© 1999 American Heart Association, Inc.
Original Contribution |
Ca2+ Handling and Sarcoplasmic Reticulum Ca2+ Content in Isolated Failing and Nonfailing Human Myocardium
From the Zentrum Innere Medizin (B.P., L.S.M., G.H.), Abteilung Kardiologie und Pneumologie, Georg-August-Universität Göttingen, Göttingen, Germany, and the Department of Physiology (D.M.B.), Loyola University Chicago, Maywood, Ill.
Correspondence to PD Dr Burkert Pieske, Zentrum Innere Medizin, Abteilung Kardiologie und Pneumologie, Georg-August-Universität Göttingen, Robert-Koch-Str. 40, 37075 Göttingen, Germany. E-mail pieske{at}med.uni-goettingen.de
Abstract—Disturbed sarcoplasmic reticulum (SR) Ca2+ content may underlie the altered force-frequency and postrest contractile behavior in failing human myocardium. We used rapid cooling contractures (RCCs) to assess SR Ca2+ content in ventricular muscle strips isolated from nonfailing and end-stage failing human hearts. With an increase in rest intervals (1 to 240 s; 37°C), nonfailing human myocardium (n=7) exhibited a parallel increase in postrest twitch force (at 240 s by 121±44%; P<0.05) and RCC amplitude (by 69±53%; P<0.05). In contrast, in failing myocardium (n=30), postrest twitch force decreased at long rest intervals and RCC amplitude declined monotonically with rest (by 25±9% and 53±9%, respectively; P<0.05). With an increase in stimulation frequencies (0.25 to 3 Hz), twitch force increased continuously in nonfailing human myocardium (n=7) by 71±17% (at 3 Hz; P<0.05) and RCC amplitude increased in parallel by 247±55% (P<0.05). In contrast, in failing myocardium (n=26), twitch force declined by 29±7% (P<0.05) and RCC amplitude increased only slightly by 36±14% (P<0.05). Paired RCCs were evoked to investigate the relative contribution of SR Ca2+ uptake and Na+/Ca2+ exchange to cytosolic Ca2+ removal during relaxation. SR Ca2+ uptake (relative to the Na+/Ca2+ exchange) increased significantly in nonfailing but not in failing human myocardium as stimulation rates increased. We conclude that the negative force-frequency relation in failing human myocardium is due to an inability of SR Ca2+ content to increase sufficiently at high frequencies and thus cannot overcome the frequency-dependent refractoriness of SR Ca2+ release. The rest-dependent decay in twitch force in failing myocardium is due to rest-dependent decline in SR Ca2+ content. These alterations could be secondary to depressed SR Ca2+-ATPase combined with enhanced cytosolic Ca2+ extrusion via Na+/Ca2+ exchange.
Key Words: Ca2+ • Na+/Ca2+ exchange • myocardial contraction • sarcoplasmic reticulum • heart failure
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R. Sah, R. J Ramirez, G. Y Oudit, D. Gidrewicz, M. G Trivieri, C. Zobel, and P. H Backx Regulation of cardiac excitation-contraction coupling by action potential repolarization: role of the transient outward potassium current (Ito) J. Physiol., January 1, 2003; 546(1): 5 - 18. [Abstract] [Full Text] [PDF]
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F. del Monte and R. J Hajjar Targeting calcium cycling proteins in heart failure through gene transfer J. Physiol., January 1, 2003; 546(1): 49 - 61. [Abstract] [Full Text] [PDF]
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W. Schillinger and H. Kogler Altered phosphorylation and Ca2+-sensitivity of myofilaments in human heart failure Cardiovasc Res, January 1, 2003; 57(1): 5 - 7. [Full Text] [PDF]
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M. T. Jiang, A. J. Lokuta, E. F. Farrell, M. R. Wolff, R. A. Haworth, and H. H. Valdivia Abnormal Ca2+ Release, but Normal Ryanodine Receptors, in Canine and Human Heart Failure Circ. Res., November 29, 2002; 91(11): 1015 - 1022. [Abstract] [Full Text] [PDF]
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B. D Stuyvers, A. D McCulloch, J. Guo, H. J Duff, and H. E D J ter Keurs Effect of stimulation rate, sarcomere length and Ca2+ on force generation by mouse cardiac muscle J. Physiol., November 1, 2002; 544(3): 817 - 830. [Abstract] [Full Text] [PDF]
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A. G Schmidt, J. Zhai, A. N Carr, M. J Gerst, J. N Lorenz, P. Pollesello, A. Annila, B. D Hoit, and E. G Kranias Structural and functional implications of the phospholamban hinge domain: impaired SR Ca2+ uptake as a primary cause of heart failure Cardiovasc Res, November 1, 2002; 56(2): 248 - 259. [Abstract] [Full Text] [PDF]
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G. Antoons, K. Mubagwa, I. Nevelsteen, and K. R Sipido Mechanisms underlying the frequency dependence of contraction and [Ca2+]i transients in mouse ventricular myocytes J. Physiol., September 15, 2002; 543(3): 889 - 898. [Abstract] [Full Text] [PDF]
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A. M. Gomez, B. Schwaller, H. Porzig, G. Vassort, E. Niggli, and M. Egger Increased Exchange Current but Normal Ca2+ Transport via Na+-Ca2+ Exchange During Cardiac Hypertrophy After Myocardial Infarction Circ. Res., August 23, 2002; 91(4): 323 - 330. [Abstract] [Full Text] [PDF]
