomyopathy. Curr. Opin. Cardiol. 2002, 17:242-252.
8. Arad M., Seidman J.G., Seidman C.E. Phenotypic diversity in hypertrophic cardiomyopathy. Hum. Mol. Genet. 2002, 11:2499-2506.
9. Maron B.J. Hypertrophic cardiomyopathy: a systematic review. JAMA 2002, 287:1308-1320.
10. Harrison D.C., Braunwald E., Glick G., Mason D.T., Chidsey C.A., Ross J. Effects of beta adrenergic blockade on the circulation with particular reference to observations in patients with hypertrophic subaortic stenosis. Circulation 1964, 29:84-98.
11. Rosing D.R., Kent K.M., Maron B.J., Epstein S.E. Verapamil therapy: a new approach to the pharmacologic treatment of hypertrophic cardiomyopathy. II. Effects on exercise capacity and symptomatic status. Circulation 1979, 60:1208-1213.
12. Sherrid M.V., Barac I., McKenna W.J., Elliott P.M., Dickie S., Chojnowska L., et al. Multicenter study of the efficacy and safety of disopyramide in obstructive hypertrophic cardiomyopathy. J. Am. Coll. Cardiol. 2005, 45:1251-1258.
13. Olivotto I., Ommen S.R., Maron M.S., Cecchi F., Maron B.J. Surgical myectomy versus alcohol septal ablation for obstructive hypertrophic cardiomyopathy. Will there ever be a randomized trial. J. Am. Coll. Cardiol. 2007, 50:831-834.
14. Ommen S.R., Maron B.J., Olivotto I., Maron M.S., Cecchi F., Betocchi S., et al. Long-term effects of surgical septal myectomy on survival in patients with obstructive hypertrophic cardiomyopathy. J. Am. Coll. Cardiol. 2005, 46:470-476.
15. Maron B.J., Nishimura R.A., McKenna W.J., Rakowski H., Josephson M.E., Kieval R.S. Assessment of permanent dual-chamber pacing as a treatment for drug-refractory symptomatic patients with obstructive hypertrophic cardiomyopathy. A randomized, double-blind, crossover study (M-PATHY). Circulation 1999, 99:2927-2933.
16. Luk A., Ahn E., Soor G.S., Butany J. Dilated cardiomyopathy: a review. J. Clin. Pathol. 2009, 62:219-225.
17. Burkett E.L., Hershberger R.E. Clinical and genetic issues in familial dilated cardiomyopathy. J. Am. Coll. Cardiol. 2005, 45:969-981.
18. Kamisago M., Sharma S.D., DePalma S.R., Solomon S., Sharma P., McDonough B., et al. Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N. Engl. J. Med. 2000, 343:1688-1696.
19. Olson T.M., Michels V.V., Thibodeau S.N., Tai Y.S., Keating M.T. Actin mutations in dilated cardiomyopathy, a heritable form of heart failure. Science 1998, 280:750-752.
20. Nicol R.L., Frey N., Olson E.N. From the sarcomere to the nucleus: role of genetics and signaling in structural heart disease. Annu. Rev. Genomics Hum. Genet. 2000, 1:179-223.
21. Ahmad F., Seidman J.G., Seidman C.E. The genetic basis for cardiac remodeling. Annu. Rev. Genomics Hum. Genet. 2005, 6:185-216.
22. Chang A.N., Potter J.D. Sarcomeric protein mutations in dilated cardiomyopathy. Heart Fail. Rev. 2005, 10:225-235.
23. Mestroni L., Rocco C., Gregori D., Sinagra G., Di L.A., Miocic S., et al. Familial dilated cardiomyopathy: evidence for genetic and phenotypic heterogeneity. Heart Muscle Disease Study Group. J. Am. Coll. Cardiol. 1999, 34:181-190.
24. Grogan M., Redfield M.M., Bailey K.R., Reeder G.S., Gersh B.J., Edwards W.D., et al. Long-term outcome of patients with biopsy-proved myocarditis: comparison with idiopathic dilated cardiomyopathy. J. Am. Coll. Cardiol. 1995, 26:80-84.
25. Richard P., Charron P., Carrier L., Ledeuil C., Cheav T., Pichereau C., et al. Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation 2003, 107:2227-2232.
26. Schmitt J.P., Debold E.P., Ahmad F., Armstrong A., Frederico A., Conner D.A., 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, 103:14525-14530.
27. Sata M., Ikebe M. Functional analysis of the mutations in the human cardiac β-myosin that are responsible for familial hypertrophic cardiomyopathy. Implication for the clinical outcome. J. Clin. Invest. 1996, 98:2866-2873.
28. Roopnarine O., Leinwand L.A. Functional analysis of myosin mutations that cause familial hypertrophic cardiomyopathy. Biophys. J. 1998, 75:3023-3030.
