Relaxation and the Role of Calcium in Isolated Contracting Myocardium from Patients with Hypertensive Heart Disease and Heart Failure with Preserved Ejection Fraction

Circulation: Heart Failure

Volumn 10, Issue 8, 2017, Pages

  Runte, K Elisabeth ^a   Bell, Stephen P ^a   Selby, Donald E ^a   Häußler, Tim N ^a   Ashikaga, Takamuru ^b   Lewinter, Martin M ^b   Palmer, Bradley M ^b   Meyer, Markus ^a  

^a FLETCHER ALLEN HEALTH CARE   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

diastole; Fura 2; heart failure; sodium

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); AMILORIDE; CALCIUM; CALCIUM CHANNEL; CALSEQUESTRIN; COPPER; FUROSEMIDE; IRON; MAGNESIUM; MYOSIN HEAVY CHAIN; PHOSPHOLAMBAN; PHOSPHORUS DERIVATIVE; RANOLAZINE; RYANODINE RECEPTOR 2; SODIUM; SODIUM CHANNEL; SODIUM PROTON EXCHANGE PROTEIN; SULFUR; ZINC;

AGED; ARTICLE; ATOMIC EMISSION SPECTROMETRY; CARDIOVASCULAR PARAMETERS; COHORT ANALYSIS; CONTROLLED STUDY; DIASTOLE; ECHOCARDIOGRAPHY; ELEMENTAL ANALYSIS; FEMALE; GENE EXPRESSION; HEART CONTRACTION; HEART FAILURE WITH PRESERVED EJECTION FRACTION; HEART LEFT VENTRICLE MASS; HEART MUSCLE BIOPSY; HEART MUSCLE CONTRACTILE FORCE; HEART VENTRICLE HYPERTROPHY; HUMAN; HUMAN TISSUE; HYPERTENSION; LUNG ARTERY PRESSURE; MAJOR CLINICAL STUDY; MALE; MUSCLE RELAXATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RELAXATION TIME; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SODIUM TRANSPORT; TIME TO PEAK TENSION; WESTERN BLOTTING; BIOPSY; CARDIAC MUSCLE; HEART FAILURE; HEART LEFT VENTRICLE FUNCTION; HEART STROKE VOLUME; HEART VENTRICLE; METABOLISM; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

AGED; BIOPSY; BLOTTING, WESTERN; CALCIUM; DIASTOLE; FEMALE; HEART FAILURE; HEART VENTRICLES; HUMANS; HYPERTENSION; MALE; MIDDLE AGED; MYOCARDIAL CONTRACTION; MYOCARDIUM; STROKE VOLUME; VENTRICULAR FUNCTION, LEFT;

EID: 85027498209     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.117.004311     Document Type: Article

References (55)

