Intracellular dyssynchrony of diastolic cytosolic [Ca2+] decay in ventricular cardiomyocytes in cardiac remodeling and human heart failure

Circulation Research

Volumn 113, Issue 5, 2013, Pages 527-538

  Hohendanner, Felix ^a   Ljubojević, Senka ^a,d   Macquaide, Niall ^c   Sacherer, Michael ^a   Sedej, Simon ^a,d   Biesmans, Liesbeth ^c   Wakula, Paulina ^a,d   Platzer, Dieter ^a   Sokolow, Sophie ^b   Herchuelz, André ^b   Antoons, Gudrun ^a   Sipido, Karin ^c   Pieske, Burkert ^a,d   Heinzel, Frank R ^a,d  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b FREE UNIVERSITY OF BRUSSELS   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

Author keywords

calcium; diastole; heart failure; mitochondria; myocytes, cardiac; ventricular remodeling

Indexed keywords

2 [4 (2,5 DIFLUOROBENZYLOXY)PHENOXY] 5 ETHOXYANILINE; ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM; CYCLOPIAZONIC ACID; FORSKOLIN; ISTAROXIME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; CALCIUM TRANSPORT; CELL SYNCHRONIZATION; CYTOSOL; DIASTOLE; HEART FAILURE; HEART HYPERTROPHY; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART VENTRICLE; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SARCOMERE LENGTH; SARCOPLASMIC RETICULUM; STIMULATION; VENTRICULAR CARDIOMYOCYTE;

CALCIUM; DIASTOLE; HEART FAILURE; MITOCHONDRIA; MYOCYTES, CARDIAC; VENTRICULAR REMODELING;

ANILINE COMPOUNDS; ANIMALS; CALCIUM SIGNALING; CALCIUM-TRANSPORTING ATPASES; COLFORSIN; CYTOSOL; DIASTOLE; ELECTRIC STIMULATION; ETIOCHOLANOLONE; HEART FAILURE; HEART VENTRICLES; HUMANS; HYPERTROPHY; HYPERTROPHY, LEFT VENTRICULAR; INDOLES; MICE; MITOCHONDRIA, HEART; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC; PHENYL ETHERS; RUTHENIUM COMPOUNDS; SARCOMERES; SARCOPLASMIC RETICULUM; SODIUM-CALCIUM EXCHANGER; SUS SCROFA; SWINE; VENTRICULAR REMODELING;

EID: 84883454811     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.113.300895     Document Type: Article

References (49)