29. Cuda G., Fananapazir L., Epstein N.D., Sellers J.R. The in vitro motility activity of β-cardiac myosin depends on the nature of the β-myosin heavy chain gene mutation in hypertrophic cardiomyopathy. J. Muscle Res. Cell. Motil. 1997, 18:275-283.
30. Tyska M.J., Hayes E., Giewat M., Seidman C.E., Seidman J.G., Warshaw D.M. Single-molecule mechanics of R403Q cardiac myosin isolated from the mouse model of familial hypertrophic cardiomyopathy. Circ. Res. 2000, 86:737-744.
31. Keller D.I., Coirault C., Rau T., Cheav T., Weyand M., Amann K., et al. Human homozygous R403W mutant cardiac myosin presents disproportionate enhancement of mechanical and enzymatic properties. J. Mol. Cell. Cardiol. 2004, 36:355-362.
32. Palmiter K.A., Tyska M.J., Haeberle J.R., Alpert N.R., Fananapazir L., Warshaw D.M. R403Q and L908V mutant β-cardiac myosin from patients with familial hypertrophic cardiomyopathy exhibit enhanced mechanical performance at the single molecule level. J. Muscle Res. Cell. Motil. 2000, 21:609-620.
33. 403/+ mouse model of familial hypertrophic cardiomyopathy. Circ. Res. 1999, 84:475-483.
34. Debold E.P., Schmitt J.P., Patlak J.B., Beck S.E., Moore J.R., Seidman J.G., 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. 2007, 293:H284-H291.
35. Semsarian C., Ahmad I., Giewat M., Georgakopoulos D., Schmitt J.P., McConnell B.K., et al. The L-type calcium channel inhibitor diltiazem prevents cardiomyopathy in a mouse model. J. Clin. Invest. 2002, 109:1013-1020.
36. 403/+ mouse model of familial hypertrophic cardiomyopathy. J. Clin. Invest. 1998, 101:1775-1783.
37. Crilley J.G., Boehm E.A., Blair E., Rajagopalan B., Blamire A.M., Styles P., 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, 41:1776-1782.
38. Solaro R.J., Rarick H.M. Troponin and tropomyosin: proteins that switch on and tune in the activity of cardiac myofilaments. Circ. Res. 1998, 83:471-480.
39. 2+ regulation of thin filament motility. Biochem. Biophys. Res. Commun. 1997, 236:760-764.
40. Kimura A. Molecular etiology and pathogenesis of hereditary cardiomyopathy. Circ. J. 2008, 72(Suppl A):A38-A48.
41. Gomes A.V., Barnes J.A., Harada K., Potter J.D. Role of troponin T in disease. Mol. Cell. Biochem. 2004, 263:115-129.
42. Tardiff J.C., Hewett T.E., Palmer B.M., Olsson C., Factor S.M., Moore R.L., et al. Cardiac troponin T mutations result in allele-specific phenotypes in a mouse model for hypertrophic cardiomyopathy. J. Clin. Invest. 1999, 104:469-481.
43. Thierfelder L., Watkins H., Macrae C., Lamas R., Mckenna W., Vosberg H.P., et al. α-Tropomyosin and cardiac troponin T mutations cause familial hypertrophic cardiomyopathy: a disease of the sarcomere. Cell 1994, 77:701-712.
44. Kimura A., Harada H., Park J.E., Nishi H., Satoh M., Takahashi M., et al. Mutations in the cardiac troponin I gene associated with hypertrophic cardiomyopathy. Nat. Genet. 1997, 16:379-382.
45. Mogensen J., Perrot A., Andersen P.S., Havndrup O., Klausen I.C., Christiansen M., et al. Clinical and genetic characteristics of α cardiac actin gene mutations in hypertrophic cardiomyopathy. J. Med. Genet. 2004, 41:e10.
46. 2+ sensitization causes susceptibility to cardiac arrhythmia in mice. J. Clin. Invest. 2008, 118:3893-3903.
47. Hernandez O.M., Housmans P.R., Potter J.D. Invited review: pathophysiology of cardiac muscle contraction and relaxation as a result of alterations in thin filament regulation. J. Appl. Physiol. 2001, 90:1125-1136.
48. Muthuchamy M., Pieples K., Rethinasamy P., Hoit B., Grupp I.L., Boivin G.P., et al. Mouse model of a familial hypertrophic cardiomyopathy mutation in α-tropomyosin manifests cardiac dysfunction. Circ. Res. 1999, 85:47-56.
49. Prabhakar R., Boivin G.P., Grupp I.L., Hoit B., Arteaga G., Solaro R.J., et al. A familial hypertrophic cardiomyopathy α-tropomyosin mutation causes severe cardiac hypertrophy and death in mice. J. Mol. Cell. Cardiol. 2001, 33:1815-1828.
