Myofilament dysfunction as an emerging mechanism of volume overload heart failure

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 6, 2014, Pages 1065-1077

  Wilson, Kristin ^a,b   Lucchesi, Pamela A ^a,b,c  

^a NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

Excitation contraction coupling; Extracellular matrix remodeling; Heart failure; Myofilament dysfunction; Volume overload

Indexed keywords

NEUROHORMONE;

AORTOCAVAL FISTULA; CALCIUM HOMEOSTASIS; CONGESTIVE CARDIOMYOPATHY; EXCITATION CONTRACTION COUPLING; EXTRACELLULAR MATRIX; GAP JUNCTION; HEART FAILURE; HEART LEFT VENTRICLE FAILURE; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HEART RIGHT VENTRICLE FUNCTION; HEART VALVE REGURGITATION; HUMAN; MAST CELL; MECHANICAL STRESS; MISSENSE MUTATION; MUSCLE CONTRACTION; MUSCLE RIGIDITY; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; HEMODYNAMICS; METABOLISM; MUSCLE FIBRIL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; EXCITATION CONTRACTION COUPLING; HEART FAILURE; HEMODYNAMICS; HUMANS; MYOFIBRILS;

EID: 84901953144     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1455-9     Document Type: Review

References (105)

1. Abassi Z, Goltsman I, Karram T, Winaver J, Hoffman A (2011) Aortocaval fistula in rat: a unique model of volume-overload congestive heart failure and cardiac hypertrophy. J Biomed Biotechnol 2011,729497:13. doi:10.1155/2011/729497
2. Al-Jassar C, Bikker H, Overduin M, Chidgey M (2013)Mechanistic basis of desmosome-targeted diseases. J Mol Biol 425(21):4006-4022. doi:10.1016/j.jmb. 2013.07.035
3. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4(7):517-529. doi:10.1038/nrm1155 (Pubitemid 36773404)
4. Bezold KL, Shaffer JF, Khosa JK, Hoye ER, Harris SP (2013) A gain-of-function mutation in the M-domain of cardiac myosin-binding protein-C increases binding to actin. J Biol Chem 288(30):21496-21505. doi:10.1074/jbc.M113.474346
5. Biesiadecki BJ, Kobayashi T, Walker JS, Solaro RJ, de Tombe PP (2007) The troponin C G159D mutation blunts myofilament desensitization induced by troponin I Ser23/24 phosphorylation. Circ Res 100(10):1486-1493. doi:10.1161/01.RES.0000267744.92677.7f (Pubitemid 46834761)
6. Boron WF, Boulpaep EL (2008) Medical physiology, 2nd edn. Elsevier Health Sciences, Philadelphia
7. Brown L (2005) Cardiac extracellular matrix: a dynamic entity. Am J Physiol Heart Circ Physiol 289(3):H973-H974. doi:10.1152/ajpheart.00443.2005
8. Brown LA, Nunez DJ, Brookes CI, Wilkins MR (1995) Selective increase in endothelin-1 and endothelin A receptor subtype in the hypertrophied myocardium of the aorto-venacaval fistula rat. Cardiovasc Res 29(6):768-774
9. Butt RP, Bishop JE (1997) Mechanical load enhances the stimulatory effect of serumgrowth factors on cardiac fibroblast procollagen synthesis. J Mol Cell Cardiol 29(4):1141-1151. doi:10.1006/jmcc.1996.0347 (Pubitemid 27211895)
10. Carabello BA (2012) Volume overload. Heart Fail Clin 8(1):33-42. doi:10.1016/j.hfc.2011.08.013
11. Carver W, Nagpal ML, Nachtigal M, Borg TK, Terracio L (1991) Collagen expression in mechanically stimulated cardiac fibroblasts. Circ Res 69(1):116-122
12. Chang AN, Harada K, Ackerman MJ, Potter JD (2005) Functional consequences of hypertrophic and dilated cardiomyopathy-causing mutations in alpha-tropomyosin. J Biol Chem 280(40):34343-34349. doi:10.1074/jbc.M505014200 (Pubitemid 41443160)
