Abstract
This study was designed to investigate the changes in cardiac contractile properties induced by triiodothyronine (T3) administration in adult rats. Myofibrils and myosin were isolated from ventricular muscles from euthyroid and hyperthyroid animals and enzymatically and electrophoretically characterized. The time course of the isometric response, the force velocity curve, the force interval relation were studied in papillary muscles isolated from the right ventricles of euthyroid and hyperthyroid rats. T3 administration induced significant increases in Mg2+ activated myofibrillar ATPase activity (+11.4%) and in Ca2+ activated myosin ATPase activity (+20.1%). Significant increases in shortening velocity at low and zero loads (+20.4%) were found in papillary muscles from treated animals when compared with the control muscles. These variations in enzymatic activity and shortening velocity could be related to the increase in the amount of the fast isomyosin V1, as shown by pyrophosphate gel electrophoresis. The negative force-frequency relation at steady state, typical of rat cardiac preparations, was observed in treated and control animals; its slope was, however, halved in hyperthyroid papillary muscles when compared with control ones. In accordance with this finding, the potentiating effect of a prolonged diastolic interval was significantly reduced in hyperthyroid papillary muscles. In the frame of an interpretation of the force interval relation on the basis of the excitation contraction coupling processes, these latter observations might indicate an enhanced activity of the sarcoplasmic reticulum. We conclude that thyroid hormone administration has a dual effect on cardiac contractility, on one hand regulating the synthesis of the different isomyosin and, on the other hand, stimulating the activity of the sarcoplasmic reticulum.
Similar content being viewed by others
References
Alpert NR, Mulieri LA (1982) Heat, mechanics and myosin ATPase in normal and hypertrophied heart muscle. Fed Proc 41:192–198
Baràny M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50:197–216
Buccino RA, Spann JF, Pool PE, Sonnenblick EH, Braunwald E (1976) Influence of the thyroid state on the intrinsic contractile properties and energy stores of the myocardium. J Clin Invest 46:1669–1681
Capasso JM, Malhotra A, Scheuer J, Sonnenblick EH (1986) Myocardial biochemical, contractile and electrical performance after imposition of hypertension in young and old rats. Circ Res 58:445–460
Chizzonite RA, Zak R (1984) Regulation of myosin isoenzyme composition in fetal and neonatal rat ventricle by endogenous thyroid hormones. J Biol Chem 259:12,628–12,632
Dillmann WH (1983) Hormonal influences on cardiac myosin ATPase activity and myosin isoenzyme distribution. Mol Cell Endocrinol 34:169–181
Ebrech G, Rupp H, Jacob R (1982) Alterations of mechanical parameters in chemically skinned preparations of rat myocardium as a function of isoenzyme pattern of myosin. Basic Res Cardiol 77:220–234
Effron MB, Ruano-Arroyo G, Spurgeon HA, Bhatnagar GM, Lakatta EG (1983) Hyperthyroid state reverses prolonged contraction in rat cardiac muscle without altering myofibrillar ATPase activity. Fed Proc 42:465 (abstract)
Eisenberg E, Hill TL, Chen YD (1980) Cross bridge model of muscle contraction: quantitative analysis. Biophys J 29:195–227
Fabiato A, Fabiato F (1979) Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 75:463–505
Flink IL, Morkin E (1977) Evidence for a new cardiac myosin species in thyrotoxic rabbits. FEBS Lett 81:391–394
Gunning JF, Harrison CE Jr, Coleman III HN (1974) Myocardial contractility and energetics following treatment with d-thyroxine. Am J Physiol 226:1166–1171
Henry PD (1975) Positive staircase effect in the rat heart. Am J Physiol 228:360–364
Hoh JFY, McGrath PA, Hale PT (1977) Electrophoretic analysis of multiple forms of rat cardiac myosin: effects of hypophysectomy and thyroxine replacement. J Mol Cell Cardiol 10:1053–1076
Horowitz M, Peyser YM, Muhlrad A (1986) Alterations in cardiac myosin isoenzymes distribution as an adaptation to chronic environmental heat stress in the rat. J Mol Cell Cardiol 18:511–516
Kim D, Smith TW (1985) Effects of thyroid hormone on calcium handling in cultured chick ventricular cells. J Physiol (Lond) 364:431–449