50. Wolska B.M., Wieczorek D.F. The role of tropomyosin in the regulation of myocardial contraction and relaxation. Pflugers Arch. 2003, 446:1-8.
51. Nakaura H., Morimoto S., Yanaga F., Nakata M., Nishi H., Imaizumi T., et al. Functional changes in troponin T by a splice donor site mutation that causes hypertrophic cardiomyopathy. Am. J. Physiol. 1999, 277:C225-C232.
52. Szczesna D., Zhang R., Zhao J., Jones M., Guzman G., Potter J.D. Altered regulation of cardiac muscle contraction by troponin T mutations that cause familial hypertrophic cardiomyopathy. J. Biol. Chem. 2000, 275:624-630.
53. 2+-sensitizing effects of the mutations at Ile-79 and Arg-92 of troponin T in hypertrophic cardiomyopathy. Am. J. Physiol. 1998, 275:C200-C207.
54. 2+ activation of myofilaments from transgenic mouse hearts expressing R92Q mutant cardiac troponin T. Am. J. Physiol. 2001, 280:H705-H713.
55. Nakaura H., Yanaga F., Ohtsuki I., Morimoto S. Effects of missense mutations Phe110Ile and Glu244Asp in human cardiac troponin T on force generation in skinned cardiac muscle fibers. J. Biochem. (Tokyo) 1999, 126:457-460.
56. Elliott K., Watkins H., Redwood C.S. Altered regulatory properties of human cardiac troponin I mutants that cause hypertrophic cardiomyopathy. J. Biol. Chem. 2000, 275:22069-22074.
57. James J., Zhang Y., Osinska H., Sanbe A., Klevitsky R., Hewett T.E., et al. Transgenic modeling of a cardiac troponin I mutation linked to familial hypertrophic cardiomyopathy. Circ. Res. 2000, 87:805-811.
58. Rajan S., Ahmed R.P., Jagatheesan G., Petrashevskaya N., Boivin G.P., Urboniene D., et al. Dilated cardiomyopathy mutant tropomyosin mice develop cardiac dysfunction with significantly decreased fractional shortening and myofilament calcium sensitivity. Circ. Res. 2007, 101:205-214.
59. 2+-desensitizing effect of a deletion mutation Delta K210 in cardiac troponin T that causes familial dilated cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:913-918.
60. 2+ desensitization. J. Mol. Cell. Cardiol. 2003, 35:1421-1427.
61. Chang A.N., Harada K., Ackerman M.J., Potter J.D. Functional consequences of hypertrophic and dilated cardiomyopathy-causing mutations in alpha-tropomyosin. J. Biol. Chem. 2005, 280:34343-34349.
62. Michele D.E., Gomez C.A., Hong K.E., Westfall M.V., Metzger J.M. Cardiac dysfunction in hypertrophic cardiomyopathy mutant tropomyosin mice is transgene-dependent, hypertrophy-independent, and improved by β-blockade. Circ. Res. 2002, 91:255-262.
63. 2+ sensitivity and tropomyosin N-domain flexibility. J. Biol. Chem. 2003, 278:41742-41748.
64. Robinson P., Griffiths P.J., Watkins H., Redwood C.S. Dilated and hypertrophic cardiomyopathy mutations in troponin and alpha-tropomyosin have opposing effects on the calcium affinity of cardiac thin filaments. Circ. Res. 2007, 101:1266-1273.
65. Kota B., Prasad A.S., Economides C., Singh B.N. Levosimendan and calcium sensitization of the contractile proteins in cardiac muscle: impact on heart failure. J. Cardiovasc. Pharmacol. Ther. 2008, 13:269-278.
66. Pollesello P., Papp Z. The cardioprotective effects of levosimendan: preclinical and clinical evidence. J. Cardiovasc. Pharmacol. 2007, 50:257-263.
67. Parissis J.T., Rafouli-Stergiou P., Paraskevaidis I., Mebazaa A. Levosimendan: from basic science to clinical practice. Heart Fail. Rev. 2008.
68. Jagatheesan G., Rajan S., Petrashevskaya N., Schwartz A., Boivin G., Vahebi S., et al. Functional importance of the carboxyl-terminal region of striated muscle tropomyosin. J. Biol. Chem. 2003, 278:23204-23211.
69. Jagatheesan G., Rajan S., Petrashevskaya N., Schwartz A., Boivin G., Arteaga G.M., et al. Rescue of tropomyosin-induced familial hypertrophic cardiomyopathy mice by transgenesis. Am. J. Physiol. 2007, 293:H949-H958.
70. Solaro R.J., Rosevear P., Kobayashi T. The unique functions of cardiac troponin I in the control of cardiac muscle contraction and relaxation. Biochem. Biophys. Res. Commun. 2008, 369:82-87.
71. Solaro R.J. Multiplex kinase signaling modifies cardiac function at the level of sarcomeric proteins. J. Biol. Chem. 2008, 283:26829-26833.