1. Kuijpers NH, Hermeling E, Bovendeerd PH, Delhaas T, Prinzen FW. Modeling cardiac electromechanics and mechanoelectrical coupling in dyssynchronous and failing hearts: Insight from adaptive computer models. J Cardiovasc Transl Res. 2012;5:159-169
2. Stevenson WG, Hernandez AF, Carson PE, et al Heart Failure Society of America Guideline Committee. Indications for cardiac resynchronization therapy: 2011 update from the Heart Failure Society of America Guideline Committee. J Card Fail. 2012;18:94-106
3. Yu CM, Chan YS, Zhang Q, Yip GW, Chan CK, Kum LC, Wu L, Lee AP, Lam YY, Fung JW. Benefits of cardiac resynchronization therapy for heart failure patients with narrow QRS complexes and coexisting systolic asynchrony by echocardiography. J Am Coll Cardiol. 2006;48:2251-2257
4. Bers DM. Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol. 2008;70:23-49
5. Baylor SM, Hollingworth S. Model of sarcomeric Ca2+ movements, including ATP Ca2+ binding and diffusion, during activation of frog skeletal muscle. J Gen Physiol. 1998;112:297-316
6. Smith G, MacQuaide N. Cytoplasmic versus intra-SR: The battle of the Ca2+ diffusion coefficients in cardiac muscle. Biophys J. 2008;95:1005-1006
7. Heinzel FR, Bito V, Volders PG, Antoons G, Mubagwa K, Sipido KR. Spatial and temporal inhomogeneities during Ca2+ release from the sarcoplasmic reticulum in pig ventricular myocytes. Circ Res. 2002;91:1023-1030
8. Heinzel FR, Bito V, Biesmans L, Wu M, Detre E, von Wegner F, Claus P, Dymarkowski S, Maes F, Bogaert J, Rademakers F, D'hooge J, Sipido K. Remodeling of T-tubules and reduced synchrony of Ca2+ release in myocytes from chronically ischemic myocardium. Circ Res. 2008;102:338-346
9. Louch WE, Mørk HK, Sexton J, Strømme TA, Laake P, Sjaastad I, Sejersted OM. T-tubule disorganization and reduced synchrony of Ca2+ release in murine cardiomyocytes following myocardial infarction. J Physiol. 2006;574:519-533
10. Kranias EG, Hajjar RJ. Modulation of cardiac contractility by the phospholamban/ SERCA2a regulatome. Circ Res. 2012;110:1646-1660
11. Ruknudin AM, Wei SK, Haigney MC, Lederer WJ, Schulze DH. Phosphorylation and other conundrums of Na/Ca exchanger, NCX1. Ann N Y Acad Sci. 2007;1099:103-118
12. Boncompagni S, Rossi AE, Mii M, Beznoussenko GV, Polishchuk RS, Dirksen RT, Protasi F. Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures. Mol Biol Cell. 2009;20:1058-1067
13. Sacherer M, Sedej S, Wakula P, Wallner M, Vos M, Kockskamper J, Stiegler P, Sereinigg M, von LD, Antoons G, Pieske B, Heinzel F. JTV519 (K201) reduces sarcoplasmic reticulum Ca(2+) leak and improves diastolic function in vitro in murine and human non-failing myocardium. Br J Pharmacol 2012;167:493-504
14. Nguidjoe E, Sokolow S, Bigabwa S, et al. Heterozygous inactivation of the Na/Ca exchanger increases glucose-induced insulin release, beta-cell proliferation, and mass. Diabetes 2011;60:2076-2085
15. Mühlfeld C, Schipke J, Schmidt A, Post H, Pieske B, Sedej S. Hypoinnervation is an early event in experimental myocardial remodelling induced by pressure overload. J Anat. 2013;222:634-644
16. Ljubojevic S, Walther S, Asgarzoei M, Sedej S, Pieske B, Kockskämper J. In situ calibration of nucleoplasmic versus cytoplasmic Ca2+ concentration in adult cardiomyocytes. Biophys J. 2011;100:2356-2366
17. Rocchetti M, Besana A, Mostacciuolo G, Micheletti R, Ferrari P, Sarkozi S, Szegedi C, Jona I, Zaza A. Modulation of sarcoplasmic reticulum function by Na+/K+ pump inhibitors with different toxicity: Digoxin and PST2744 [(E,Z)-3-((2-aminoethoxy)imino)androstane-6,17-dione hydrochloride]. J Pharmacol Exp Ther. 2005;313:207-215
18. Díaz ME, Trafford AW, Eisner DA. The role of intracellular Ca buffers in determining the shape of the systolic Ca transient in cardiac ventricular myocytes. Pflugers Arch. 2001;442:96-100
19. Heinzel FR, MacQuaide N, Biesmans L, Sipido K. Dyssynchrony of Ca2+ release from the sarcoplasmic reticulum as subcellular mechanism of cardiac contractile dysfunction. J Mol Cell Cardiol. 2011;50:390-400
20. Louch WE, Bito V, Heinzel FR, Macianskiene R, Vanhaecke J, Flameng W, Mubagwa K, Sipido KR. Reduced synchrony of Ca2+ release with loss of T-tubules-a comparison to Ca2+ release in human failing cardiomyocytes. Cardiovasc Res. 2004;62:63-73
21. Bers DM. Excitation-Contraction Coupling and Cardiac Contractile Force. 2nd ed. Dodrecht, The Netherlands: kluver Academic Publishers; 2001
22. Stern MD. Theory of excitation-contraction coupling in cardiac muscle. Biophys J. 1992;63:497-517
23. Song LS, Sobie EA, McCulle S, Lederer WJ, Balke CW, Cheng H. Orphaned ryanodine receptors in the failing heart. Proc Natl Acad Sci U S A. 2006;103:4305-4310
24. Pieske B, Maier LS, Bers DM, Hasenfuss G. Ca2+ handling and sarcoplasmic reticulum Ca2+ content in isolated failing and nonfailing human myocardium. Circ Res. 1999;85:38-46
