Summary
Steps involved in excitation-contraction coupling in mammalian myocardium have been derived using a relatively limited number of animal species. However, the use of animal models for investigations into excitation-contraction coupling in normal and disease states has encompassed a wide range of animal species. We addressed the question as to whether excitation-contraction coupling as currently understood applies to intracellular calcium handling in myocardium from multiple mammalian species, amphibian, and avian myocardium. The bioluminescent calcium indicator aequorin was used to record intracellular calcium transients in both ventricular and atrial tissue. We report that in all mammalian and avian species studied the calcium transient recorded in both ventricular and atrial myocardium is monophasic and reflects calcium release and re-uptake by the sarcoplasmic reticulum. In contrast, the Ca2+ transient recorded from salamander myocardium is prolonged relative to mammalian and avian myocardium, and appears to reflect in part trans-sarcolemmal calcium entry. Only in diseased myocardium derived from human and swine myocardium was a second component detected in the calcium transient. These data indicate that sarcoplasmic reticulum calcium handling is pivotal in excitation-contraction coupling for multiple species with differing physiologies. Also, in disease states, intracellular calcium handling is often affected with resultant alterations in the time-course and/or configuration of the calcium transient.
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References
Allen DG, Blinks JR (1978) Calcium transients in aequorin-injected frog cardiac muscle. Natue, 273:509–513
Allen DG, Kurihara S (1980) Calcium transients in mammalian ventricular muscle. Eur Heart J 1 (Suppl A):5–15
Bing OHL, Books WW, Perreault CL, Morgan JP (1989) Calcium transients and inotrophy in hypertrophied and failing myocardium from the spontaneously hypertensive rat. Circulation 80:II-502
Blinks JR, Endoh M (1986) Modification of myofibrillar responsiveness to Ca++ as an inotropic mechanism. Circulation 73(Suppl III):85–98
Blinks JR, Rudel R, Taylor SR (1978) Calcium transients in isolated amphibian skeletal muscle fibers: Detection with aequorin. J Physiol 277:291–323
Blinks JR, Wier WG, Hess P, Prendergast FG (1982) Measurement of Ca2+ concentrations in living cells. Prog Biophys Mol Biol 40:1–114
Endoh M, Blinks JR (1988) Actions of sympathomimetic amines on the Ca2+ transients and contractions of rabbit myocardium: reciprocal changes in myofibrillar responsiveness to Ca2+ mediated through alpha- and beta-adrenoceptors. Circ Res 62(2):247–265
Fabiato A (1981) Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricle. J Gen Physiol 78:457–497
Fabiato A (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245(14):C1-C14
Groden DL, Guan Z, Biagi BA, Altschuld RA, Stokes BT (1989) Calcium transients and electrophysiology in failing rat myocytes. Circulation 80(4):II-504
Gwathmey JK, Briggs GM, Slawsky MT, Perreault CL, Wei JY, Morgan JP (1987) Effect of exercise conditioning on intracellular calcium handling in heart muscle from aged rats. Circulation 76:IV-332
Gwathmey JK, Copelas L, MacKinnon R, Schoen F, Feldman MD, Grossman W, Morgan JP (1987) Abnormal intracellular calcium handling in myocardium from patients with end-stage heart failure. Circ Res 61:70–76
Gwathmey JK, Morgan JP (1985) Altered calcium handling in experimental pressure-overload hypertrophy in the ferret. Circ Res 57:836–843
Gwathmey JK, Morgan JP (1986) Subcellular mechanisms of inotropic agents. In: Allert JA, Adams HR (eds) New perspectives in veterinary pharmacology and therapeutics. Columbia, Missouri: University of Missouri, pp 116–180
Gwathmey JK, Nakao S, Matsumori A, Als V, Serur JR, Murphy JC, Abelmann WH (1986) Large animal model of viral myocarditis. Circulation 74:163
Harigaya S, Schwartz A (1969) Rate of calcium binding and uptake in normal animal and failing human cardiac muscle. Circ Res 25:781–794
Kavaler F (1974) Electromechanical time course in frog ventricle: Manipulation of calcium level during voltage clamp. J Mol Cell Cardiol 6:575–580
Kihara Y, Morgan JP (1989) A comparative study of three methods for intracellular calcium loading of the calcium indicator aequorin in ferret papillary muscles. Biochem Biophys Res Commun 162:402–407
Kirchberger MA, Tada M, Katz AM (1974) Adenosine 3′,5′ monophosphate dependent protein kinase-catalyzed phosphorylation reaction and its relationship to calcium transport in cardiac sarcoplasmic reticulum. J Biol Chem 249:6166–6173
Kihara Y, Gwathmey JK, Grorgan JP (1989) Mechanisms of positive inotropic effects and delayed relaxation produced by DPI 201–106 in mammalian working myocardium: Effects on intracellular calcium handling. Br J Pharmacol 96:927–939
Lakatta EG (1987) Do hypertension and aging have a similar effect on myocardium? Circulation 75 (suppl I):169–177
Li O, Bragi B, Starling R, Hohl C, Altschuld R, Stokes B (1989) Characteristics of calcium transients and electrophysiology in hurman ventricular myocytes. Biophys J 55:488a
MacKinnon R, Gwathmey JK, Allen PD, Briggs GM, Morgan JP (1988) Modulation by the thyroid state of intracellular calcium and contractility in ferret ventricular myocardium. Circ Res 63:1080–1089
Marsh JD, Allen PD (1989) Developmental regulation of cardiac calcium channels and contractile sensitivity to [Ca]0. Am J Physiol 256:H179-H187
Morgan JP, Blinks JR (1982) Intracellular Ca++ transients in the cat papillary muscle. Can J Physiol Pharmacol 60:524–528
Morgan JP, Morgan KG (1984) Calcium and cardiovascular function: intracellular calcium levels during contraction and relaxation of mammalian cardiac and vascular smooth muscle as detected with aequorin. Am J Med 77 (suppl 5A):33–46
Morgan JP, Morgan KG (1984) A chemical procedure for loading the calcium indicator aequorin into mammalian working myocardium. Pflügers Arch 400:338–340
Sen L, Smith W (1989) Cardiac sarcoplasmic reticulum dysfunction in cardiomyopathic hamster. Circulation 80(4):II-503
Siri FM, Nordin CW, Sonnenblick EH, Aronson RS (1989) Reduced peak systolic myoplasmic calcium in hypertrophied guinea pig myocytes. Circulation 80(4):II-503
Slawsky MT, Gwathmey JK, Come PC, Abelman WH (1989) Porcine model of myocarditis leading to dilated cardiomyopathy. J Am Coll Cardiol 13(2):253A
The Merck Veterinary Manual Sixth Edition Editors: Clarence M. Fraser and Asa Mays. Published by Merck and Co., Inc. Rahway, N.J., U.S.A., 1986
Warren SE, Hague NL, Morgan JP (1989) Normal intracellular calcium availability in the hypertrophic Syrian hamster. Clin Res 37:305A
Wier WG (1980) Calcium transients during excitation-contraction coupling in mammalian heart: aequorin signals of canine Purkinje fibers. Science 207:1085–1087
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Gwathmey, J.K., Morgan, J.P. Calcium handling in myocardium from amphibian, avian, and mammalian species: the search for two components. J Comp Physiol B 161, 19–25 (1991). https://doi.org/10.1007/BF00258742
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DOI: https://doi.org/10.1007/BF00258742