72. Sheehan K.A., Ke Y., Solaro R.J. P21 activated kinase-1 and its role in integrated regulation of cardiac contractility. Am. J. Physiol. 2007, ;293:R963-73.
73. Haworth R.S., Cuello F., Herron T.J., Franzen G., Kentish J.C., Gautel M., et al. Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function. Circ. Res. 2004, 95:1091-1099.
74. 2+ sensitivity in ventricular myocytes. Circ. Res. 2007, 100:864-873.
75. Strang K.T., Sweitzer N.K., Greaser M.L., Moss R.L. β-Adrenergic receptor stimulation increases unloaded shortening velocity of skinned single ventricular myocytes from rats. Circ. Res. 1994, 74:542-549.
76. Zhang R., Zhao J., Mandveno A., Potter J.D. Cardiac troponin, I phosphorylation increases the rate of cardiac muscle relaxation. Circ. Res. 1995, 76:1028-1035.
77. 2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovasc. Res. 2003, 57:37-47.
78. Messer A.E., Jacques A.M., Marston S.B. Troponin phosphorylation and regulatory function in human heart muscle: dephosphorylation of Ser23/24 on troponin I could account for the contractile defect in end-stage heart failure. J. Mol. Cell. Cardiol. 2007, 42:247-259.
79. de Waard M.C., Van D., Bito V., Ozdemir S., Biesmans L., Boontje N.M., et al. Early exercise training normalizes myofilament function and attenuates left ventricular pump dysfunction in mice with a large myocardial infarction. Circ. Res. 2007, 100:1079-1088.
80. 2+ as a therapeutic target for familial hypertrophic cardiomyopathy. J. Mol.Cell. Cardiol. 2009, 46(5):S36.
81. Haikala H., Kaivola J., Nissinen E., Wall P., Levijoki J., Linden I.B. Cardiac troponin C as a target protein for a novel calcium sensitizing drug, levosimendan. J. Mol. Cell. Cardiol. 1995, 27:1859-1866.
82. + channel in rat arterial myocytes. Eur. J. Pharmacol. 1997, 333:249-259.
83. + channel in rat ventricular cells. J. Pharmacol. Exp. Ther. 1997, 283:375-383.
84. Pagel P.S., Harkin C.P., Hettrick D.A., Warltier D.C. Levosimendan (OR-1259), a myofilament calcium sensitizer, enhances myocardial contractility but does not alter isovolumic relaxation in conscious and anesthetized dogs. Anesthesiology 1994, 81:974-987.
85. Du C.K., Morimoto S., Nishii K., Minakami R., Ohta M., Tadano N., et al. Knock-in mouse model of dilated cardiomyopathy caused by troponin mutation. Circ. Res. 2007, 101:185-194.
86. Bers D.M. Excitation-Contraction Coupling and Cardiac Contractile Force 2001, Kluwer Academic Publishers.
87. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
88. 2+ mediated through α- and β-adrenoceptors. Circ. Res. 1988, 62:247-265.
89. Spurgeon H.A., DuBell W.H., Stern M.D., Sollott S.J., Ziman B.D., Silverman H.S., et al. Cytosolic calcium and myofilaments in single rat cardiac myocytes achieve a dynamic equilibrium during twitch relaxation. J. Physiol. 1992, 447:83-102.
90. Wolska B.M., Kitada Y., Palmiter K.A., Westfall M.V., Johnson M.D., Solaro R.J. CGP-48506 increases contractility of ventricular myocytes and myofilaments by effects on actin-myosin reaction. Am. J. Physiol. 1996, 270:H24-H32.
91. Janssen P.M., Stull L.B., Marban E. Myofilament properties comprise the rate-limiting step for cardiac relaxation at body temperature in the rat. Am. J. Physiol. 2002, 282:H499-H507.
92. Hasenfuss G., Pieske B. Calcium cycling in congestive heart failure. J. Mol. Cell. Cardiol. 2002, 34:951-969.
93. 2+. Am. J. Physiol. 1996, 271:C391-C397.
94. Wolska B.M., Arteaga G.M., Pena J.R., Nowak G., Phillips R.M., Sahai S., et al. Expression of slow skeletal troponin I in hearts of phospholamban knockout mice alters the relaxant effect of β-adrenergic stimulation. Circ. Res. 2002, 90:882-888.
95. Li L., Desantiago J., Chu G., Kranias E.G., Bers D.M. Phosphorylation of phospholamban and troponin I in β-adrenergic-induced acceleration of cardiac relaxation. Am. J. Physiol. 2000, 278:H769-H779.
96. Pena J.R., Wolska B.M. Troponin, I phosphorylation plays an important role in the relaxant effect of β-adrenergic stimulation in mouse hearts. Cardiovasc. Res. 2004, 61:756-763.