1. Levy D, Anderson KM, Savage DD, Kannel WB, Christiansen JC, Castelli WP. Echocardiographically detected left ventricular hypertrophy: prevalence and risk factors. The Framingham heart study. Ann Intern Med. 1988;108:7-13.
2. Schirmer H, Lunde P, Rasmussen K. Prevalence of left ventricular hypertrophy in a general population; the Tromsø study. Eur Heart J. 1999;20:429-438.
3. Drazner MH. The progression of hypertensive heart disease. Circulation. 2011;123:327-334. doi: 10. 1161/CIRCULATIONAHA. 108. 845792.
4. Movahed MR, Martinez A, Greaves J, Greaves S, Morrell H, Hashemzadeh M. Left ventricular hypertrophy is associated with obesity, male gender, and symptoms in healthy adolescents. Obesity (Silver Spring). 2009;17:606-610. doi: 10. 1038/oby. 2008. 563.
5. Aljaroudi W, Alraies MC, Halley C, Rodriguez L, Grimm RA, Thomas JD, Jaber WA. Impact of progression of diastolic dysfunction on mortality in patients with normal ejection fraction. Circulation. 2012;125:782-788. doi: 10. 1161/CIRCULATIONAHA. 111. 066423.
6. Owan TE, Hodge DO, Herges RM, Jacobsen SJ, Roger VL, Redfield MM. Trends in prevalence and outcome of heart failure with preserved ejection fraction. N Engl J Med. 2006;355:251-259. doi: 10. 1056/NEJMoa052256.
7. Zile MR, Baicu CF, Ikonomidis JS, Stroud RE, Nietert PJ, Bradshaw AD, Slater R, Palmer BM, Van Buren P, Meyer M, Redfield MM, Bull DA, Granzier HL, LeWinter MM. Myocardial stiffness in patients with heart failure and a preserved ejection fraction: contributions of collagen and titin. Circulation. 2015;131:1247-1259. doi: 10. 1161/CIRCULATIONAHA. 114. 013215.
8. Borbély A, van der Velden J, Papp Z, Bronzwaer JG, Edes I, Stienen GJ, Paulus WJ. Cardiomyocyte stiffness in diastolic heart failure. Circulation. 2005;111:774-781. doi: 10. 1161/01. CIR. 0000155257. 33485. 6D.
9. Borbély A, Falcao-Pires I, van Heerebeek L, Hamdani N, Edes I, Gavina C, Leite-Moreira AF, Bronzwaer JG, Papp Z, van der Velden J, Stienen GJ, Paulus WJ. Hypophosphorylation of the stiff N2B titin isoform raises cardiomyocyte resting tension in failing human myocardium. Circ Res. 2009;104:780-786. doi: 10. 1161/CIRCRESAHA. 108. 193326.
10. LeWinter MM, Granzier H. Cardiac titin: a multifunctional giant. Circulation. 2010;121:2137-2145. doi: 10. 1161/CIRCULATIONAHA. 109. 860171.
11. Donaldson C, Palmer BM, Zile M, Maughan DW, Ikonomidis JS, Granzier H, Meyer M, VanBuren P, LeWinter MM. Myosin cross-bridge dynamics in patients with hypertension and concentric left ventricular remodeling. Circ Heart Fail. 2012;5:803-811. doi: 10. 1161/CIRCHEARTFAILURE. 112. 968925.
12. Selby DE, Palmer BM, LeWinter MM, Meyer M. Tachycardia-induced diastolic dysfunction and resting tone in myocardium from patients with a normal ejection fraction. J Am Coll Cardiol. 2011;58:147-154. doi: 10. 1016/j. jacc. 2010. 10. 069.
13. Bers DM, Barry WH, Despa S. Intracellular Na+ regulation in cardiac myocytes. Cardiovasc Res. 2003;57:897-912.
14. Morrow DA, Scirica BM, Karwatowska-Prokopczuk E, Murphy SA, Budaj A, Varshavsky S, Wolff AA, Skene A, McCabe CH, Braunwald E; MERLINTIMI 36 Trial Investigators. Effects of ranolazine on recurrent cardiovascular events in patients with non-ST-elevation acute coronary syndromes: the MERLIN-TIMI 36 randomized trial. JAMA. 2007;297:1775-1783. doi: 10. 1001/jama. 297. 16. 1775.
15. Matsumura H, Hara A, Hashizume H, Maruyama K, Abiko Y. Protective effects of ranolazine, a novel anti-ischemic drug, on the hydrogen peroxideinduced derangements in isolated, perfused rat heart: comparison with dichloroacetate. Jpn J Pharmacol. 1998;77:31-39.
