Abstract
The roles of the sarcoplasmic reticulum (SR) Ca(2+)-ATPase and Na(+)-Ca2+ exchange in Ca2+ removal from cytosol were compared in isolated rabbit and rat ventricular myocytes during caffeine contractures and electrically stimulated twitches. Cell shortening and intracellular calcium concentration ([Ca2+]i) were measured in indo-1-loaded cells. Na(+)-Ca2+ exchange was inhibited by replacement of external Na+ by Li+. To avoid net changes in cell or SR Ca2+ load during a twitch in 0 Na+ solution, intracellular Na+ (Na+i) was depleted using a long pre-perfusion with 0 Na+, 0 Ca2+ solution. SR Ca2+ accumulation was inhibited by caffeine or thapsigargin (TG). Relaxation of steady-state twitches was 2-fold faster in rat than in rabbit (before and after Na+i depletion). In contrast, caffeine contractures (where SR Ca2+ accumulation is inhibited), relaxed faster in rabbit cells. Removal of external Na+ increased the half-time for relaxation of caffeine contractures 15- and 5-fold in rabbit and rat myocytes respectively (and increased contracture amplitude in rabbit cells only). The time course of relaxation in 0 Na+, 0 Ca2+ solution was similar in the two species. Inhibition of the Na(+)-Ca2+ exchange during a twitch increased the [Ca2+]i transient amplitude (delta[Ca2+]i) by 50% and the time constant of [Ca2+]i decline (tau) by 45% in rabbit myocytes. A smaller increase in tau (20%) and no change in delta[Ca2+]i were observed in rat cells in 0 Na+ solution. [Ca2+]i transients remained more rapid in rat cells. Inhibition of the SR Ca(2+)-ATPase during a twitch enhanced delta[Ca2+]i by 25% in both species. The increase in tau after TG exposure was greater in rat (9-fold) than in rabbit myocytes (2-fold), which caused [Ca2+]i decline to be 70% slower in rat compared with rabbit cells. The time course of [Ca2+]i decline during twitch in TG-treated cells was similar to that during caffeine application in control cells. Combined inhibition of these Ca2+ transport systems markedly slowed the time course of [Ca2+]i decline, so that tau was virtually the same in both species and comparable to that during caffeine application in 0 Na+, 0 Ca2+ solution. Thus, the combined participation of slow Ca2+ transport mechanisms (mitochondrial Ca2+ uptake and sarcolemmal Ca(2+)-ATPase) is similar in these species. We conclude that during the decline of the [Ca2+]i transient, the Na(+)-Ca2+ exchange is about 2- to 3-fold faster in rabbit than in rat, whereas the SR Ca(2+)-ATPase is 2- to 3-fold faster in the rat.(ABSTRACT TRUNCATED AT 400 WORDS)
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bassani J. W., Bassani R. A., Bers D. M. Ca2+ cycling between sarcoplasmic reticulum and mitochondria in rabbit cardiac myocytes. J Physiol. 1993 Jan;460:603–621. doi: 10.1113/jphysiol.1993.sp019489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bassani J. W., Bassani R. A., Bers D. M. Twitch-dependent SR Ca accumulation and release in rabbit ventricular myocytes. Am J Physiol. 1993 Aug;265(2 Pt 1):C533–C540. doi: 10.1152/ajpcell.1993.265.2.C533. [DOI] [PubMed] [Google Scholar]
- Bassani R. A., Bassani J. W., Bers D. M. Mitochondrial and sarcolemmal Ca2+ transport reduce [Ca2+]i during caffeine contractures in rabbit cardiac myocytes. J Physiol. 1992;453:591–608. doi: 10.1113/jphysiol.1992.sp019246. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bean B. P., Rios E. Nonlinear charge movement in mammalian cardiac ventricular cells. Components from Na and Ca channel gating. J Gen Physiol. 1989 Jul;94(1):65–93. doi: 10.1085/jgp.94.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bers D. M., Bassani R. A., Bassani J. W., Baudet S., Hryshko L. V. Paradoxical twitch potentiation after rest in cardiac muscle: increased fractional release of SR calcium. J Mol Cell Cardiol. 1993 Sep;25(9):1047–1057. doi: 10.1006/jmcc.1993.1117. [DOI] [PubMed] [Google Scholar]