97. 2+-ATPase increases cardiac contractility in transgenic mouse hearts. Circ. Res. 1998, 83:1205-1214.
98. Brittsan A.G., Kranias E.G. Phospholamban and cardiac contractile function. J. Mol. Cell. Cardiol. 2000, 32:2131-2139.
99. Koss K.L., Grupp I.L., Kranias E.G. The relative phospholamban and SERCA2 ratio: a critical determinant of myocardial contractility. Basic Res. Cardiol. 1997, 92(Suppl. 1):17-24.
100. Meyer M., Bluhm W.F., He H., Post S.R., Giordano F.J., Lew W.Y., et al. Phospholamban-to-SERCA2 ratio controls the force-frequency relationship. Am. J. Physiol. 1999, 276:H779-H785.
101. 2+-ATPase activity and phosphorylation level of phospholamban. Am. J. Physiol. 1999, 277:H474-H480.
102. 2+-exchanger protein levels and diastolic function of failing human myocardium. Circulation 1999, 99:641-648.
103. Arai M., Matsui H., Periasamy M. Sarcoplasmic reticulum gene expression in cardiac hypertrophy and heart failure. Circ. Res. 1994, 74:555-564.
104. Miyamoto M.I., del Monte F., Schmidt U., DiSalvo T.S., Kang Z.B., Matsui T., et al. Adenoviral gene transfer of SERCA2a improves left-ventricular function in aortic-banded rats in transition to heart failure. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:793-798.
105. 2+-ATPase in a rat model of heart failure. Circulation 2001, 104:1424-1429.
106. Federica D.M., Harding S.E., Schmidt U., Matsui T., Kang Z.B., Dec G.W., et al. Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation 1999, 100:2308-2311.
107. 2+ ATPase modifies the transition from hypertrophy to early heart failure. Circ. Res. 2001, 89:422-429.
108. Pena J.R., Goldspink P.H., Prabhakar R., del Monte F., Hajjar R.J., Wieczorek D.F., et al. Neonatal gene transfer of SERCA2a improves the response to β-adrenergic stimulation in a FHC α-tropomyosin (Glu180Gly) mouse model. FASEB J. 2004, 18:A1216-A1217.
109. Pena J.R., Szkudlarek A.C., Goldspink P.H., Heinrich L.S., Prabhakar R., Monte F., et al. Neonatal gene transfer of SERCA2a alters hypertrophic gene expression and improves the response to β-adrenergic stimulation in a FHC α-tropomyosin (Glu180Gly) mouse model. Circulation 2006, 114:166.
110. Suarez J., Belke D.D., Gloss B., Dieterle T., McDonough P.M., Kim Y.K., et al. In vivo adenoviral transfer of sorcin reverses cardiac contractile abnormalities of diabetic cardiomyopathy. Am. J. Physiol. 2004, 286:H68-H75.
111. Huq F., Lebeche D., Iyer V., Liao R., Hajjar R.J. Gene transfer of parvalbumin improves diastolic dysfunction in senescent myocytes. Circulation 2004, 109:2780-2785.
112. Coutu P., Bennett C.N., Favre E.G., Day S.M., Metzger J.M. Parvalbumin corrects slowed relaxation in adult cardiac myocytes expressing hypertrophic cardiomyopathy-linked α-tropomyosin mutations. Circ. Res. 2004, 94:1235-1241.
113. Arber S., Hunter J.J., Ross J., Hongo M., Sansig G., Borg J., et al. MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 1997, 88:393-403.
114. Minamisawa S., Hoshijima M., Chu G., Ward C.A., Frank K., Gu Y., et al. Chronic phospholamban-sarcoplasmic reticulum calcium ATPase interaction is the critical calcium cycling defect in dilated cardiomyopathy. Cell 1999, 99:313-322.
115. Sato Y., Kiriazis H., Yatani A., Schmidt A.G., Hahn H., Ferguson D.G., et al. Rescue of contractile parameters and myocyte hypertrophy in calsequestrin overexpressing myocardium by phospholamban ablation. J. Biol. Chem. 2001, 276:9392-9399.
116. Sato Y., Ferguson D.G., Sako H., Dorn G.W., Kadambi V.J., Yatani A., et al. Cardiac-specific overexpression of mouse cardiac calsequestrin is associated with depressed cardiovascular function and hypertrophy in transgenic mice. J. Biol. Chem. 1998, 273:28470-28477.
117. Delling U., Sussman M.A., Molkentin J.D. Re-evaluating sarcoplasmic reticulum function in heart failure. Nat. Med. 2000, 6:942-943.
118. del Monte F., Harding S.E., Dec G.W., Gwathmey J.K., Hajjar R.J. Targeting phospholamban by gene transfer in human heart failure. Circulation 2002, 105:904-907.
