Abstract
Sarcomere length measurement by microscopic and laser diffraction techniques in trabeculae of rat heart, superfused with Krebs-Henseleit solution at 21 degrees C, showed spontaneous local sarcomere shortening after electrically stimulated twitches. The contractions originated in a region of several hundred micrometers throughout the width of the muscle close to the end of the preparation that was damaged by dissection. The contractions propagated at a constant velocity along the trabeculae. The velocity of propagation increased from 0 to 10 mm/s in proportion to the number of stimuli (3-30) in a train of electrically evoked twitches at 2 Hz and at an external calcium ion concentration ([Ca++]o) of 1.5 mM. At a constant number of stimuli (n), the velocity of propagation increased from 0 to 15 mm/s with [Ca++]o increasing from 1 to 7 mM. In addition, increase of n and [Ca++]o led to an increase of the extent of local sarcomere shortening during the spontaneous contractions, and the occurrence of multiple contractions. Spontaneous contractions with much internal shortening and a high velocity of propagation frequently induced spontaneous synchronized contractions and eventually arrhythmias. Propagation of spontaneous contractions at low and variable velocity is consistent with the hypothesis that calcium leakage into damaged cells causes spontaneous calcium release from the overloaded sarcoplasmic reticulum in the damaged cells. This process propagates as a result of diffusion of calcium into adjacent cells, which triggers calcium release from their sarcoplasmic reticulum. We postulate that the propagation velocity depends on the intracellular calcium ion concentration, with increases with n and [Ca++]o.
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- Allen D. G., Eisner D. A., Orchard C. H. Characterization of oscillations of intracellular calcium concentration in ferret ventricular muscle. J Physiol. 1984 Jul;352:113–128. doi: 10.1113/jphysiol.1984.sp015281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Allen D. G., Eisner D. A., Pirolo J. S., Smith G. L. The relationship between intracellular calcium and contraction in calcium-overloaded ferret papillary muscles. J Physiol. 1985 Jul;364:169–182. doi: 10.1113/jphysiol.1985.sp015737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aronson R. S. Afterpotentials and triggered activity in hypertrophied myocardium from rats with renal hypertension. Circ Res. 1981 May;48(5):720–727. doi: 10.1161/01.res.48.5.720. [DOI] [PubMed] [Google Scholar]
- Backx P. H., de Tombe P. P., Van Deen J. H., Mulder B. J., ter Keurs H. E. A model of propagating calcium-induced calcium release mediated by calcium diffusion. J Gen Physiol. 1989 May;93(5):963–977. doi: 10.1085/jgp.93.5.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bers D. M. Ca influx and sarcoplasmic reticulum Ca release in cardiac muscle activation during postrest recovery. Am J Physiol. 1985 Mar;248(3 Pt 2):H366–H381. doi: 10.1152/ajpheart.1985.248.3.H366. [DOI] [PubMed] [Google Scholar]
- Cannell M. B., Allen D. G. Model of calcium movements during activation in the sarcomere of frog skeletal muscle. Biophys J. 1984 May;45(5):913–925. doi: 10.1016/S0006-3495(84)84238-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Capogrossi M. C., Kort A. A., Spurgeon H. A., Lakatta E. G. Single adult rabbit and rat cardiac myocytes retain the Ca2+- and species-dependent systolic and diastolic contractile properties of intact muscle. J Gen Physiol. 1986 Nov;88(5):589–613. doi: 10.1085/jgp.88.5.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cohen C. J., Fozzard H. A., Sheu S. S. Increase in intracellular sodium ion activity during stimulation in mammalian cardiac muscle. Circ Res. 1982 May;50(5):651–662. doi: 10.1161/01.res.50.5.651. [DOI] [PubMed] [Google Scholar]
- Cranefield P. F. Action potentials, afterpotentials, and arrhythmias. Circ Res. 1977 Oct;41(4):415–423. doi: 10.1161/01.res.41.4.415. [DOI] [PubMed] [Google Scholar]
- Daniels M., Noble M. I., ter Keurs H. E., Wohlfart B. Velocity of sarcomere shortening in rat cardiac muscle: relationship to force, sarcomere length, calcium and time. J Physiol. 1984 Oct;355:367–381. doi: 10.1113/jphysiol.1984.sp015424. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Di Gennaro M., Valle R., Pahor M., Carbonin P. Abolition of digitalis tachyarrhythmias by caffeine. Am J Physiol. 1983 Feb;244(2):H215–H221. doi: 10.1152/ajpheart.1983.244.2.H215. [DOI] [PubMed] [Google Scholar]
- Eisner D. A., Lederer W. J. The role of the sodium pump in the effects of potassium-depleted solutions on mammalian cardiac muscle. J Physiol. 1979 Sep;294:279–301. doi: 10.1113/jphysiol.1979.sp012930. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fabiato A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol. 1983 Jul;245(1):C1–14. doi: 10.1152/ajpcell.1983.245.1.C1. [DOI] [PubMed] [Google Scholar]
