Negative control mechanism with features of adaptation controls Ca2+ release in cardiac myocytes (original) (raw)
Abstract
The central paradox of cardiac excitation-contraction coupling is that Ca(2+)-induced Ca2+ release (CICR), an inherently self-regenerating process, is finely graded by surface membrane Ca2+ current (ICa). By using FPL64176, a novel Ca2+ channel agonist that reduces inactivation of ICa, a rapid negative control mechanism was unmasked at the Ca2+ release level in isolated rat ventricular myocytes. This mechanism terminates CICR independently of the duration of trigger ICa and before the sarcoplasmic reticulum becomes depleted of Ca2+. In its ability to be reactivated by incremental increases in trigger ICa, this mechanism differs from conventional inactivation/desensitization and is similar to the mechanism of increment detection or adaptation described for intracellular Ca2+ release channels. These results indicate that ryanodine receptor adaptation regulates Ca2+ release in cardiac muscle, accounting for or contributing to the graded nature of CICR and, additionally, permitting stores to reload at later times during Ca2+ entry.
Selected References
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- 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]
- Cannell M. B., Berlin J. R., Lederer W. J. Effect of membrane potential changes on the calcium transient in single rat cardiac muscle cells. Science. 1987 Dec 4;238(4832):1419–1423. doi: 10.1126/science.2446391. [DOI] [PubMed] [Google Scholar]
- Chamberlain B. K., Volpe P., Fleischer S. Calcium-induced calcium release from purified cardiac sarcoplasmic reticulum vesicles. General characteristics. J Biol Chem. 1984 Jun 25;259(12):7540–7546. [PubMed] [Google Scholar]
- Chu A., Fill M., Stefani E., Entman M. L. Cytoplasmic Ca2+ does not inhibit the cardiac muscle sarcoplasmic reticulum ryanodine receptor Ca2+ channel, although Ca(2+)-induced Ca2+ inactivation of Ca2+ release is observed in native vesicles. J Membr Biol. 1993 Jul;135(1):49–59. doi: 10.1007/BF00234651. [DOI] [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]
- Cohen N. M., Lederer W. J. Changes in the calcium current of rat heart ventricular myocytes during development. J Physiol. 1988 Dec;406:115–146. doi: 10.1113/jphysiol.1988.sp017372. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dettbarn C., Palade P. Arachidonic acid-induced Ca2+ release from isolated sarcoplasmic reticulum. Biochem Pharmacol. 1993 Mar 24;45(6):1301–1309. doi: 10.1016/0006-2952(93)90283-3. [DOI] [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. Use of chlorotetracycline fluorescence to demonstrate Ca2+-induced release of Ca2+ from the sarcoplasmic reticulum of skinned cardiac cells. Nature. 1979 Sep 13;281(5727):146–148. doi: 10.1038/281146a0. [DOI] [PubMed] [Google Scholar]
- Fabiato A. Simulated calcium current can both cause calcium loading in and trigger calcium release from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985 Feb;85(2):291–320. doi: 10.1085/jgp.85.2.291. [DOI] [PMC free article] [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]
- Ferris C. D., Cameron A. M., Huganir R. L., Snyder S. H. Quantal calcium release by purified reconstituted inositol 1,4,5-trisphosphate receptors. Nature. 1992 Mar 26;356(6367):350–352. doi: 10.1038/356350a0. [DOI] [PubMed] [Google Scholar]
- Györke S., Fill M. Ryanodine receptor adaptation: control mechanism of Ca(2+)-induced Ca2+ release in heart. Science. 1993 May 7;260(5109):807–809. doi: 10.1126/science.8387229. [DOI] [PubMed] [Google Scholar]
- Györke S., Palade P. Ca(2+)-dependent negative control mechanism for Ca(2+)-induced Ca2+ release in crayfish muscle. J Physiol. 1994 Apr 15;476(2):315–322. doi: 10.1113/jphysiol.1994.sp020133. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Györke S., Palade P. Role of local Ca2+ domains in activation of Ca(2+)-induced Ca2+ release in crayfish muscle fibers. Am J Physiol. 1993 Jun;264(6 Pt 1):C1505–C1512. doi: 10.1152/ajpcell.1993.264.6.C1505. [DOI] [PubMed] [Google Scholar]
- Hadley R. W., Hume J. R. An intrinsic potential-dependent inactivation mechanism associated with calcium channels in guinea-pig myocytes. J Physiol. 1987 Aug;389:205–222. doi: 10.1113/jphysiol.1987.sp016654. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Lee K. S., Marban E., Tsien R. W. Inactivation of calcium channels in mammalian heart cells: joint dependence on membrane potential and intracellular calcium. J Physiol. 1985 Jul;364:395–411. doi: 10.1113/jphysiol.1985.sp015752. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meissner G., Henderson J. S. Rapid calcium release from cardiac sarcoplasmic reticulum vesicles is dependent on Ca2+ and is modulated by Mg2+, adenine nucleotide, and calmodulin. J Biol Chem. 1987 Mar 5;262(7):3065–3073. [PubMed] [Google Scholar]
- Muallem S., Pandol S. J., Beeker T. G. Hormone-evoked calcium release from intracellular stores is a quantal process. J Biol Chem. 1989 Jan 5;264(1):205–212. [PubMed] [Google Scholar]
- Rampe D., Lacerda A. E. A new site for the activation of cardiac calcium channels defined by the nondihydropyridine FPL 64176. J Pharmacol Exp Ther. 1991 Dec;259(3):982–987. [PubMed] [Google Scholar]
- Sipido K. R., Wier W. G. Flux of Ca2+ across the sarcoplasmic reticulum of guinea-pig cardiac cells during excitation-contraction coupling. J Physiol. 1991 Apr;435:605–630. doi: 10.1113/jphysiol.1991.sp018528. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stern M. D., Lakatta E. G. Excitation-contraction coupling in the heart: the state of the question. FASEB J. 1992 Sep;6(12):3092–3100. doi: 10.1096/fasebj.6.12.1325933. [DOI] [PubMed] [Google Scholar]
- Stern M. D. Theory of excitation-contraction coupling in cardiac muscle. Biophys J. 1992 Aug;63(2):497–517. doi: 10.1016/S0006-3495(92)81615-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tate C. A., Bick R. J., Chu A., Van Winkle W. B., Entman M. L. Nucleotide specificity of cardiac sarcoplasmic reticulum. GTP-induced calcium accumulation and GTPase activity. J Biol Chem. 1985 Aug 15;260(17):9618–9623. [PubMed] [Google Scholar]
- Wier W. G., Egan T. M., López-López J. R., Balke C. W. Local control of excitation-contraction coupling in rat heart cells. J Physiol. 1994 Feb 1;474(3):463–471. doi: 10.1113/jphysiol.1994.sp020037. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yazawa K., Kaibara M., Ohara M., Kameyama M. An improved method for isolating cardiac myocytes useful for patch-clamp studies. Jpn J Physiol. 1990;40(1):157–163. doi: 10.2170/jjphysiol.40.157. [DOI] [PubMed] [Google Scholar]