16. Maltsev VA, Sabbah HN, Higgins RS, Silverman N, Lesch M, Undrovinas AI. Novel, ultraslow inactivating sodium current in human ventricular cardiomyocytes. Circulation. 1998;98:2545-2552.
17. Zaza A, Belardinelli L, Shryock JC. Pathophysiology and pharmacology of the cardiac "late sodium current. " Pharmacol Ther. 2008;119:326-339. doi: 10. 1016/j. pharmthera. 2008. 06. 001.
18. Song Y, Shryock JC, Wu L, Belardinelli L. Antagonism by ranolazine of the pro-arrhythmic effects of increasing late INa in guinea pig ventricular myocytes. J Cardiovasc Pharmacol. 2004;44:192-199.
19. Fraser H, Belardinelli L, Wang L, Light PE, McVeigh JJ, Clanachan AS. Ranolazine decreases diastolic calcium accumulation caused by ATX-II or ischemia in rat hearts. J Mol Cell Cardiol. 2006;41:1031-1038. doi: 10. 1016/j. yjmcc. 2006. 08. 012.
20. Sossalla S, Wagner S, Rasenack EC, Ruff H, Weber SL, Schöndube FA, Tirilomis T, Tenderich G, Hasenfuss G, Belardinelli L, Maier LS. Ranolazine improves diastolic dysfunction in isolated myocardium from failing human hearts-role of late sodium current and intracellular ion accumulation. J Mol Cell Cardiol. 2008;45:32-43. doi: 10. 1016/j. yjmcc. 2008. 03. 006.
21. Maier LS, Layug B, Karwatowska-Prokopczuk E, Belardinelli L, Lee S, Sander J, Lang C, Wachter R, Edelmann F, Hasenfuss G, Jacobshagen C. RAnoLazIne for the treatment of diastolic heart failure in patients with preserved ejection fraction: the RALI-DHF proof-of-concept study. JACC Heart Fail. 2013;1:115-122. doi: 10. 1016/j. jchf. 2012. 12. 002.
22. Mulieri LA, Hasenfuss G, Ittleman F, Blanchard EM, Alpert NR. Protection of human left ventricular myocardium from cutting injury with 2, 3-butanedione monoxime. Circ Res. 1989;65:1441-1449.
23. Paulus WJ, Tschöpe C, Sanderson JE, Rusconi C, Flachskampf FA, Rademakers FE, Marino P, Smiseth OA, De Keulenaer G, Leite-Moreira AF, Borbély A, Edes I, Handoko ML, Heymans S, Pezzali N, Pieske B, Dickstein K, Fraser AG, Brutsaert DL. How to diagnose diastolic heart failure: a consensus statement on the diagnosis of heart failure with normal left ventricular ejection fraction by the Heart Failure and Echocardiography Associations of the European Society of Cardiology. Eur Heart J. 2007;28:2539-2550. doi: 10. 1093/eurheartj/ehm037.
24. Donaldson C, Taatjes DJ, Zile M, Palmer B, VanBuren P, Spinale F, Maughan D, Von Turkovich M, Bishop N, LeWinter MM. Combined immunoelectron microscopic and computer-assisted image analyses to detect advanced glycation end-products in human myocardium. Histochem Cell Biol. 2010;134:23-30. doi: 10. 1007/s00418-010-0706-x.
25. Mulieri LA, Barnes W, Leavitt BJ, Ittleman FP, LeWinter MM, Alpert NR, Maughan DW. Alterations of myocardial dynamic stiffness implicating abnormal crossbridge function in human mitral regurgitation heart failure. Circ Res. 2002;90:66-72.
26. Meyer M, Keweloh B, Güth K, Holmes JW, Pieske B, Lehnart SE, Just H, Hasenfuss G. Frequency-dependence of myocardial energetics in failing human myocardium as quantified by a new method for the measurement of oxygen consumption in muscle strip preparations. J Mol Cell Cardiol. 1998;30:1459-1470. doi: 10. 1006/jmcc. 1998. 0706.
27. Meyer M, Schillinger W, Pieske B, Holubarsch C, Heilmann C, Posival H, Kuwajima G, Mikoshiba K, Just H, Hasenfuss G. Alterations of sarcoplasmic reticulum proteins in failing human dilated cardiomyopathy. Circulation. 1995;92:778-784.
