Summary
Thyroid hormones (TH) have previously been shown to alter the force and velocity of cardiac muscle contractions. To investigate the mechanism responsible for these alterations, excess amounts of thyroxine (T4, 1μM) were applied on rat heart cells grown in cell culture. We found the following biochemical alterations: a) 40% decrease in the myoglobin content within 2 days; b) 25% increase in the rate of Ca-uptake into sacroplasmic reticulum (SR) in myocytes following chemical skinning; and c) a two-fold increase in Na−K-ATPase activity measured by86Rb-uptake. These changes support our hypothesis that TH induce the transition of slow-twitch (“red”) muscles towards the fast-twitch (“white”) muscle type. This may explain the changes in contractile activity known to occur under TH influence.
Similar content being viewed by others
References
Binah O, Rubinstein E, Gilat E (1987) Effect of thyroid hormone on the action potential and membrane currents of guinea pig ventricular myocytes. Pflügers Arch 409:214–216
Briggs FN, Poland JL, Solaro RJ (1977) Relative capabilities of sarcoplasmic reticulum in fast and slow mammalian skeletal muscles. J Physiol (Lond) 266:587–594
Brik H, Gamliel A, Shainberg A (1989) Characterization of sarcoplasmic reticulum in skinned muscle cultures. Biochim Biophys Acta 980:273–280
Buccino RA, Spann JF Jr, Pool PE, Sonnenblick EH, Braunwald E (1967) Influence of the thyroid state on the intrinsic contractile properties and energy stores of the myocardium. J Clin Invest 46:1669–1682
Capelli V, Moggio R, Polla B, Bottinelli R, Pogesi C, Reggiani C (1988) The dual effect of thyroid hormones on contractile properties of rat myocardium. Pflügers Arch 411:620–627
Caroni P, Carafoli E (1981) The Ca2+ pumping ATPase of heart sarcolemma characterization, calmodulin dependence, and partial purification. J Biol Chem 256:3263–3270
Carter WJ, Benjamin WS, Faas FH (1982) Effect of experimental hyperthyroidism on protein turnover in skeletal and cardiac muscle as measured by14C-tyrosine infusion. Biochem J 204:69–74
Chuch SH, Mullancy JM, Ghosh TK, Zachaky AL, Gill D (1987) GTP- and inositol 1,4,5-triphosphate-activated intracellular calcium movements in neuronal and smooth muscle cell lines. J Biol Chem 262:13857–13864
Conway G, Heazlitt RA, Fowler NO, Gabel M, Green S (1976) The effect of hyperthyroidism on the sarcoplasmic reticulum and myosin ATPase of dog heart. J Mol Cell Cardiol 8:39–51
Curfman GD, Crowley TJ, Smith TW (1979) Thyroid-induced alterations in myocardial sodium and potassium-activated adenosine triphosphatase, monovalent cation active transport, and cardiac glycoside binding. J Clin Invest 59:586–590
Davis PJ, Blas SD (1981) In vitro stimulation of human red blood cell Ca2+-ATPase by thyroid hormone. Biochem Biophys Res Comm 99:1073–1080
Djaldetti M, Gilgal R, Shainberg A, Klein B, Zahavi I (1988) EM observations on the effect of anthracycline drugs in cultured newborn rat cardiomyocytes. Basic Res Cardiol 83:672–677
Endo M (1977) Calcium release from the sarcoplasmic reticulum. Physiol Rev 57:71–108
Endo M, Iioni M (1980) Specific perforation of muscle cell membranes with preserved SR function by saponin treatment. J Musel Res and Cell Motility 1:89–100
Erdmann E, Brown L, Werdan K, Berger H (1987) Multiple forms of the cardiac glycoside receptor with different affinities for cardiac glycosides. In: Beamish RE, Panagia V, Dhalla NS (eds) Pharmacological aspects of heart disease: M Nijhoff Publishing, Boston, pp 261–271
Everts ME, Clausen T (1986) Effects of thyroid hormones on calcium contents and45Ca-exchange in rat skeletal muscle. Am J Physiol 251:E258-E265
Fiehn W, Peter JB (1971) Properties of the fragmented sarcoplasmic reticulum from fast twitch and slow twitch muscles. J Clin Invest 50:570–573
Flink IL, Rader JH, Morkin E (1979) Thyroid hormone stimulates synthesis of a cardiac myosin isozyme. Comparison of the two-dimensional electrophoretic patterns of the cyanogen bromide peptides of cardiac myosin heavy chains from euthyroid and thyrotoxic rabbits. J Biol Chem 254:3105–3110
Gold HK, Spann JF, Braunwald E (1970) Effect of alterations in the thyroid state on the intrinsic contractile properties of isolated rat skeletal muscle. J Clin Invest 49:849–854
Goodkind MJ, Damback GE, Thyrum PT, Luchi RJ (1974) Effect of thyroxine on ventricular myocardial contractility and ATPase activity in guinea pigs. Am J Physiol 226:66–72
Grossman W, Rubin NL, Johnson CW (1971) The enhanced myocardial contractility of thyrotoxicosis. Ann Intern Med 74:869–874
Hasselbach W (1964) Relaxing factor and the relaxation of muscle. Prog Biophys Mol Biol 14:167–222
Hirata M, Koga T (1982) ATP-dependent Ca2+ accumulation in intracellular membranes of guinea pig macrophages after saponin treatment. Biochem Biophys Res Commun 104:1544–1549