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D. E. Michele, C. A. Gomez, K. E. Hong, M. V. Westfall, and J. M. Metzger Cardiac Dysfunction in Hypertrophic Cardiomyopathy Mutant Tropomyosin Mice Is Transgene-Dependent, Hypertrophy-Independent, and Improved by {beta}-Blockade Circ. Res., August 9, 2002; 91(3): 255 - 262. [Abstract] [Full Text] [PDF]
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B. Pieske, L. S. Maier, V. Piacentino III, J. Weisser, G. Hasenfuss, and S. Houser Rate Dependence of [Na+]i and Contractility in Nonfailing and Failing Human Myocardium Circulation, July 23, 2002; 106(4): 447 - 453. [Abstract] [Full Text] [PDF]
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N. R. Alpert, L. A. Mulieri, and D. Warshaw The failing human heart Cardiovasc Res, April 1, 2002; 54(1): 1 - 10. [Full Text] [PDF]
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G. Hasenfuss, L. S. Maier, H.-P. Hermann, C. LUers, M. HUnlich, O. Zeitz, P. M.L. Janssen, and B. Pieske Influence of Pyruvate on Contractile Performance and Ca2+ Cycling in Isolated Failing Human Myocardium Circulation, January 15, 2002; 105(2): 194 - 199. [Abstract] [Full Text] [PDF]
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 D. J. Thuerauf, H. Hoover, J. Meller, J. Hernandez, L. Su, C. Andrews, W. H. Dillmann, P. M. McDonough, and C. C. Glembotski Sarco/endoplasmic Reticulum Calcium ATPase-2 Expression Is Regulated by ATF6 during the Endoplasmic Reticulum Stress Response. INTRACELLULAR SIGNALING OF CALCIUM STRESS IN A CARDIAC MYOCYTE MODEL SYSTEM J. Biol. Chem., December 14, 2001; 276(51): 48309 - 48317. [Abstract] [Full Text] [PDF]
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A. O. Verkerk, M. W. Veldkamp, A. Baartscheer, C. A. Schumacher, C. Klopping, A. C.G. van Ginneken, and J. H. Ravesloot Ionic Mechanism of Delayed Afterdepolarizations in Ventricular Cells Isolated From Human End-Stage Failing Hearts Circulation, November 27, 2001; 104(22): 2728 - 2733. [Abstract] [Full Text] [PDF]
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J. M. Cotton, M. T. Kearney, P. A. MacCarthy, R. M. Grocott-Mason, D. R. McClean, C. Heymes, P. J. Richardson, and A. M. Shah Effects of Nitric Oxide Synthase Inhibition on Basal Function and the Force-Frequency Relationship in the Normal and Failing Human Heart In Vivo Circulation, November 6, 2001; 104(19): 2318 - 2323. [Abstract] [Full Text] [PDF]
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F. Somura, H. Izawa, M. Iwase, Y. Takeichi, R. Ishiki, T. Nishizawa, A. Noda, K. Nagata, Y. Yamada, and M. Yokota Reduced Myocardial Sarcoplasmic Reticulum Ca2+-ATPase mRNA Expression and Biphasic Force-Frequency Relations in Patients With Hypertrophic Cardiomyopathy Circulation, August 7, 2001; 104(6): 658 - 663. [Abstract] [Full Text] [PDF]
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S. Adachi-Akahane and Y. Kurachi New Era for Translational Research in Cardiac Arrhythmias Circ. Res., June 8, 2001; 88(11): 1095 - 1096. [Full Text] [PDF]
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I. A. Hobai and B. O'Rourke Decreased Sarcoplasmic Reticulum Calcium Content Is Responsible for Defective Excitation-Contraction Coupling in Canine Heart Failure Circulation, March 20, 2001; 103(11): 1577 - 1584. [Abstract] [Full Text] [PDF]
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J. M. O'Donnell, C. M. Sumbilla, H. Ma, I. K. G. Farrance, M. Cavagna, M. G. Klein, and G. Inesi Tight Control of Exogenous SERCA Expression Is Required to Obtain Acceleration of Calcium Transients With Minimal Cytotoxic Effects in Cardiac Myocytes Circ. Res., March 2, 2001; 88(4): 415 - 421. [Abstract] [Full Text] [PDF]
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C. M.N. Terracciano, K. D. Philipson, and K. T. MacLeod Overexpression of the Na+/Ca2+ exchanger and inhibition of the sarcoplasmic reticulum Ca2+-ATPase in ventricular myocytes from transgenic mice Cardiovasc Res, January 1, 2001; 49(1): 38 - 47. [Abstract] [Full Text] [PDF]
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W. H. Barry Na+-Ca2+ Exchange in Failing Myocardium : Friend or Foe? Circ. Res., September 29, 2000; 87(7): 529 - 531. [Full Text] [PDF]
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K. Ito, X. Yan, M. Tajima, Z. Su, W. H. Barry, and B. H. Lorell Contractile Reserve and Intracellular Calcium Regulation in Mouse Myocytes From Normal and Hypertrophied Failing Hearts Circ. Res., September 29, 2000; 87(7): 588 - 595. [Abstract] [Full Text] [PDF]
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L. S. Maier, P. Barckhausen, J. Weisser, I. Aleksic, M. Baryalei, and B. Pieske Ca2+ handling in isolated human atrial myocardium Am J Physiol Heart Circ Physiol, September 1, 2000; 279(3): H952 - H958. [Abstract] [Full Text] [PDF]
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D. M. Bers Calcium Fluxes Involved in Control of Cardiac Myocyte Contraction Circ. Res., August 18, 2000; 87(4): 275 - 281. [Full Text] [PDF]
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L. Sen, G. Cui, G. C. Fonarow, and H. Laks Differences in mechanisms of SR dysfunction in ischemic vs. idiopathic dilated cardiomyopathy Am J Physiol Heart Circ Physiol, August 1, 2000; 279(2): H709 - H718. [Abstract] [Full Text] [PDF]
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