13. Chang AN, Potter JD (2005) Sarcomeric protein mutations in dilated cardiomyopathy. Heart Fail Rev 10(3):225-235. doi:10.1007/s10741-005-5252-6 (Pubitemid 43115832)
14. Chen PP, Patel JR, Powers PA, Fitzsimons DP, Moss RL (2012) Dissociation of structural and functional phenotypes in cardiac myosin-binding protein C conditional knockout mice. Circulation 126(10):1194-1205. doi:10.1161/ circulationaha.111.089219
15. Chen YW, Pat B, Gladden JD, Zheng J, Powell P, Wei CC, Cui X, Husain A, Dell'Italia LJ (2011) Dynamic molecular and histopathological changes in the extracellular matrix and inflammation in the transition to heart failure in isolated volume overload. Am J Physiol Heart Circ Physiol 300(6):H2251-H2260. doi:10.1152/ajpheart.01104.2010
16. Chopra A, Patel A, Shieh AC, Janmey PA, Kresh JY (2012) alpha-Catenin localization and sarcomere self-organization on N-cadherin adhesive patterns aremyocyte contractility driven. PLoS One 7(10):e47592. doi:10.1371/journal. pone.0047592
17. Clemen CS, Herrmann H, Strelkov SV, Schroder R (2013) Desminopathies: pathology and mechanisms. Acta Neurophatol 125(1):47-75. doi:10.1007/s00401-012- 1057-6
18. Colson BA, Patel JR, Chen PP, Bekyarova T, Abdalla MI, Tong CW, Fitzsimons DP, Irving TC, Moss RL (2012) Myosin binding protein-C phosphorylation is the principal mediator of protein kinase A effects on thick filament structure in myocardium. J Mol Cell Cardiol 53(5):609-616. doi:10.1016/j.yjmcc.2012.07.012
19. Coulton AT, Stelzer JE (2012) Cardiac myosin binding protein C and its phosphorylation regulate multiple steps in the cross-bridge cycle of muscle contraction. Biochemistry 51(15):3292-3301. doi:10.1021/bi300085x
20. De Mello WC, Danser AH (2000) Angiotensin II and the heart: on the intracrine renin-angiotensin system. Hypertension 35(6):1183-1188 (Pubitemid 30413647)
21. Du CK, Morimoto S, Nishii K, Minakami R, Ohta M, Tadano N, Lu QW, Wang YY, Zhan DY, Mochizuki M, Kita S, Miwa Y, Takahashi-Yanaga F, Iwamoto T, Ohtsuki I, Sasaguri T (2007) Knock-in mouse model of dilated cardiomyopathy caused by troponin mutation. Circ Res 101(2):185-194. doi:10.1161/circresaha.106.146670 (Pubitemid 47196586)
22. Duffy HS (2012) The molecular mechanisms of gap junction remodeling. Heart Rhythm 9(8):1331-1334. doi:10.1016/j.hrthm.2011.11.048
23. Flaim SF, Minteer WJ, Nellis SH, Clark DP (1979) Chronic arteriovenous shunt: evaluation of a model for heart failure in rat. Am J Physiol 236(5):H698-H704 (Pubitemid 9212795)
24. Fontes MSC, van Veen TAB, de Bakker JMT, van Rijen HVM (2012) Functional consequences of abnormal Cx43 expression in the heart. BBA Biomembr 1818(8):2020-2029. doi:10.1016/j.bbamem.2011.07.039
25. Gardner JD, Murray DB, Voloshenyuk TG, Brower GL, Bradley JM, Janicki JS (2010) Estrogen attenuates chronic volume overload induced structural and functional remodeling in male rat hearts. Am J Physiol Heart Circ Physiol 298(2):H497-H504. doi:10.1152/ajpheart.00336.2009
26. GautelM, Zuffardi O, Freiburg A, Labeit S (1995) Phosphorylation switches specific for the cardiac isoform of myosin binding protein-C: a modulator of cardiac contraction? EMBO J 14(9):1952-1960
27. Giovannone S, Remo BF, Fishman GI (2012) Channeling diversity: gap junction expression in the heart. Heart Rhythm9(7):1159-1162. doi:10.1016/j.hrthm.2011.11.040