119. Hoshijima M., Ikeda Y., Iwanaga Y., Minamisawa S., Date M.O., Gu Y., et al. Chronic suppression of heart-failure progression by a pseudophosphorylated mutant of phospholamban via in vivo cardiac rAAV gene delivery. Nat. Med. 2002, 8:864-871.
120. Song Q., Schmidt A.G., Hahn H.S., Carr A.N., Frank B., Pater L., et al. Rescue of cardiomyocyte dysfunction by phospholamban ablation does not prevent ventricular failure in genetic hypertrophy. J. Clin. Invest. 2003, 111:859-867.
121. Freeman K., Lerman I., Kranias E.G., Bohlmeyer T., Bristow M.R., Lefkowitz R.J., et al. Alterations in cardiac adrenergic signaling and calcium cycling differentially affect the progression of cardiomyopathy. J. Clin. Invest. 2001, 107:967-974.
122. Pena J.R., Goldspink P.H., Heinrich L.S., Kranias E.G., Wieczorek D.F., Wolska B.M. Phospholamban knockout alters hypertrophic gene expression and improves cardiac function in a HCM α-tropomyosin (Glu180Gly) mouse. Circ. Res. 2008, 103:E40.
123. Westermann D., Knollmann B.C., Steendijk P., Rutschow S., Riad A., Pauschinger M., et al. Diltiazem treatment prevents diastolic heart failure in mice with familial hypertrophic cardiomyopathy. Eur. J. Heart Fail. 2006, 8:115-121.
124. Marian A.J., Yu Q.T., Workman R., Greve G., Roberts R. Angiotensin-converting enzyme polymorphism in hypertrophic cardiomyopathy and sudden cardiac death. Lancet 1993, 342:1085-1086.
125. Tesson F., Dufour C., Moolman J.C., Carrier L., al-Mahdawi S., Chojnowska L., et al. The influence of the angiotensin I converting enzyme genotype in familial hypertrophic cardiomyopathy varies with the disease gene mutation. J. Mol. Cell. Cardiol. 1997, 29:831-838.
126. Candy G.P., Skudicky D., Mueller U.K., Woodiwiss A.J., Sliwa K., Luker F., et al. Association of left ventricular systolic performance and cavity size with angiotensin-converting enzyme genotype in idiopathic dilated cardiomyopathy. Am. J. Cardiol. 1999, 83:740-744.
127. Tsoutsman T., Lam L., Semsarian C. Genes, calcium and modifying factors in hypertrophic cardiomyopathy. Clin. Exp. Pharmacol. Physiol. 2006, 33:139-145.
128. Brugada R., Kelsey W., Lechin M., Zhao G., Yu Q.T., Zoghbi W., et al. Role of candidate modifier genes on the phenotypic expression of hypertrophy in patients with hypertrophic cardiomyopathy. J. Investig. Med. 1997, 45:542-551.
129. Doolan G., Nguyen L., Chung J., Ingles J., Semsarian C. Progression of left ventricular hypertrophy and the angiotensin-converting enzyme gene polymorphism in hypertrophic cardiomyopathy. Int. J. Cardiol. 2004, 96:157-163.
130. Deinum J., van Gool J.M., Kofflard M.J., Ten Cate F.J., Danser A.H., Angiotensin I.I. type 2 receptors and cardiac hypertrophy in women with hypertrophic cardiomyopathy. Hypertension 2001, 38:1278-1281.
131. Forleo C., Sorrentino S., Guida P., Romito R., De T.E., Iacoviello M., et al. Beta1- and beta2-adrenergic receptor polymorphisms affect susceptibility to idiopathic dilated cardiomyopathy. J. Cardiovasc. Med. (Hagerstown) 2007, 8:589-595.
132. Lechin M., Quinones M.A., Omran A., Hill R., Yu Q.T., Rakowski H., et al. Angiotensin-I converting enzyme genotypes and left ventricular hypertrophy in patients with hypertrophic cardiomyopathy. Circulation 1995, 92:1808-1812.
133. Osterop A.P., Kofflard M.J., Sandkuijl L.A., Ten Cate F.J., Krams R., Schalekamp M.A., et al. AT1 receptor A/C1166 polymorphism contributes to cardiac hypertrophy in subjects with hypertrophic cardiomyopathy. Hypertension 1998, 32:825-830.
134. Patel R., Lim D.S., Reddy D., Nagueh S.F., Lutucuta S., Sole M.J., et al. Variants of trophic factors and expression of cardiac hypertrophy in patients with hypertrophic cardiomyopathy. J. Mol. Cell. Cardiol. 2000, 32:2369-2377.
135. Ishanov A., Okamoto H., Yoneya K., Watanabe M., Nakagawa I., Machida M., et al. Angiotensinogen gene polymorphism in Japanese patients with hypertrophic cardiomyopathy. Am. Heart J. 1997, 133:184-189.
136. 2-adrenergic receptor polymorphism adversely affects the outcome of congestive heart failure. J. Clin. Invest. 1998, 102:1534-1539.