- Bers D. M., Bridge J. H. Relaxation of rabbit ventricular muscle by Na-Ca exchange and sarcoplasmic reticulum calcium pump. Ryanodine and voltage sensitivity. Circ Res. 1989 Aug;65(2):334–342. doi: 10.1161/01.res.65.2.334. [DOI] [PubMed] [Google Scholar]
- Bers D. M., Bridge J. H., Spitzer K. W. Intracellular Ca2+ transients during rapid cooling contractures in guinea-pig ventricular myocytes. J Physiol. 1989 Oct;417:537–553. doi: 10.1113/jphysiol.1989.sp017817. [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]
- Bers D. M., Christensen D. M., Nguyen T. X. Can Ca entry via Na-Ca exchange directly activate cardiac muscle contraction? J Mol Cell Cardiol. 1988 May;20(5):405–414. doi: 10.1016/s0022-2828(88)80132-9. [DOI] [PubMed] [Google Scholar]
- Bers D. M., Lederer W. J., Berlin J. R. Intracellular Ca transients in rat cardiac myocytes: role of Na-Ca exchange in excitation-contraction coupling. Am J Physiol. 1990 May;258(5 Pt 1):C944–C954. doi: 10.1152/ajpcell.1990.258.5.C944. [DOI] [PubMed] [Google Scholar]
- Beuckelmann D. J., Wier W. G. Mechanism of release of calcium from sarcoplasmic reticulum of guinea-pig cardiac cells. J Physiol. 1988 Nov;405:233–255. doi: 10.1113/jphysiol.1988.sp017331. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bridge J. H., Spitzer K. W., Ershler P. R. Relaxation of isolated ventricular cardiomyocytes by a voltage-dependent process. Science. 1988 Aug 12;241(4867):823–825. doi: 10.1126/science.3406740. [DOI] [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]
- Crespo L. M., Grantham C. J., Cannell M. B. Kinetics, stoichiometry and role of the Na-Ca exchange mechanism in isolated cardiac myocytes. Nature. 1990 Jun 14;345(6276):618–621. doi: 10.1038/345618a0. [DOI] [PubMed] [Google Scholar]
- Fabiato A. Calcium release in skinned cardiac cells: variations with species, tissues, and development. Fed Proc. 1982 May;41(7):2238–2244. [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. Time and calcium dependence of activation and inactivation of calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985 Feb;85(2):247–289. doi: 10.1085/jgp.85.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
- Horackova M. Possible role of Na(+)-Ca2+ exchange in the regulation of contractility in isolated adult ventricular myocytes from rat and guinea pig. Can J Physiol Pharmacol. 1989 Dec;67(12):1525–1533. doi: 10.1139/y89-246. [DOI] [PubMed] [Google Scholar]
- Hove-Madsen L., Bers D. M. Passive Ca buffering and SR Ca uptake in permeabilized rabbit ventricular myocytes. Am J Physiol. 1993 Mar;264(3 Pt 1):C677–C686. doi: 10.1152/ajpcell.1993.264.3.C677. [DOI] [PubMed] [Google Scholar]
- Hove-Madsen L., Bers D. M. Sarcoplasmic reticulum Ca2+ uptake and thapsigargin sensitivity in permeabilized rabbit and rat ventricular myocytes. Circ Res. 1993 Nov;73(5):820–828. doi: 10.1161/01.res.73.5.820. [DOI] [PubMed] [Google Scholar]
- Hryshko L. V., Stiffel V., Bers D. M. Rapid cooling contractures as an index of sarcoplasmic reticulum calcium content in rabbit ventricular myocytes. Am J Physiol. 1989 Nov;257(5 Pt 2):H1369–H1377. doi: 10.1152/ajpheart.1989.257.5.H1369. [DOI] [PubMed] [Google Scholar]
- Josephson I. R., Sanchez-Chapula J., Brown A. M. A comparison of calcium currents in rat and guinea pig single ventricular cells. Circ Res. 1984 Feb;54(2):144–156. doi: 10.1161/01.res.54.2.144. [DOI] [PubMed] [Google Scholar]
- Kirby M. S., Sagara Y., Gaa S., Inesi G., Lederer W. J., Rogers T. B. Thapsigargin inhibits contraction and Ca2+ transient in cardiac cells by specific inhibition of the sarcoplasmic reticulum Ca2+ pump. J Biol Chem. 1992 Jun 25;267(18):12545–12551. [PubMed] [Google Scholar]
- Leblanc N., Hume J. R. Sodium current-induced release of calcium from cardiac sarcoplasmic reticulum. Science. 1990 Apr 20;248(4953):372–376. doi: 10.1126/science.2158146. [DOI] [PubMed] [Google Scholar]