28. Granzier H, Wu Y, Siegfried L, LeWinter M (2005) Titin: physiological function and role in cardiomyopathy and failure. Heart Fail Rev 10(3):211-223. doi:10.1007/s10741-005-5251-7 (Pubitemid 43115831)
29. Guggilam A, Hutchinson KR, West TA, Kelly AP, Galantowicz ML, Davidoff AJ, Sadayappan S, Lucchesi PA (2013) In vivo and in vitro cardiac responses to beta-adrenergic stimulation in volume-overload heart failure. J Mol Cell Cardiol 57:47-58. doi:10.1016/j.yjmcc.2012.11.013
30. Gupta MK, Gulick J, James J, Osinska H, Lorenz JN, Robbins J (2013) Functional dissection of myosin binding protein C phosphorylation. J Mol Cell Cardiol 64:39-50. doi:10.1016/j.yjmcc.2013.08.006
31. Hasenfuss G (1998) Animal models of human cardiovascular disease, heart failure and hypertrophy. Cardiovasc Res 39(1):60-76
32. Houser SR, Margulies KB, Murphy AM, Spinale FG, Francis GS, Prabhu SD, Rockman HA, Kass DA, Molkentin JD, Sussman MA, Koch WJ, American Heart Association Council on Basic Cardiovascular Sciences CoCC, Council on Functional G, Translational B (2012) Animal models of heart failure: a scientific statement from the American Heart Association. Circ Res 111(1):131-150. doi:10.1161/RES.0b013e3182582523
33. Husse B, Briest W, Homagk L, Isenberg G, Gekle M (2007) Cyclical mechanical stretch modulates expression of collagen I and collagen III by PKC and tyrosine kinase in cardiac fibroblasts. Am J Physiol Regul Integr Comp Physiol 293(5):R1898-R1907. doi:10.1152/ajpregu.00804.2006 (Pubitemid 350085665)
34. Hutchinson KR, Guggilam A, Cismowski MJ, Galantowicz ML, West TA, Stewart JA Jr, Zhang X, Lord KC, Lucchesi PA (2011) Temporal pattern of left ventricular structural and functional remodeling following reversal of volume overload heart failure. J Appl Physiol 111(6):1778-1788. doi:10.1152/ japplphysiol.00691.2011
35. Hutchinson KR, Stewart JA Jr, Lucchesi PA (2010) Extracellular matrix remodeling during the progression of volume overload-induced heart failure. J Mol Cell Cardiol 48(3):564-569. doi:10.1016/j.yjmcc.2009.06.001
36. Janicki JS, Brower GL (2002) The role of myocardial fibrillar collagen in ventricular remodeling and function. J Card Fail 8(6 Suppl):S319-S325. doi:10.1054/jcaf.2002.129260
37. Jobe LJ, Melendez GC, Levick SP, Du Y, Brower GL, Janicki JS (2009) TNF-alpha inhibition attenuates adverse myocardial remodeling in a rat model of volume overload. Am J Physiol Heart Circ Physiol 297(4):H1462-H1468. doi:10.1152/ajpheart.00442.2009
38. Juric D, Yao X, Thandapilly S, Louis X, Cantor E, Chaze B, Wojciechowski P, Vasanji Z, Yang T, Wigle J, Netticadan T (2010) Defects in ryanodine receptor function are associated with systolic dysfunction in rats subjected to volume overload. Exp Physiol 95(8):869-879. doi:10.1113/expphysiol.2009.052100
39. Katz AM, Konstam MA (2009) Heart failure: pathophysiology, molecular biology, and clinical management. Wolters Kluwer Health, Philadelphia
40. Kim KH, Kim YJ, Lee SP, Kim HK, Seo JW, Sohn DW, Oh BH, Park YB (2011) Survival, exercise capacity, and left ventricular remodeling in a rat model of chronic mitral regurgitation: serial echocardiography and pressure-volume analysis. Korean Circ J 41(10):603-611. doi:10.4070/kcj.2011.41.10.603