25. Drago GA, Colyer J, Lederer WJ. Immunofluorescence localization of SERCA2a and the phosphorylated forms of phospholamban in intact rat cardiac ventricular myocytes. Ann N Y Acad Sci. 1998;853:273-279
26. Vangheluwe P, Louch WE, Ver Heyen M, Sipido K, Raeymaekers L, Wuytack F. Ca2+ transport ATPase isoforms SERCA2a and SERCA2b are targeted to the same sites in the murine heart. Cell Calcium. 2003;34:457-464
27. Hove-Madsen L, Bers DM. Sarcoplasmic reticulum Ca2+ uptake and thapsigargin sensitivity in permeabilized rabbit and rat ventricular myocytes. Circ Res. 1993;73:820-828
28. Csordás G, Renken C, Várnai P, Walter L, Weaver D, Buttle KF, Balla T, Mannella CA, Hajnóczky G. Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol. 2006;174:915-921
29. De Marchi U, Castelbou C, Demaurex N. Uncoupling protein 3 (UCP3) modulates the activity of Sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) by decreasing mitochondrial ATP production. J Biol Chem. 2011;286:32533-32541
30. Arnaudeau S, Kelley WL, Walsh JV, Jr, Demaurex N. Mitochondria recycle Ca(2+) to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J Biol Chem. 2001;276: 29430-29439
31. Edman KA. The role of non-uniform sarcomere behaviour during relaxation of striated muscle. Eur Heart J. 1980;suppl A:49-57
32. Edman KA, Flitney FW. Laser diffraction studies of sarcomere dynamics during 'isometric' relaxation in isolated muscle fibres of the frog. J Physiol. 1982;329:1-20
33. Stern MD, Capogrossi MC, Lakatta EG. Spontaneous calcium release from the sarcoplasmic reticulum in myocardial cells: Mechanisms and consequences. Cell Calcium. 1988;9:247-256
34. Caputo C, Edman KA, Lou F, Sun YB. Variation in myoplasmic Ca2+ concentration during contraction and relaxation studied by the indicator fluo-3 in frog muscle fibres. J Physiol. 1994;478 (pt 1):137-148
35. Backx PH, Gao WD, Azan-Backx MD, Marban E. The relationship between contractile force and intracellular [Ca2+] in intact rat cardiac trabeculae. J Gen Physiol. 1995;105:1-19
36. Janssen PM, Stull LB, Marbán E. Myofilament properties comprise the rate-limiting step for cardiac relaxation at body temperature in the rat. Am J Physiol Heart Circ Physiol. 2002;282:H499-H507
37. del Monte F, Harding SE, Schmidt U, Matsui T, Kang ZB, Dec GW, Gwathmey JK, Rosenzweig A, Hajjar RJ. Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation. 1999;100:2308-2311
38. Müller OJ, Lange M, Rattunde H, Lorenzen HP, Müller M, Frey N, Bittner C, Simonides W, Katus HA, Franz WM. Transgenic rat hearts overexpressing SERCA2a show improved contractility under baseline conditions and pressure overload. Cardiovasc Res. 2003;59:380-389
39. Bluhm WF, Kranias EG, Dillmann WH, Meyer M. Phospholamban: A major determinant of the cardiac force-frequency relationship. Am J Physiol Heart Circ Physiol. 2000;278:H249-H255
40. He H, Giordano FJ, Hilal-Dandan R, Choi DJ, Rockman HA, McDonough PM, Bluhm WF, Meyer M, Sayen MR, Swanson E, Dillmann WH. Overexpression of the rat sarcoplasmic reticulum Ca2+ ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J Clin Invest. 1997;100:380-389
41. Stehle R, Krüger M, Pfitzer G. Force kinetics and individual sarcomere dynamics in cardiac myofibrils after rapid ca(2+) changes. Biophys J. 2002;83:2152-2161
42. Ter Keurs HE, Wakayama Y, Miura M, Stuyvers BD, Boyden PA, Landesberg A. Spatial nonuniformity of contraction causes arrhythmogenic Ca2+ waves in rat cardiac muscle. Ann N Y Acad Sci. 2005;1047:345-365
43. Miura M, Nishio T, Hattori T, Murai N, Stuyvers BD, Shindoh C, Boyden PA. Effect of nonuniform muscle contraction on sustainability and frequency of triggered arrhythmias in rat cardiac muscle. Circulation. 2010;121:2711-2717
44. Jessup M, Abraham WT, Casey DE, Feldman AM, Francis GS, Ganiats TG, Konstam MA, Mancini DM, Rahko PS, Silver MA, Stevenson LW, Yancy CW. 2009 focused update: ACCF/AHA Guidelines for the Diagnosis and Management of Heart Failure in Adults: A report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines: Developed in collaboration with the International Society for Heart and Lung Transplantation. Circulation. 2009;119:1977-2016
45. Chen L, Gong Q, Stice JP, Knowlton AA. Mitochondrial OPA1, apoptosis, and heart failure. Cardiovasc Res. 2009;84:91-99
46. Barth E, Stämmler G, Speiser B, Schaper J. Ultrastructural quantitation of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man. J Mol Cell Cardiol. 1992;24:669-681
47. Isoda K, Kamezawa Y, Tada N, Sato M, Ohsuzu F. Myocardial hypertrophy in transgenic mice overexpressing human interleukin 1alpha. J Card Fail. 2001;7:355-364
48. Mészáros J, Lévai G. Ultrastructural and electrophysiological alterations during the development of catecholamine-induced cardiac hypertrophy and failure. Acta Biol Hung. 1990;41:289-307
49. Coleman R, Silbermann M, Gershon D, Reznick AZ. Giant mitochondria in the myocardium of aging and endurance-trained mice. Gerontology. 1987;33:34-39