28. Subramanian M, Hunt AL, Petrucci GA, Chen Z, Hendley ED, Palmer BM. Differential metal content and gene expression in rat left ventricular hypertrophy due to hypertension and hyperactivity. J Trace Elem Med Biol. 2014;28:311-316. doi: 10. 1016/j. jtemb. 2014. 02. 002.
29. Mohammed SF, Hussain S, Mirzoyev SA, Edwards WD, Maleszewski JJ, Redfield MM. Coronary microvascular rarefaction and myocardial fibrosis in heart failure with preserved ejection fraction. Circulation. 2015;131:550-559. doi: 10. 1161/CIRCULATIONAHA. 114. 009625.
30. Shah AM, Shah SJ, Anand IS, Sweitzer NK, O'Meara E, Heitner JF, Sopko G, Li G, Assmann SF, McKinlay SM, Pitt B, Pfeffer MA, Solomon SD; TOPCAT Investigators. Cardiac structure and function in heart failure with preserved ejection fraction: baseline findings from the echocardiographic study of the treatment of preserved cardiac function heart failure with an aldosterone antagonist trial. Circ Heart Fail. 2014;7:104-115. doi: 10. 1161/CIRCHEARTFAILURE. 113. 000887.
31. Zile MR, Gottdiener JS, Hetzel SJ, McMurray JJ, Komajda M, McKelvie R, Baicu CF, Massie BM, Carson PE; I-PRESERVE Investigators. Prevalence and significance of alterations in cardiac structure and function in patients with heart failure and a preserved ejection fraction. Circulation. 2011;124:2491-2501. doi: 10. 1161/CIRCULATIONAHA. 110. 011031.
32. Pitt B, Pfeffer MA, Assmann SF, Boineau R, Anand IS, Claggett B, Clausell N, Desai AS, Diaz R, Fleg JL, Gordeev I, Harty B, Heitner JF, Kenwood CT, Lewis EF, O'Meara E, Probstfield JL, Shaburishvili T, Shah SJ, Solomon SD, Sweitzer NK, Yang S, McKinlay SM; TOPCAT Investigators. Spironolactone for heart failure with preserved ejection fraction. N Engl J Med. 2014;370:1383-1392. doi: 10. 1056/NEJMoa1313731.
33. Zile MR, Baicu CF, Gaasch WH. Diastolic heart failure-abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med. 2004;350:1953-1959. doi: 10. 1056/NEJMoa032566.
34. Hwang SJ, Melenovsky V, Borlaug BA. Implications of coronary artery disease in heart failure with preserved ejection fraction. J Am Coll Cardiol. 2014;63(25 pt A):2817-2827. doi: 10. 1016/j. jacc. 2014. 03. 034.
35. Borlaug BA, Lam CS, Roger VL, Rodeheffer RJ, Redfield MM. Contractility and ventricular systolic stiffening in hypertensive heart disease insights into the pathogenesis of heart failure with preserved ejection fraction. J Am Coll Cardiol. 2009;54:410-418. doi: 10. 1016/j. jacc. 2009. 05. 013.
36. Ikonomidis I, Lekakis JP, Nikolaou M, Paraskevaidis I, Andreadou I, Kaplanoglou T, Katsimbri P, Skarantavos G, Soucacos PN, Kremastinos DT. Inhibition of interleukin-1 by anakinra improves vascular and left ventricular function in patients with rheumatoid arthritis. Circulation. 2008;117:2662-2669. doi: 10. 1161/CIRCULATIONAHA. 107. 731877.
37. Van Tassell BW, Seropian IM, Toldo S, Mezzaroma E, Abbate A. Interleukin-1? induces a reversible cardiomyopathy in the mouse. Inflamm Res. 2013;62:637-640. doi: 10. 1007/s00011-013-0625-0.
38. Alpert NR, Leavitt BJ, Ittleman FP, Hasenfuss G, Pieske B, Mulieri LA. A mechanistic analysis of the force-frequency relation in non-failing and progressively failing human myocardium. Basic Res Cardiol. 1998;93(suppl 1):23-32.
39. Higginbotham MB, Morris KG, Williams RS, McHale PA, Coleman RE, Cobb FR. Regulation of stroke volume during submaximal and maximal upright exercise in normal man. Circ Res. 1986;58:281-291.
40. Meyer M, McEntee RK, Nyotowidjojo I, Chu G, LeWinter MM. Relationship of exercise capacity and left ventricular dimensions in patients with a normal ejection fraction. An exploratory study. PLoS One. 2015;10:e0119432. doi: 10. 1371/journal. pone. 0119432.