137. 2-Adrenergic receptor polymorphisms and sudden cardiac death: a signal to follow. Circulation 2006, 113:1818-1820.
138. 2 adrenergic receptors in Polish patients with idiopathic dilated cardiomyopathy. Kardiol. Pol. 2009, 67:235-241.
139. 2c-adrenoreceptor variants as predictors of clinical aspects of dilated cardiomyopathy in people of African ancestry. Cardiovasc. J. Afr. 2008, 19:188-193.
140. Liggett S.B., Cresci S., Kelly R.J., Syed F.M., Matkovich S.J., Hahn H.S., et al. A GRK5 polymorphism that inhibits β-adrenergic receptor signaling is protective in heart failure. Nat. Med. 2008, 14:510-517.
141. 2-adrenoreceptor gene variants on cardiac cavity size and systolic function in idiopathic dilated cardiomyopathy. Pharmacogenomics J. 2007, 7:339-345.
142. 1-adrenergic receptor gene polymorphisms in Mexican patients with idiopathic dilated cardiomyopathy. Exp. Mol. Pathol. 2006, 80:279-282.
143. Forleo C., Resta N., Sorrentino S., Guida P., Manghisi A., De L., et al. Association of β-adrenergic receptor polymorphisms and progression to heart failure in patients with idiopathic dilated cardiomyopathy. Am. J. Med. 2004, 117:451-458.
144. Herrmann S., Schmidt-Petersen K., Pfeifer J., Perrot A., Bit-Avragim N., Eichhorn C., et al. A polymorphism in the endothelin-A receptor gene predicts survival in patients with idiopathic dilated cardiomyopathy. Eur. Heart J. 2001, 22:1948-1953.
145. 1-adrenoceptor gene and evaluation of its role in idiopathic dilated cardiomyopathy. CARDIGENE Group. J. Mol. Cell. Cardiol. 1999, 31:1025-1032.
146. Loh E., Rebbeck T.R., Mahoney P.D., Denofrio D., Swain J.L., Holmes E.W. Common variant in AMPD1 gene predicts improved clinical outcome in patients with heart failure. Circulation 1999, 99:1422-1425.
147. Yoneya K., Okamoto H., Machida M., Onozuka H., Noguchi M., Mikami T., et al. Angiotensin-converting enzyme gene polymorphism in Japanese patients with hypertrophic cardiomyopathy. Am. Heart J. 1995, 130:1089-1093.
148. Perkins M.J., Van Driest S.L., Ellsworth E.G., Will M.L., Gersh B.J., Ommen S.R., et al. Gene-specific modifying effects of pro-LVH polymorphisms involving the renin-angiotensin-aldosterone system among 389 unrelated patients with hypertrophic cardiomyopathy. Eur. Heart J. 2005, 26:2457-2462.
149. Pitt B., Williams G., Remme W., Martinez F., Lopez-Sendon J., Zannad F., et al. The EPHESUS trial: eplerenone in patients with heart failure due to systolic dysfunction complicating acute myocardial infarction.
150. Pitt B., Zannad F., Remme W.J., Cody R., Castaigne A., Perez A., et al. The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N. Engl. J. Med. 1999, 341:709-717.
151. Blauwet L.A., Ackerman M.J., Edwards W.D., Riehle D.L., Ommen S.R. Myocardial fibrosis in patients with symptomatic obstructive hypertrophic cardiomyopathy: correlation with echocardiographic measurements, sarcomeric genotypes, and pro-left ventricular hypertrophy polymorphisms involving the renin-angiotensin-aldosterone system. Cardiovasc. Pathol. 2009, 18:262-268.
152. Chai W., Hoedemaekers Y., van Schaik R.H., van F.M., Garrelds I.M., Saris J.J., et al. Cardiac aldosterone in subjects with hypertrophic cardiomyopathy. J. Renin. Angiotensin Aldosterone Syst. 2006, 7:225-230.
153. Tsybouleva N., Zhang L., Chen S., Patel R., Lutucuta S., Nemoto S., et al. Aldosterone, through novel signaling proteins, is a fundamental molecular bridge between the genetic defect and the cardiac phenotype of hypertrophic cardiomyopathy. Circulation 2004, 109:1284-1291.
154. Rao L., Zhou B., Wang B., Wang Y.P., Li Y.B., Zhang L. [Study on association between aldosterone synthase gene polymorphism and the left ventricular structure and function of patients with dilated cardiomyopathy in China]. Sichuan Daxue Xuebao Yixue Ban. 2004, 35:809-811.
155. Yamada Y., Ichihara S., Fujimura T., Yokota M. Lack of association of polymorphisms of the angiotensin converting enzyme and angiotensinogen genes with nonfamilial hypertrophic or dilated cardiomyopathy. Am. J. Hypertens. 1997, 10:921-928.