41. Kim KH, Kim YJ, Ohn JH, Yang J, Lee SE, Lee SW, Kim HK, Seo JW, Sohn DW(2012) Long-term effects of sildenafil in a rat model of chronic mitral regurgitation: benefits of ventricular remodeling and exercise capacity. Circulation 125(11):1390-1401. doi:10.1161/circulationaha.111.065300
42. Kleaveland JP, Kussmaul WG, Vinciguerra T, Diters R, Carabello BA (1988)Volume overload hypertrophy in a closed-chest model of mitral regurgitation. Am J Physiol 254(6 Pt 2):H1034-H1041
43. Kooij V, Holewinski RJ, Murphy AM, Van Eyk JE (2013) Characterization of the cardiac myosin binding protein-C phosphoproteome in healthy and failing human hearts. J Mol Cell Cardiol 60:116-120. doi:10.1016/j.yjmcc.2013.04.012
44. Levick SP, Melendez GC, Plante E, McLarty JL, Brower GL, Janicki JS (2011) Cardiac mast cells: the centrepiece in adverse myocardial remodelling. Cardiovasc Res 89(1):12-19. doi:10.1093/cvr/cvq272
45. Li J, Lu H, Plante E, Melendez GC, Levick SP, Janicki JS (2012) Stem cell factor is responsible for the rapid response in mature mast cell density in the acutely stressed heart. J Mol Cell Cardiol 53(4):469-474. doi:10.1016/j.yjmcc. 2012.07.011
46. Lim CC, Yang H, Yang M, Wang CK, Shi J, Berg EA, Pimentel DR, Gwathmey JK, Hajjar RJ, Helmes M, Costello CE, Huo S, Liao R (2008) A novel mutant cardiac troponin C disrupts molecular motions critical for calcium binding affinity and cardiomyocyte contractility. Biophys J 94(9):3577-3589. doi:10.1529/biophysj.107.112896
47. Liu Y, Dillon AR, Tillson M, Makarewich C, Nguyen V, Dell'Italia L, Sabri AK, Rizzo V, Tsai EJ (2013) Volume overload induces differential spatiotemporal regulation of myocardial soluble guanylyl cyclase in eccentric hypertrophy and heart failure. J Mol Cell Cardiol 60:72-83. doi:10.1016/j.yjmcc.2013.03.019
48. Lou Q, Janardhan A, Efimov IR (2012) Remodeling of calcium handling in human heart failure. Adv Exp Med Biol 740:1145-1174. doi:10.1007/978-94-007- 2888-2-52
49. Lu QW, Wu XY, Morimoto S (2013) Inherited cardiomyopathies caused by troponin mutations. J Geriatr Cardiol JGC 10(1):91-101. doi:10.3969/j.issn.1671- 5411.2013.01.014
50. McGinley JC, Berretta RM, Chaudhary K, Rossman E, Bratinov GD, Gaughan JP, Houser S, Margulies KB (2007) Impaired contractile reserve in severe mitral valve regurgitation with a preserved ejection fraction. Eur J Heart Fail 9(9):857-864. doi:10.1016/j.ejheart.2007.05.013 (Pubitemid 47332314)
51. McLaughlin HM, Kelly MA, Hawley PP, Darras BT, Funke B, Picker J (2013) Compound heterozygosity of predicted loss-of-function DES variants in a family with recessive desminopathy. BMC Med Genet 14:68. doi:10.1186/1471-2350-14-68
52. McLendon PM, Robbins J (2011) Desmin-related cardiomyopathy: an unfolding story. AmJ Physiol Heart Circ Physiol 301(4):H1220-H1228. doi:10.1152/ajpheart. 00601.2011
53. Melenovsky V (2013) Cardiac adaptation to volume overload. In: Ostadal B, Dhalla NS (eds) Cardiac adaptations: vol 4. Advances in biochemistry in health and disease. Springer, New York, pp 167-199. doi:10.1007/978-1-4614-5203-4-9
54. Memo M, Leung MC, Ward DG, dos Remedios C, Morimoto S, Zhang L, Ravenscroft G, McNamara E, Nowak KJ, Marston SB, Messer AE (2013) Familial dilated cardiomyopathy mutations uncouple troponin I phosphorylation from changes in myofibrillar Ca(2)(+) sensitivity. Cardiovasc Res 99(1):65-73. doi:10.1093/cvr/cvt071