Limas CJ (1978) Enhanced phosphorylation of myocardial sarcoplasmic reticulum in experimental hyperthyrodism. Am J Physiol 234:H426-H431
Litten RZ, Martin BJ, Buchthal RH, Nagai R, Low RB, Alpert NR (1985) Heterogeneity of myosin isoenzyme content of rabbit heart. Circ Res 57:406–414
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Martin AF, Pagani ED, Solaro RJ (1982) Thyroxine induced redistribution of isoenzymes of rabbit ventricular myosin. Circ Res 50:117–124
Martin AF, Robinson DC, Dowell RT (1985) Isomyosin and thyroid hormone levels in pressure overloaded weanling and adult rat hearts. Am J Physiol 248:H305-H310
Maruyama M, Goodkind MJ (1968) Effect of thyroid hormone on the force frequency relationship of atrial myocardium from the guinea pig. Circ Res 23:734–751
McKinnon R, Morgan JP (1986) Influence of the thyroid state on the calcium transient in ventricular muscle. Pflügers Arch 407:142–144
Morkin E (1979) Stimulation of cardiac myosin adenosin triphosphatase in thyrotoxicosis. Circ Res 44:1–7
Morkin E, Flink IL, Goldman S (1983) Biochemical and physiological effects of thyroid hormone on cardiac performance. Prog Cardiovasc Dis 25:435–464
Nayler WG, Merrilees NCR, Chipperfield D, Kurtz JB (1971) Influence of hyperthyroidism on the uptake and binding of calcium by cardiac microsomal fractions and mitochondrial structure. Cardiovasc Res 5:469–482
Orchard CH, Lakatta EG (1985) Intracellular calcium transients and developed tension in rat heart muscle. J Gen Physiol 86:637–651
Pagani ED, Julian FJ (1984) Rabbit papillary muscle myosin isoenzymes and the velocity of muscle shortening. Circ Res 54:586–594
Pagani ED, Solaro RJ (1983) Swimming exercise, thyroid state and the distribution of myosin isoenzymes in rat heart. Am J Physiol 245:H713-H720
Poggesi C, Everts M, Polla B, Tanzi F, Reggiani C (1987) Influence of thyroid state on mechanical restitution of rat myocardium. Circ Res 60:142–151
Ragnarsdottir K, Wohlfart B, Johnnsson M (1982) Mechanical restitution of the rat papillary muscle. Acta Physiol Scand 115:183–191
Rovetto MJ, Hjalmarson AC, Morgan HE, Barrett MJ, Goldstein RA (1972) Hormonal control of cardiac myosin triphosphatase in the rat. Circ Res 31:397–409
Rupp H (1982) The adaptive changes in the isoenzyme pattern of myosin from hypertrophied rat myocardium as a result of pressure overload and physical training. Basic Res Cardiol 76:79–88
Samuel JL, Rappaport L, Syrovy I, Winsnewsky C, Marotte F, Whalen RG, Schwartz K (1986) Differential effect of thyroxine on atrial and ventricular isomyosins in rats. Am J Physiol 250:H333-H341
Schouten VJA, ter Keurs HEDJ (1986) The force frequency relationship in rat myocardium. Pflügers Arch 407:14–17
Schwartz K, Lecarpentier Y, Martin JL, Lompre AM, Mercadier JJ, Swynghedauw B (1981) Myosin isoenzimic distribution correlates with speed of myocardial contraction. J Mol Cell Cardiol 13:1071–1075
Sheer D, Morkin E (1984) Myosin isoenzyme expression in rat ventricle: effects of thyroid hormone analogs, catecholamines, glucocorticoids and high carbohydrate diet. J Pharmacol Exp Ther 229:872–879
Solaro RJ, Pang DC, Briggs FN (1971) Purification of cardiac myofibrils with Triton X-100. Biochim Biophys Acta 245:259–262
Strauer BE, Scherpe A (1975) Experimental hyperthyroidism. II. Mechanics of contraction and relaxation of isolated ventricular myocardium. Basic Res Cardiol 70:130–141
Suko J (1973) The calcium pump of cardiac sarcoplasmic reticulum. Functional alterations at different levels of the thyroid state in rabbits. J Physiol (Lond) 228:563–582
Swynghedauw B (1986) Developmental and functional adaptation of contractile proteins in cardiac and skeletal muscles. Physiol Rev 66:710–771
Wei JY, Spurgeon HA, Lakatta EG (1982) Electromechanical responsiveness of hyperthyroid cardiac muscle to beta-adrenergic stimulation. Am J Physiol 243:E114-E122
Yazaki Y, Raben MS (1975) Effect of the thyroid state on the enzymatic characteristics of cardiac myosin. A difference in behaviour of rat and rabbit cardiac muscle. Circ Res 36:208–215
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cappelli, V., Moggio, R., Polla, B. et al. The dual effect of thyroid hormones on contractile properties of rat myocardium. Pflugers Arch. 411, 620–627 (1988). https://doi.org/10.1007/BF00580857
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00580857