156. Buck P.C., Fernandes F., Arteaga E., Matsumoto A.Y., Araujo A.Q., Oliveira E.M., et al. Association of angiotensin-converting enzyme activity and polymorphism with echocardiographic measures in familial and nonfamilial hypertrophic cardiomyopathy. Braz. J. Med. Biol. Res. 2009, 42:717-721.
157. Goineau S., Pape D., Guillo P., Ramee M.P., Bellissant E. Combined effects of enalapril and spironolactone in hamsters with dilated cardiomyopathy. J. Cardiovasc. Pharmacol. 2003, 41:49-59.
158. Laviolle B., Pape D., Turlin B., Bellissant E. Direct effects of 3 combinations of enalapril, metoprolol, and spironolactone on cardiac remodeling in dilated cardiomyopathic hamsters. J. Card. Fail. 2006, 12:752-758.
159. Lim D.S., Lutucuta S., Bachireddy P., Youker K., Evans A., Entman M., et al. Angiotensin II blockade reverses myocardial fibrosis in a transgenic mouse model of human hypertrophic cardiomyopathy. Circulation 2001, 103:789-791.
160. Penicka M., Gregor P., Kerekes R., Marek D., Curila K., Krupicka J. The effects of candesartan on left ventricular hypertrophy and function in nonobstructive hypertrophic cardiomyopathy: a pilot, randomized study. J. Mol. Diagn. 2009, 11:35-41.
161. Araujo A.Q., Arteaga E., Ianni B.M., Buck P.C., Rabello R., Mady C. Effect of Losartan on left ventricular diastolic function in patients with nonobstructive hypertrophic cardiomyopathy. Am. J. Cardiol. 2005, 96:1563-1567.
162. Patel R., Nagueh S.F., Tsybouleva N., Abdellatif M., Lutucuta S., Kopelen H.A., et al. Simvastatin induces regression of cardiac hypertrophy and fibrosis and improves cardiac function in a transgenic rabbit model of human hypertrophic cardiomyopathy. Circulation 2001, 104:317-324.
163. Senthil V., Chen S.N., Tsybouleva N., Halder T., Nagueh S.F., Willerson J.T., et al. Prevention of cardiac hypertrophy by atorvastatin in a transgenic rabbit model of human hypertrophic cardiomyopathy. Circ. Res. 2005, 97:285-292.
164. Marian A.J., Senthil V., Chen S.N., Lombardi R. Antifibrotic effects of antioxidant N-acetylcysteine in a mouse model of human hypertrophic cardiomyopathy mutation. J. Am. Coll. Cardiol. 2006, 47:827-834.
165. Wang J., Xu S.J., Zhou H., Wang L.J., Hu B., Fang F., et al. A novel mutation of the beta myosin heavy chain gene responsible for familial hypertrophic cardiomyopathy. Clin. Cardiol. 2009, 32:E16-E21.
166. Landstrom A.P., Parvatiyar M.S., Pinto J.R., Marquardt M.L., Bos J.M., Tester D.J., et al. Molecular and functional characterization of novel hypertrophic cardiomyopathy susceptibility mutations in TNNC1-encoded troponin C. J. Mol. Cell. Cardiol. 2008, 45:281-288.
167. Arimura T., Matsumoto Y., Okazaki O., Hayashi T., Takahashi M., Inagaki N., et al. Structural analysis of obscurin gene in hypertrophic cardiomyopathy. Biochem. Biophys. Res. Commun. 2007, 362:281-287.
168. Duboscq-Bidot L., Xu P., Charron P., Neyroud N., Dilanian G., Millaire A., et al. Mutations in the Z-band protein myopalladin gene and idiopathic dilated cardiomyopathy. Cardiovasc. Res. 2008, 77:118-125.
169. Arimura T., Bos J.M., Sato A., Kubo T., Okamoto H., Nishi H., et al. Cardiac ankyrin repeat protein gene (ANKRD1) mutations in hypertrophic cardiomyopathy. J. Am. Coll. Cardiol. 2009, 54:334-342.
170. Duboscq-Bidot L., Charron P., Ruppert V., Fauchier L., Richter A., Tavazzi L., et al. Mutations in the ANKRD1 gene encoding CARP are responsible for human dilated cardiomyopathy. Eur. Heart J. 2009, 30:2128-2136.
171. Osio A., Tan L., Chen S.N., Lombardi R., Nagueh S.F., Shete S., et al. Myozenin 2 is a novel gene for human hypertrophic cardiomyopathy. Circ. Res. 2007, 100:766-768.
172. Landstrom A.P., Weisleder N., Batalden K.B., Bos J.M., Tester D.J., Ommen S.R., et al. Mutations in JPH2-encoded junctophilin-2 associated with hypertrophic cardiomyopathy in humans. J. Mol. Cell. Cardiol. 2007, 42:1026-1035.