- Lewartowski B., Hansford R. G., Langer G. A., Lakatta E. G. Contraction and sarcoplasmic reticulum Ca2+ content in single myocytes of guinea pig heart: effect of ryanodine. Am J Physiol. 1990 Oct;259(4 Pt 2):H1222–H1229. doi: 10.1152/ajpheart.1990.259.4.H1222. [DOI] [PubMed] [Google Scholar]
- Lewartowski B., Wolska B. M. The effect of thapsigargin on sarcoplasmic reticulum Ca2+ content and contractions in single myocytes of guinea-pig heart. J Mol Cell Cardiol. 1993 Jan;25(1):23–29. doi: 10.1006/jmcc.1993.1004. [DOI] [PubMed] [Google Scholar]
- Mitchell M. R., Powell T., Terrar D. A., Twist V. W. Electrical activity and contraction in cells isolated from rat and guinea-pig ventricular muscle: a comparative study. J Physiol. 1987 Oct;391:527–544. doi: 10.1113/jphysiol.1987.sp016754. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Negretti N., O'Neill S. C., Eisner D. A. The relative contributions of different intracellular and sarcolemmal systems to relaxation in rat ventricular myocytes. Cardiovasc Res. 1993 Oct;27(10):1826–1830. doi: 10.1093/cvr/27.10.1826. [DOI] [PubMed] [Google Scholar]
- Näbauer M., Callewaert G., Cleemann L., Morad M. Regulation of calcium release is gated by calcium current, not gating charge, in cardiac myocytes. Science. 1989 May 19;244(4906):800–803. doi: 10.1126/science.2543067. [DOI] [PubMed] [Google Scholar]
- O'Neill S. C., Valdeolmillos M., Lamont C., Donoso P., Eisner D. A. The contribution of Na-Ca exchange to relaxation in mammalian cardiac muscle. Ann N Y Acad Sci. 1991;639:444–452. doi: 10.1111/j.1749-6632.1991.tb17331.x. [DOI] [PubMed] [Google Scholar]
- Rousseau E., Meissner G. Single cardiac sarcoplasmic reticulum Ca2+-release channel: activation by caffeine. Am J Physiol. 1989 Feb;256(2 Pt 2):H328–H333. doi: 10.1152/ajpheart.1989.256.2.H328. [DOI] [PubMed] [Google Scholar]
- Shattock M. J., Bers D. M. Inotropic response to hypothermia and the temperature-dependence of ryanodine action in isolated rabbit and rat ventricular muscle: implications for excitation-contraction coupling. Circ Res. 1987 Dec;61(6):761–771. doi: 10.1161/01.res.61.6.761. [DOI] [PubMed] [Google Scholar]
- Shattock M. J., Bers D. M. Rat vs. rabbit ventricle: Ca flux and intracellular Na assessed by ion-selective microelectrodes. Am J Physiol. 1989 Apr;256(4 Pt 1):C813–C822. doi: 10.1152/ajpcell.1989.256.4.C813. [DOI] [PubMed] [Google Scholar]
- Sutko J. L., Willerson J. T. Ryanodine alteration of the contractile state of rat ventricular myocardium. Comparison with dog, cat, and rabbit ventricular tissues. Circ Res. 1980 Mar;46(3):332–343. doi: 10.1161/01.res.46.3.332. [DOI] [PubMed] [Google Scholar]
- Varro A., Negretti N., Hester S. B., Eisner D. A. An estimate of the calcium content of the sarcoplasmic reticulum in rat ventricular myocytes. Pflugers Arch. 1993 Apr;423(1-2):158–160. doi: 10.1007/BF00374975. [DOI] [PubMed] [Google Scholar]
- Vetter R., Kemsies C., Schulze W. Sarcolemmal Na+-Ca2+ exchange and sarcoplasmic reticulum Ca2+ uptake in several cardiac preparations. Biomed Biochim Acta. 1987;46(8-9):S375–S381. [PubMed] [Google Scholar]
- Wendt I. R., Stephenson D. G. Effects of caffeine on Ca-activated force production in skinned cardiac and skeletal muscle fibres of the rat. Pflugers Arch. 1983 Aug;398(3):210–216. doi: 10.1007/BF00657153. [DOI] [PubMed] [Google Scholar]
- Wier W. G. Cytoplasmic [Ca2+] in mammalian ventricle: dynamic control by cellular processes. Annu Rev Physiol. 1990;52:467–485. doi: 10.1146/annurev.ph.52.030190.002343. [DOI] [PubMed] [Google Scholar]
- Wrzosek A., Schneider H., Grueninger S., Chiesi M. Effect of thapsigargin on cardiac muscle cells. Cell Calcium. 1992 May;13(5):281–292. doi: 10.1016/0143-4160(92)90063-x. [DOI] [PubMed] [Google Scholar]