Abstract
1. Species differences in the activity of the exchanger were evaluated in isolated myocytes from rat, guinea-pig, hamster ventricles and human atria. Fluorescence measurements using fura-2 were carried out in conjunction with the whole-cell patch-clamp technique for simultaneous recording of membrane currents and intracellular Ca2+ concentration. 2. Ca2+ release from sarcoplasmic reticulum (SR) induced either by rapid application of caffeine or by Ca2+ current elicited inward Na(+)-Ca2+ exchange currents (INa-Ca). The magnitude of INa-Ca was largest in hamster, smallest in rat, with guinea-pig and human myocytes having intermediate values. The ratio of caffeine-induced exchanger current densities, normalized with respect to the peak Ca2+ release, was 4:2:1.5:1 for hamster > guinea-pig > or = human > or = rat myocytes. 3. The rates of Ca2+ removal in the presence of caffeine, which reflect primarily the Ca2+ extruding activity of the Na(+)-Ca2+ exchanger, followed the same order of hamster > guinea-pig > or = human > or = rat. 4. The kinetics of INa-Ca vs. Ca2+ transients were different among species. In rat myocytes, the kinetics of the INa-Ca and the Ca2+ transients were similar, with INa-Ca linearly proportional to intracellular Ca2+ concentration ([Ca2+]i). In hamster myocytes, the time course of INa-Ca tracked only the declining phase of the Ca2+ transient with INa-Ca having faster kinetics during the Ca2+ release. These findings suggest that the Ca2+ concentrations in the vicinity of the exchanger were significantly higher than those of the cytosol during Ca2+ release in hamster myocytes. 5. We concluded that there are significant species differences in the exchanger activity of cardiac myocytes, arising from differences in exchanger densities, their modulation and/or their spatial distribution with respect to the ryanodine receptors of cardiac myocytes.
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- Bassani J. W., Bassani R. A., Bers D. M. Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol. 1994 Apr 15;476(2):279–293. doi: 10.1113/jphysiol.1994.sp020130. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baylor S. M., Hollingworth S. Fura-2 calcium transients in frog skeletal muscle fibres. J Physiol. 1988 Sep;403:151–192. doi: 10.1113/jphysiol.1988.sp017244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berlin J. R., Konishi M. Ca2+ transients in cardiac myocytes measured with high and low affinity Ca2+ indicators. Biophys J. 1993 Oct;65(4):1632–1647. doi: 10.1016/S0006-3495(93)81211-6. [DOI] [PMC free article] [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. Species differences and the role of sodium-calcium exchange in cardiac muscle relaxation. Ann N Y Acad Sci. 1991;639:375–385. doi: 10.1111/j.1749-6632.1991.tb17326.x. [DOI] [PubMed] [Google Scholar]
- Beuckelmann D. J., Wier W. G. Sodium-calcium exchange in guinea-pig cardiac cells: exchange current and changes in intracellular Ca2+. J Physiol. 1989 Jul;414:499–520. doi: 10.1113/jphysiol.1989.sp017700. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bouchard R. A., Clark R. B., Giles W. R. Regulation of unloaded cell shortening by sarcolemmal sodium-calcium exchange in isolated rat ventricular myocytes. J Physiol. 1993 Sep;469:583–599. doi: 10.1113/jphysiol.1993.sp019831. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bouchard R. A., Clark R. B., Giles W. R. Role of sodium-calcium exchange in activation of contraction in rat ventricle. J Physiol. 1993 Dec;472:391–413. doi: 10.1113/jphysiol.1993.sp019953. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bridge J. H., Smolley J. R., Spitzer K. W. The relationship between charge movements associated with ICa and INa-Ca in cardiac myocytes. Science. 1990 Apr 20;248(4953):376–378. doi: 10.1126/science.2158147. [DOI] [PubMed] [Google Scholar]
- Callewaert G., Cleemann L., Morad M. Caffeine-induced Ca2+ release activates Ca2+ extrusion via Na+-Ca2+ exchanger in cardiac myocytes. Am J Physiol. 1989 Jul;257(1 Pt 1):C147–C152. doi: 10.1152/ajpcell.1989.257.1.C147. [DOI] [PubMed] [Google Scholar]
- Campbell D. L., Giles W. R., Robinson K., Shibata E. F. Studies of the sodium-calcium exchanger in bull-frog atrial myocytes. J Physiol. 1988 Sep;403:317–340. doi: 10.1113/jphysiol.1988.sp017251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cleemann L., Morad M. Role of Ca2+ channel in cardiac excitation-contraction coupling in the rat: evidence from Ca2+ transients and contraction. J Physiol. 1991 Jan;432:283–312. doi: 10.1113/jphysiol.1991.sp018385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Egan T. M., Noble D., Noble S. J., Powell T., Spindler A. J., Twist V. W. Sodium-calcium exchange during the action potential in guinea-pig ventricular cells. J Physiol. 1989 Apr;411:639–661. doi: 10.1113/jphysiol.1989.sp017596. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Egan T. M., Noble D., Noble S. J., Powell T., Spindler A. J., Twist V. W. Sodium-calcium exchange during the action potential in guinea-pig ventricular cells. J Physiol. 1989 Apr;411:639–661. doi: 10.1113/jphysiol.1989.sp017596. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Escande D., Loisance D., Planche C., Coraboeuf E. Age-related changes of action potential plateau shape in isolated human atrial fibers. Am J Physiol. 1985 Oct;249(4 Pt 2):H843–H850. doi: 10.1152/ajpheart.1985.249.4.H843. [DOI] [PubMed] [Google Scholar]