- Fabiato A., Fabiato F. Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol. 1975 Aug;249(3):469–495. doi: 10.1113/jphysiol.1975.sp011026. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fabiato A., Fabiato F. Excitation-contraction coupling of isolated cardiac fibers with disrupted or closed sarcolemmas. Calcium-dependent cyclic and tonic contractions. Circ Res. 1972 Sep;31(3):293–307. doi: 10.1161/01.res.31.3.293. [DOI] [PubMed] [Google Scholar]
- Ferrier G. R. The effects of tension on acetylstrophanthidin-induced transient depolarizations and aftercontractions in canine myocardial and Purkinje tissues. Circ Res. 1976 Mar;38(3):156–162. doi: 10.1161/01.res.38.3.156. [DOI] [PubMed] [Google Scholar]
- Gillis J. M., Thomason D., Lefèvre J., Kretsinger R. H. Parvalbumins and muscle relaxation: a computer simulation study. J Muscle Res Cell Motil. 1982 Dec;3(4):377–398. doi: 10.1007/BF00712090. [DOI] [PubMed] [Google Scholar]
- Hiraoka M., Okamoto Y., Sano T. Oscillatory afterpotentials in dog ventricular muscle fibers. Circ Res. 1981 Apr;48(4):510–518. doi: 10.1161/01.res.48.4.510. [DOI] [PubMed] [Google Scholar]
- Housmans P. R., Lee N. K., Blinks J. R. Active shortening retards the decline of the intracellular calcium transient in mammalian heart muscle. Science. 1983 Jul 8;221(4606):159–161. doi: 10.1126/science.6857274. [DOI] [PubMed] [Google Scholar]
- KAUFMANN R., FLECKENSTEIN A., ANTONI H. URSACHEN UND AUSLOESUNGSBEDINGUNGEN VON MYOKARD-KONTRAKTIONEN OHNE REGULAERES AKTIONSPOTENTIAL. Pflugers Arch Gesamte Physiol Menschen Tiere. 1963 Nov 29;278:435–446. [PubMed] [Google Scholar]
- Kass R. S., Lederer W. J., Tsien R. W., Weingart R. Role of calcium ions in transient inward currents and aftercontractions induced by strophanthidin in cardiac Purkinje fibres. J Physiol. 1978 Aug;281:187–208. doi: 10.1113/jphysiol.1978.sp012416. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kass R. S., Tsien R. W. Fluctuations in membrane current driven by intracellular calcium in cardiac Purkinje fibers. Biophys J. 1982 Jun;38(3):259–269. doi: 10.1016/S0006-3495(82)84557-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kort A. A., Lakatta E. G. Calcium-dependent mechanical oscillations occur spontaneously in unstimulated mammalian cardiac tissues. Circ Res. 1984 Apr;54(4):396–404. doi: 10.1161/01.res.54.4.396. [DOI] [PubMed] [Google Scholar]
- Krueger J. W., Pollack G. H. Myocardial sarcomere dynamics during isometric contraction. J Physiol. 1975 Oct;251(3):627–643. doi: 10.1113/jphysiol.1975.sp011112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mary-Rabine L., Hordof A. J., Danilo P., Jr, Malm J. R., Rosen M. R. Mechanisms for impulse initiation in isolated human atrial fibers. Circ Res. 1980 Aug;47(2):267–277. doi: 10.1161/01.res.47.2.267. [DOI] [PubMed] [Google Scholar]
- Matsuda H., Noma A., Kurachi Y., Irisawa H. Transient depolarization and spontaneous voltage fluctuations in isolated single cells from guinea pig ventricles. Calcium-mediated membrane potential fluctuations. Circ Res. 1982 Aug;51(2):142–151. doi: 10.1161/01.res.51.2.142. [DOI] [PubMed] [Google Scholar]
- Morad M., Cleemann L. Role of Ca2+ channel in development of tension in heart muscle. J Mol Cell Cardiol. 1987 Jun;19(6):527–553. doi: 10.1016/s0022-2828(87)80360-7. [DOI] [PubMed] [Google Scholar]
- Pollack G. H. AV nodal transmission: a proposed electromechanical mechanism. J Electrocardiol. 1974;7(3):245–258. doi: 10.1016/s0022-0736(74)80036-1. [DOI] [PubMed] [Google Scholar]
- Ragnarsdóttir K., Wohlfart B., Jóhannsson M. Mechanical restitution of the rat papillary muscle. Acta Physiol Scand. 1982 Jun;115(2):183–191. doi: 10.1111/j.1748-1716.1982.tb07064.x. [DOI] [PubMed] [Google Scholar]
- Schouten V. J., van Deen J. K., de Tombe P., Verveen A. A. Force-interval relationship in heart muscle of mammals. A calcium compartment model. Biophys J. 1987 Jan;51(1):13–26. doi: 10.1016/S0006-3495(87)83307-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stern M. D., Kort A. A., Bhatnagar G. M., Lakatta E. G. Scattered-light intensity fluctuations in diastolic rat cardiac muscle caused by spontaneous Ca++-dependent cellular mechanical oscillations. J Gen Physiol. 1983 Jul;82(1):119–153. doi: 10.1085/jgp.82.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wier W. G., Cannell M. B., Berlin J. R., Marban E., Lederer W. J. Cellular and subcellular heterogeneity of [Ca2+]i in single heart cells revealed by fura-2. Science. 1987 Jan 16;235(4786):325–328. doi: 10.1126/science.3798114. [DOI] [PubMed] [Google Scholar]
- Wohlfart B., Noble M. I. The cardiac excitation-contraction cycle. Pharmacol Ther. 1982;16(1):1–43. doi: 10.1016/0163-7258(82)90030-4. [DOI] [PubMed] [Google Scholar]
- ter Keurs H. E., Backx P. H., de Tombe P. P., Mulder B. J. Aftercontractions and excitation-contraction coupling in rat cardiac muscle. Can J Physiol Pharmacol. 1988 Sep;66(9):1239–1245. doi: 10.1139/y88-204. [DOI] [PubMed] [Google Scholar]
- ter Keurs H. E., Rijnsburger W. H., van Heuningen R., Nagelsmit M. J. Tension development and sarcomere length in rat cardiac trabeculae. Evidence of length-dependent activation. Circ Res. 1980 May;46(5):703–714. doi: 10.1161/01.res.46.5.703. [DOI] [PubMed] [Google Scholar]