55. Mirza M, Marston S, Willott R, Ashley C, Mogensen J, McKenna W, Robinson P, Redwood C, Watkins H (2005) Dilated cardiomyopathy mutations in three thin filament regulatory proteins result in a common functional phenotype. J Biol Chem 280(31):28498-28506. doi:10.1074/jbc.M412281200 (Pubitemid 41105750)
56. Mogensen J, Murphy RT, Shaw T, Bahl A, Redwood C, Watkins H, Burke M, Elliott PM, McKenna WJ (2004) Severe disease expression of cardiac troponin C and T mutations in patients with idiopathic dilated cardiomyopathy. J Am Coll Cardiol 44(10):2033-2040. doi:10.1016/j.jacc.2004.08.027 (Pubitemid 39473290)
57. Mohamed AS, Dignam JD, Schlender KK (1998) Cardiac myosin-binding protein C (MyBP-C): identification of protein kinase A and protein kinase C phosphorylation sites. Arch Biochem Biophys 358(2):313-319. doi:10.1006/abbi. 1998.0857 (Pubitemid 28480950)
58. Moore JR, Leinwand L, Warshaw DM (2012) Understanding cardiomyopathy phenotypes based on the functional impact of mutations in the myosin motor. Circ Res 111(3):375-385. doi:10.1161/circresaha.110.223842
59. Morimoto S (2008) Sarcomeric proteins and inherited cardiomyopathies. Cardiovasc Res 77(4):659-666. doi:10.1093/cvr/cvm084
60. 2+-desensitizing effect of a deletion mutation ΔK210 in cardiac troponin T that causes familial dilated cardiomyopathy. Proc Natl Acad Sci 99(2):913-918. doi:10.1073/pnas.022628899
61. Murray DB, Gardner JD, Brower GL, Janicki JS (2008) Effects of nonselective endothelin-1 receptor antagonism on cardiacmast cell-mediated ventricular remodeling in rats. Am J Physiol Heart Circ Physiol 294(3):H1251-H1257. doi:10.1152/ajpheart.00622.2007 (Pubitemid 351468721)
62. Olson TM, Illenberger S, Kishimoto NY, Huttelmaier S, Keating MT, Jockusch BM (2002) Metavinculin mutations alter actin interaction in dilated cardiomyopathy. Circulation 105(4):431-437 (Pubitemid 34141698)
63. Olson TM, Michels VV, Thibodeau SN, Tai YS, Keating MT (1998) Actin mutations in dilated cardiomyopathy, a heritable form of heart failure. Science 280(5364):750-752 (Pubitemid 28243352)
64. Palmer BM, Schmitt JP, Seidman CE, Seidman JG, Wang Y, Bell SP, Lewinter MM, Maughan DW (2013) Elevated rates of force development and MgATP binding in F764L and S532P myosin mutations causing dilated cardiomyopathy. J Mol Cell Cardiol 57:23-31. doi:10.1016/j.yjmcc.2012.12.022
65. Perry GJ, Mori T, Wei CC, Xu XY, Chen YF, Oparil S, Lucchesi P, Dell'Italia LJ (2001) Genetic variation in angiotensin-converting enzyme does not prevent development of cardiac hypertrophy or upregulation of angiotensin II in response to aortocaval fistula. Circulation 103(7):1012-1016 (Pubitemid 32183809)
66. 2+ content in isolated failing and nonfailing human myocardium. Circ Res 85(1):38-46
67. Pinto JR, Siegfried JD, Parvatiyar MS, Li D, Norton N, Jones MA, Liang J, Potter JD, Hershberger RE (2011) Functional characterization of TNNC1 rare variants identified in dilated cardiomyopathy. J Biol Chem 286(39):34404-34412. doi:10.1074/jbc.M111.267211
68. Posch MG, Posch MJ, Geier C, Erdmann B, MuellerW, Richter A, Ruppert V, Pankuweit S, Maisch B, Perrot A, Buttgereit J, Dietz R, HaverkampW, Ozcelik C (2008)Amissense variant in desmoglein-2 predisposes to dilated cardiomyopathy. Mol Genet Metab 95(1-2):74-80. doi:10.1016/j.ymgme.2008.06.005