Hoh JFY, McGrath PA, Hale PT (1978) Electrophoretic analysis of multiple forms of rat cardiac myosin: effects of hypophysectomy and thyroid replacement. J Mol Cell Cardiol 10:1053–1076
Ianuzzo CD, Patel P, Chen V, O'Brien P (1980) A possible thyroidal trophic influence on fast and slow skeletal muscle myosin. In: Pette D (ed) Plasticity of Muscle: Walter de Gruyter, Berlin New York, pp 593–605
Kessler-Ieekson G (1988) Effect of triiodothyronine on cultured neonatal rat heart cells: beating rate, myosin subunits and CK isozymes. J Molec Cell Cardiol 20:649–655
Kim HD, Witmann FAJ, Fitts RH (1981) A comparison of sarcoplasmic reticulum function in fast and slow skeletal muscle using crude homogenate and isolated vesicles. Life Sci 28:2223–2229
Kim D, Smith TW (1984) Effects of thyroid hormone on sodium pump sites, sodium content and contractile response to cardiac glycosides in cultured chick ventricular cells. J Clin Invest 74:1481–1488
Kim D, Smith TW (1985) Effects of thyroid hormone on calcium handling in cultured chick ventricular cells. J Physiol (Lond.) 364:131–149
Kim D, Smith TW, Marsh JD (1987) Effect of thyroid hormone on slow calcium channel function in cultured chick ventricular cells. J Clin Invest 80:88–94
Kjeldsen K, Everts EM, Clausen T (1986) The effects of thyroid hormones in3H-ouabain binding site concentration, Na, K-contents and86-Rb-efflux in rat skeletal muscle. Pflügers Arch 406:529–535
Limas CJ (1986) Calcium transport by the cardiac sarcoplasmic reticulum in different functional states. In: Rupp H (ed) The Regulation of Heart Function Basic Concepts and Clinical Applications. Thieme, New York, pp 145–148
Ling E, O'Brien PJ, Slaerno T, Ianuzzo CD (1988) Effects of different thyroid treatments on the biochemical characteristics of rabbit myocardium. Can J Cardiol 4:301–306
Lowry OH, Rosebrough NJ, Farr AL, Randal RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Martonosi A, Roufa D, Boland R, Keyes E, Tillack TW (1977) Development of sarcoplasmic reticulum in cultured chicken muscle. J Biol Chem 252:318–332
Morkin C, Flinik IL, Goldman S (1983) Biochemical and physiological effects of thyroid hormone on cardiac performance. Prog Cardiovasc Dis 25:435–464
Morrison GR (1965) Fluorometric microdetermination of heme protein. Anal Chem 37:1124–1127
Nwoye L, Mommaerts WFHM, Simpson DR, Seraydarian K, Marusich M (1982) Evidence for a direct action of thyroid hormone in specifying muscle properties. Am J Physiol 242:R401-R408
Oppenheimer JH (1979) Thyroid hormone action at the cellular level. Science 203:971–979
Philipson KD, Edelman IS (1977) Thyroid hormone control of Na+−K+-ATPase and K+-dependent phosphatase in rat heart. Am J Physiol 232:C196-C201
Rodgers RS, Black S, Katz S, McNeil JH (1986) Thyroidectomy of SHR: effects on ventricular relaxation and on SR calcium uptake activity. Am J Physiol 250:H861-H865
Rudinger A, Mylotte KM, Davis PJ, Blas SD (1984) Rabbit myocardial membrane Ca2+-adenosine triphosphatase activity: Stimulation in vitro by thyroid hormone. Arch Biochem Biophys 229:379–385
Rupp H, Jacob R (1986) Myocardial transitions between fast and slow-type muscles as monitored by the population of myosin isoenzymes. In: Rupp H (ed) The Regulation of Heart Function Basic Concepts and Clinical Applications. Thieme, New York, pp 271–291
Seeman P (1967) Transient holes in the erythrocyte membrane during hypotonic hemolysis and stable holes in the membrane after lysis by saponin and lysolecithin. J Cell Biol 32:55–70
Shainberg A, Yagil G, Yaffe D (1971) Alteration of enzymatic activities during muscle differentiation in vitro. Develop Biol 25:1–29
Shainberg A, Brik H, Bar-Shavit R, Sampson SR (1984) Inhibition of acetylcholine receptor synthesis by thyroid hormones. J Endocr 101:141–147
Simonides WS, Hardeveld C Van (1985) The effect of hypothyroidism on sarcoplasmic reticulum in fast twitch muscle of the rat. Biochim Biophys Acta 844:129–141
Suko J (1971) Alterations of Ca2+-activated ATPase of cardiac sarcoplasmic reticulum in hyper- and hypothyroidism. Biochim Biophys Acta 252:324–327
Suko J (1973) The calcium pump of cardiac sarcoploasmic reticulum Functional alterations of different levels of thyroid state in rabbits. J Physiol (Lond.) 228:563–581
Tada M, Yasmamoto T, Tonomura Y (1978) Molecular mechanism of active calcium transport by sarcoplasmic reticulum. Physiol Rev 58:1–79
Vale MGP, Carvalho AP (1973) Effects of Ruthenium red on Ca2+ uptake and ATPase of sarcoplasmic reticulum of rabbit skeletal muscle. Biochem Biophys Acta 325:29–37
Winder WW, Holloszy JO (1977) Response of mitochondria of different types of skeletal muscle to thyrotoxicosis. Am J Physiol 232:C180-C184
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Brik, H., Shainberg, A. Thyroxine induces transition of red towards white muscle in cultured heart cells. Basic Res Cardiol 85, 237–246 (1990). https://doi.org/10.1007/BF01907112
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF01907112