41. Chung CS, Hutchinson KR, Methawasin M, Saripalli C, Smith JE 3rd, Hidalgo CG, Luo X, Labeit S, Guo C, Granzier HL. Shortening of the elastic tandem immunoglobulin segment of titin leads to diastolic dysfunction. Circulation. 2013;128:19-28. doi: 10. 1161/CIRCULATIONAHA. 112. 001268.
42. López B, González A, Hermida N, Valencia F, de Teresa E, Díez J. Role of lysyl oxidase in myocardial fibrosis: from basic science to clinical aspects. Am J Physiol Heart Circ Physiol. 2010;299:H1-H9. doi: 10. 1152/ ajpheart. 00335. 2010.
43. Pieske B, Maier LS, Piacentino V 3rd, Weisser J, Hasenfuss G, Houser S. Rate dependence of [Na+]i and contractility in nonfailing and failing human myocardium. Circulation. 2002;106:447-453.
44. Rubin Y, Kessler-Icekson G, Navon G. The effect of furosemide on calcium ion concentration in myocardial cells. Cell Calcium. 1995;18:135-139.
45. Dikshit K, Vyden JK, Forrester JS, Chatterjee K, Prakash R, Swan HJ. Renal and extrarenal hemodynamic effects of furosemide in congestive heart failure after acute myocardial infarction. N Engl J Med. 1973;288:1087-1090. doi: 10. 1056/NEJM197305242882102.
46. Kohmoto O, Krueger JA, Barry WH. Activation of furosemide-sensitive K+ fluxes in myocytes by ouabain and recovery from metabolic inhibition. Am J Physiol. 1990;259(3 pt 2):H962-H972.
47. Cingolani HE, Ennis IL. Sodium-hydrogen exchanger, cardiac overload, and myocardial hypertrophy. Circulation. 2007;115:1090-1100. doi: 10. 1161/CIRCULATIONAHA. 106. 626929.
48. von Lewinski D, Kockskämper J, Zhu D, Post H, Elgner A, Pieske B. Reduced stretch-induced force response in failing human myocardium caused by impaired Na(+)-contraction coupling. Circ Heart Fail. 2009;2:47-55. doi: 10. 1161/CIRCHEARTFAILURE. 108. 794065.
49. Engelhardt S, Hein L, Keller U, Klämbt K, Lohse MJ. Inhibition of Na(+)-H(+) exchange prevents hypertrophy, fibrosis, and heart failure in beta(1)-adrenergic receptor transgenic mice. Circ Res. 2002;90:814-819.
50. Chahine M, Bkaily G, Nader M, Al-Khoury J, Jacques D, Beier N, Scholz W. NHE-1-dependent intracellular sodium overload in hypertrophic hereditary cardiomyopathy: prevention by NHE-1 inhibitor. J Mol Cell Cardiol. 2005;38:571-582. doi: 10. 1016/j. yjmcc. 2005. 01. 003.
51. Cheitlin MD, Byrd R, Benowitz N, Liu E, Modin G. Amiloride improves hemodynamics in patients with chronic congestive heart failure treated with chronic digoxin and diuretics. Cardiovasc Drugs Ther. 1991;5:719-725.
52. Studer R, Reinecke H, Bilger J, Eschenhagen T, Böhm M, Hasenfuss G, Just H, Holtz J, Drexler H. Gene expression of the cardiac Na(+)-Ca2+ exchanger in end-stage human heart failure. Circ Res. 1994;75:443-453.
53. LeWinter MM, Meyer M. Mechanisms of diastolic dysfunction in heart failure with a preserved ejection fraction: if it's not one thing it's another. Circ Heart Fail. 2013;6:1112-1115. doi: 10. 1161/CIRCHEARTFAILURE. 113. 000825.
54. van Heerebeek L, Borbély A, Niessen HW, Bronzwaer JG, van der Velden J, Stienen GJ, Linke WA, Laarman GJ, Paulus WJ. Myocardial structure and function differ in systolic and diastolic heart failure. Circulation. 2006;113:1966-1973. doi: 10. 1161/CIRCULATIONAHA. 105. 587519.
55. Rosas PC, Liu Y, Abdalla MI, Thomas CM, Kidwell DT, Dusio GF, Mukhopadhyay D, Kumar R, Baker KM, Mitchell BM, Powers PA, Fitzsimons DP, Patel BG, Warren CM, Solaro RJ, Moss RL, Tong CW. Phosphorylation of cardiac myosin-binding protein-C is a critical mediator of diastolic function. Circ Heart Fail. 2015;8:582-594. doi: 10. 1161/CIRCHEARTFAILURE. 114. 001550.