69. Preston LC, Lipscomb S, Robinson P, Mogensen J, McKenna WJ, Watkins H, Ashley CC, Redwood CS (2007) Functional effects of the DCM mutant Gly159Asp troponin C in skinned muscle fibres. Pflugers Arch Eur J Physiol 453(6):771-776. doi:10.1007/s00424-006-0161-7 (Pubitemid 46294929)
70. PrevisMJ, Beck Previs S, Gulick J, Robbins J, Warshaw DM (2012) Molecular mechanics of cardiac myosin-binding protein C in native thick filaments. Science 337(6099):1215-1218. doi:10.1126/science.1223602
71. PuM, Gao Z, Pu DK, DavidsonWR Jr (2013) Effects of early, late, and long-term nonselective beta-blockade on left ventricular remodeling, function, and survival in chronic organic mitral regurgitation. Circ Heart Fail 6(4):756-762. doi:10.1161/circheartfailure.112.000196
72. Pu M, Gao Z, Zhang X, Liao D, Pu DK, Brennan T, Davidson WR Jr (2009) Impact of mitral regurgitation on left ventricular anatomic and molecular remodeling and systolic function: implication for outcome. Am J Physiol Heart Circ Physiol 296(6):H1727-H1732. doi:10.1152/ajpheart.00882.2008
73. Rajan S, Ahmed RP, Jagatheesan G, Petrashevskaya N, Boivin GP, Urboniene D, Arteaga GM, Wolska BM, Solaro RJ, Liggett SB, Wieczorek DF (2007) Dilated cardiomyopathy mutant tropomyosin mice develop cardiac dysfunction with significantly decreased fractional shortening and myofilament calcium sensitivity. Circ Res 101(2):205-214. doi:10.1161/circresaha.107.148379 (Pubitemid 47196588)
74. Redwood C, Robinson P (2013) Alpha-tropomyosin mutations in inherited cardiomyopathies. J Muscle Res Cell Motil 34(3-4):285-294. doi:10.1007/s10974- 013-9358-5
75. Reid AC, Silver RB, Levi R (2007) Renin: at the heart of the mast cell. Immunol Rev 217:123-140. doi:10.1111/j.1600-065X.2007.00514.x (Pubitemid 46718147)
76. Remo BF, Giovannone S, Fishman GI (2012) Connexin43 cardiac gap junction remodeling: lessons from genetically engineered murine models. J Membr Biol 245(5-6):275-281. doi:10.1007/s00232-012-9448-0
77. Ruzicka M, Keeley FW, Leenen FH (1994) The renin-angiotensin system and volume overload-induced changes in cardiac collagen and elastin. Circulation 90(4):1989-1996 (Pubitemid 24320952)
78. Ryan TD, Rothstein EC, Aban I, Tallaj JA, Husain A, Lucchesi PA, Dell' Italia LJ (2007) Left ventricular eccentric remodeling and matrix loss are mediated by bradykinin and precede cardiomyocyte elongation in rats with volume overload. J Am Coll Cardiol 49(7):811-821. doi:10.1016/j.jacc.2006.06.083 (Pubitemid 46240707)
79. Sabri A, Rafiq K, Seqqat R, KolpakovMA, Dillon R, Dell'Italia LJ (2008) Sympathetic activation causes focal adhesion signaling alteration in early compensated volume overload attributable to isolated mitral regurgitation in the dog. Circ Res 102(9):1127-1136. doi:10.1161/circresaha.107.163642 (Pubitemid 351667867)
80. Sadayappan S, de Tombe PP (2013) Cardiac myosin binding protein-C as a central target of cardiac sarcomere signaling: a special mini review series. Pflugers Arch Eur J Physiol. doi:10.1007/s00424-013-1396-8
81. Sadayappan S, Gulick J, Osinska H, Barefield D, Cuello F, Avkiran M, Lasko VM, Lorenz JN, Maillet M, Martin JL, Brown JH, Bers DM, Molkentin JD, James J, Robbins J (2011) A critical function for Ser-282 in cardiac Myosin binding protein-C phosphorylation and cardiac function. Circ Res 109(2):141-150. doi:10.1161/CIRCRESAHA.111.242560