- Fabiato A., Fabiato F. Calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cells from adult human, dog, cat, rabbit, rat, and frog hearts and from fetal and new-born rat ventricles. Ann N Y Acad Sci. 1978 Apr 28;307:491–522. doi: 10.1111/j.1749-6632.1978.tb41979.x. [DOI] [PubMed] [Google Scholar]
- Frank J. S., Mottino G., Reid D., Molday R. S., Philipson K. D. Distribution of the Na(+)-Ca2+ exchange protein in mammalian cardiac myocytes: an immunofluorescence and immunocolloidal gold-labeling study. J Cell Biol. 1992 Apr;117(2):337–345. doi: 10.1083/jcb.117.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Giles W., Shimoni Y. Comparison of sodium-calcium exchanger and transient inward currents in single cells from rabbit ventricle. J Physiol. 1989 Oct;417:465–481. doi: 10.1113/jphysiol.1989.sp017813. [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]
- Hatem S. N., Sham J. S., Morad M. Enhanced Na(+)-Ca2+ exchange activity in cardiomyopathic Syrian hamster. Circ Res. 1994 Feb;74(2):253–261. doi: 10.1161/01.res.74.2.253. [DOI] [PubMed] [Google Scholar]
- Hilgemann D. W., Collins A. Mechanism of cardiac Na(+)-Ca2+ exchange current stimulation by MgATP: possible involvement of aminophospholipid translocase. J Physiol. 1992 Aug;454:59–82. doi: 10.1113/jphysiol.1992.sp019254. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hilgemann D. W., Nicoll D. A., Philipson K. D. Charge movement during Na+ translocation by native and cloned cardiac Na+/Ca2+ exchanger. Nature. 1991 Aug 22;352(6337):715–718. doi: 10.1038/352715a0. [DOI] [PubMed] [Google Scholar]
- Isenberg G., Klockner U. Calcium tolerant ventricular myocytes prepared by preincubation in a "KB medium". Pflugers Arch. 1982 Oct;395(1):6–18. doi: 10.1007/BF00584963. [DOI] [PubMed] [Google Scholar]
- Kieval R. S., Bloch R. J., Lindenmayer G. E., Ambesi A., Lederer W. J. Immunofluorescence localization of the Na-Ca exchanger in heart cells. Am J Physiol. 1992 Aug;263(2 Pt 1):C545–C550. doi: 10.1152/ajpcell.1992.263.2.C545. [DOI] [PubMed] [Google Scholar]
- Kimura J., Noma A., Irisawa H. Na-Ca exchange current in mammalian heart cells. Nature. 1986 Feb 13;319(6054):596–597. doi: 10.1038/319596a0. [DOI] [PubMed] [Google Scholar]
- Kohomoto O., Levi A. J., Bridge J. H. Relation between reverse sodium-calcium exchange and sarcoplasmic reticulum calcium release in guinea pig ventricular cells. Circ Res. 1994 Mar;74(3):550–554. doi: 10.1161/01.res.74.3.550. [DOI] [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]
- Levi A. J., Spitzer K. W., Kohmoto O., Bridge J. H. Depolarization-induced Ca entry via Na-Ca exchange triggers SR release in guinea pig cardiac myocytes. Am J Physiol. 1994 Apr;266(4 Pt 2):H1422–H1433. doi: 10.1152/ajpheart.1994.266.4.H1422. [DOI] [PubMed] [Google Scholar]
- Lipp P., Pott L., Callewaert G., Carmeliet E. Simultaneous recording of Indo-1 fluorescence and Na+/Ca2+ exchange current reveals two components of Ca2(+)-release from sarcoplasmic reticulum of cardiac atrial myocytes. FEBS Lett. 1990 Nov 26;275(1-2):181–184. doi: 10.1016/0014-5793(90)81467-3. [DOI] [PubMed] [Google Scholar]
- Mitra R., Morad M. A uniform enzymatic method for dissociation of myocytes from hearts and stomachs of vertebrates. Am J Physiol. 1985 Nov;249(5 Pt 2):H1056–H1060. doi: 10.1152/ajpheart.1985.249.5.H1056. [DOI] [PubMed] [Google Scholar]
- Niggli E., Lederer W. J. Molecular operations of the sodium-calcium exchanger revealed by conformation currents. Nature. 1991 Feb 14;349(6310):621–624. doi: 10.1038/349621a0. [DOI] [PubMed] [Google Scholar]
- Noma A., Shioya T., Paver L. F., Twist V. W., Powell T. Cytosolic free Ca2+ during operation of sodium-calcium exchange in guinea-pig heart cells. J Physiol. 1991 Oct;442:257–276. doi: 10.1113/jphysiol.1991.sp018792. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Näbauer M., Morad M. Modulation of contraction by intracellular Na+ via Na(+)-Ca2+ exchange in single shark (Squalus acanthias) ventricular myocytes. J Physiol. 1992 Nov;457:627–637. doi: 10.1113/jphysiol.1992.sp019398. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sham J. S., Cleemann L., Morad M. Functional coupling of Ca2+ channels and ryanodine receptors in cardiac myocytes. Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):121–125. doi: 10.1073/pnas.92.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sham J. S., Cleemann L., Morad M. Gating of the cardiac Ca2+ release channel: the role of Na+ current and Na(+)-Ca2+ exchange. Science. 1992 Feb 14;255(5046):850–853. doi: 10.1126/science.1311127. [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]