82. Salameh A, Dhein S (2013) Effects ofmechanical forces and stretch on intercellular gap junction coupling. Biochim Biophys Acta 1828(1):147-156. doi:10.1016/j.bbamem.2011.12.030
83. Saygili E, Rana OR, Meyer C, Gemein C, Andrzejewski MG, Ludwig A, Weber C, Schotten U, Kruttgen A, Weis J, Schwinger RH, Mischke K, Rassaf T, Kelm M, Schauerte P (2009) The angiotensin-calcineurin - NFAT pathway mediates stretch-induced up-regulation of matrix metalloproteinases-2/-9 in atrial myocytes. Basic Res Cardiol 104(4):435 -448. doi:10.1007/s00395-008-0772-6
84. Scheuermann-Freestone M, Freestone NS, Langenickel T, Hohnel K, Dietz R, Willenbrock R (2001) A new model of congestive heart failure in the mouse due to chronic volume overload. Eur J Heart Fail 3(5):535-543 (Pubitemid 34619194)
85. Schmitt JP, Debold EP, Ahmad F, Armstrong A, Frederico A, Conner DA, Mende U, Lohse MJ, Warshaw D, Seidman CE, Seidman JG (2006) Cardiac myosin missense mutations cause dilated cardiomyopathy in mouse models and depress molecular motor function. Proc Natl Acad Sci U S A 103(39):14525-14530. doi:10.1073/pnas.0606383103 (Pubitemid 44484783)
86. 2+ release promote eccentric myocardial remodeling and pump failure death in response to pressure overload. J Am Coll Cardiol. doi:10.1016/j.jacc.2013.11.010
87. Seqqat R, Guo X, Rafiq K, Kolpakov MA, Guo J, Koch WJ, Houser SR, Dell'Italia LJ, Sabri A (2012) Beta1-adrenergic receptors promote focal adhesion signaling downregulation and myocyte apoptosis in acute volume overload. JMol Cell Cardiol 53(2):240-249. doi:10.1016/j.yjmcc.2012.05.004
88. Severs NJ, Bruce AF, Dupont E, Rothery S (2008) Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res 80(1):9-19. doi:10.1093/cvr/cvn133
89. Shah SJ, Aistrup GL, Gupta DK, O'Toole MJ, Nahhas AF, Schuster D, Chirayil N, Bassi N, Ramakrishna S, Beussink L, Misener S, Kane B, Wang D, Randolph B, Ito A, Wu M, Akintilo L, Mongkolrattanothai T, Reddy M, Kumar M, Arora R, Ng J, Wasserstrom JA (2013) Ultrastructural and cellular basis for the development of abnormal myocardial mechanics during the transition from hypertension to heart failure. Am J Physiol Heart Circ Physiol. doi:10.1152/ajpheart.00642.2013
90. Sheikh F, Ross RS, Chen J (2009) Cell-cell connection to cardiac disease. Trends Cardiovasc Med 19(6):182-190. doi:10.1016/j.tcm.2009.12.001
91. Song W, Dyer E, Stuckey D, Leung MC, Memo M, Mansfield C, Ferenczi M, Liu K, Redwood C, Nowak K, Harding S, Clarke K, Wells D, Marston S (2010) Investigation of a transgenic mouse model of familial dilated cardiomyopathy. J Mol Cell Cardiol 49(3):380-389. doi:10.1016/j.yjmcc.2010.05.009
92. Stewart JA Jr, Wei CC, Brower GL, Rynders PE, Hankes GH, Dillon AR, Lucchesi PA, Janicki JS, Dell'Italia LJ (2003) Cardiac mast cell- and chymase-mediated matrix metalloproteinase activity and left ventricular remodeling in mitral regurgitation in the dog. J Mol Cell Cardiol 35(3):311-319 (Pubitemid 36379175)
93. Swynghedauw B (1986) Developmental and functional adaptation of contractile proteins in cardiac and skeletal muscles. Physiol Rev 66(3):710-771
94. Tavora F, Zhang M, Cresswell N, Li L, Fowler D, FrancoM, Burke A (2013) Quantitative immunohistochemistry of desmosomal proteins (plakoglobin, desmoplakin and plakophilin), Connexin-43, and N-cadherin in arrhythmogenic cardiomyopathy: an autopsy study. Open Cardiovasc Med J 7:28 - 35. doi:10.2174/1874192401307010028
95. Taylor MR, Slavov D, Ku L, Di Lenarda A, Sinagra G, Carniel E, Haubold K, Boucek MM, Ferguson D, Graw SL, Zhu X, Cavanaugh J, Sucharov CC, Long CS, Bristow MR, Lavori P, Mestroni L, Familial Cardiomyopathy R, Bank BD (2007) Prevalence of desmin mutations in dilated cardiomyopathy. Circulation 115(10):1244-1251. doi:10.1161/circulationaha.106.646778 (Pubitemid 46594768)
96. Wang TL, Yang YH, Chang H, Hung CR (2004) Angiotensin II signals mechanical stretch-induced cardiac matrix metalloproteinase expression via JAK-STAT pathway. J Mol Cell Cardiol 37(3):785-794. doi:10.1016/j.yjmcc.2004.06. 016 (Pubitemid 39194570)
97. Wang XH, Zhuo XZ, Ni YJ, Gong M, Wang TZ, Lu Q, Ma AQ (2012) Improvement of cardiac function and reversal of gap junction remodeling by neuregulin-1beta in volume-overloaded rats with heart failure. J Geriatr Cardiol JGC 9(2):172-179. doi:10.3724/sp.j.1263.2012.03271
98. Wang Y, Tanner BC, Lombardo AT, Tremble SM, Maughan DW, Vanburen P, Lewinter MM, Robbins J, Palmer BM (2013) Cardiac myosin isoforms exhibit differential rates of MgADP release and MgATP binding detected by myocardial viscoelasticity. J Mol Cell Cardiol 54:1-8. doi:10.1016/j.yjmcc.2012.10.010
99. Weber KT (1989) Cardiac interstitium in health and disease: the fibrillar collagen network. J Am Coll Cardiol 13(7):1637-1652
100. Wei CC, Chen Y, Powell LC, Zheng J, Shi K, Bradley WE, Powell PC, Ahmad S, Ferrario CM, Dell'Italia LJ (2012) Cardiac kallikrein-kinin system is upregulated in chronic volume overload and mediates an inflammatory induced collagen loss. PLoS One 7(6):e40110. doi:10.1371/journal.pone.0040110
101. Wei CC, Hase N, Inoue Y, Bradley EW, Yahiro E, Li M, Naqvi N, Powell PC, Shi K, Takahashi Y, Saku K, Urata H, Dell'Italia LJ, Husain A (2010) Mast cell chymase limits the cardiac efficacy of Ang I-converting enzyme inhibitor therapy in rodents. J Clin Investig 120(4):1229-1239. doi:10.1172/jci39345
102. Wei CC, Lucchesi PA, Tallaj J, BradleyWE, Powell PC, Dell'Italia LJ (2003) Cardiac interstitial bradykinin and mast cells modulate pattern of LV remodeling in volume overload in rats. Am J Physiol Heart Circ Physiol 285(2):H784-H792. doi:10.1152/ajpheart.00793.2001
103. Wei S, Guo A, Chen B, KutschkeW, Xie YP, Zimmerman K, Weiss RM, AndersonME, Cheng H, Song LS (2010) T-tubule remodeling during transition from hypertrophy to heart failure. Circ Res 107(4):520-531. doi:10.1161/circresaha. 109.212324
104. Wolny M, Colegrave M, Colman L, White E, Knight PJ, Peckham M (2013) Cardiomyopathy mutations in the tail of beta-cardiac myosin modify the coiled-coil structure and affect integration into thick filaments in muscle sarcomeres in adult cardiomyocytes. J Biol Chem 288(44):31952-31962. doi:10.1074/jbc.M113.513291
105. Zheng J, Yancey DM, Ahmed MI, Wei CC, Powell PC, Shanmugam M, Gupta H, Lloyd SG, McGiffin DC, Schiros CG, Denney TS Jr, Babu GJ, Dell'Italia LJ (2013) Increased sarcolipin expression and adrenergic drive in humans with preserved left ventricular ejection fraction and chronic isolated mitral regurgitation. Circ Heart Fail. doi:10.1161/circheartfailure.113.000519