Abstract
Applying a brief repolarizing pre-pulse to a depolarized frog skeletal muscle fiber restores a small fraction of the transverse tubule membrane voltage sensors from the inactivated state. During a subsequent depolarizing test pulse we detected brief, highly localized elevations of myoplasmic Ca2+ concentration (Ca2+ "sparks") initiated by restored voltage sensors in individual triads at all test pulse voltages. The latency histogram of these events gives the gating pattern of the sarcoplasmic reticulum (SR) calcium release channels controlled by the restored voltage sensors. Both event frequency and clustering of events near the start of the test pulse increase with test pulse depolarization. The macroscopic SR calcium release waveform, obtained from the spark latency histogram and the estimated open time of the channel or channels underlying a spark, exhibits an early peak and rapid marked decline during large depolarizations. For smaller depolarizations, the release waveform exhibits a smaller peak and a slower decline. However, the mean use time and mean amplitude of the individual sparks are quite similar at all test depolarizations and at all times during a given depolarization, indicating that the channel open times and conductances underlying sparks are essentially independent of voltage. Thus, the voltage dependence of SR Ca2+ release is due to changes in the frequency and pattern of occurrence of individual, voltage-independent, discrete release events.
MeSH Terms
Animals
Electric Stimulation
Evoked Potentials
Fluorescence
In Vitro Techniques
Ion Channel Gating
Kinetics
Muscle, Skeletal/metabolism,physiology
Rana pipiens
Sarcoplasmic Reticulum/metabolism,physiology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Klein M G
Department of Biochemistry and Molecular Biology, University of Maryland School of Medicine, 108 North Greene Street, Baltimore, MD 21201, USA.
Lacampagne A
Schneider M F
References (19)
19 references, click to expand
-
A non-linear voltage dependent charge movement in frog skeletal muscle.
J Physiol. 1976 Jan;254(2):245-83
PMID: 1082506
-
Potassium contractures in single muscle fibres.
J Physiol. 1960 Sep;153:386-403
PMID: 13714849
-
Measurement and modification of free calcium transients in frog skeletal muscle fibres by a metallochromic indicator dye.
J Physiol. 1983 Oct;343:161-96
PMID: 6606034
-
Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients.
J Physiol. 1983 Nov;344:625-66
PMID: 6655593
-
Time course of calcium release and removal in skeletal muscle fibers.
Biophys J. 1984 Mar;45(3):637-41
PMID: 6608964
-
Inactivation of calcium release from the sarcoplasmic reticulum in frog skeletal muscle.
J Physiol. 1988 Nov;405:727-45
PMID: 2855645
-
Effects of caffeine on calcium release from the sarcoplasmic reticulum in frog skeletal muscle fibres.
J Physiol. 1990 Jun;425:599-626
PMID: 2213590
-
Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle.
Science. 1993 Oct 29;262(5134):740-4
PMID: 8235594
-
Control of calcium release in functioning skeletal muscle fibers.
Annu Rev Physiol. 1994;56:463-84
PMID: 8010748
-
Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors.
Annu Rev Physiol. 1994;56:485-508
PMID: 7516645
-
Structure and development of E-C coupling units in skeletal muscle.
Annu Rev Physiol. 1994;56:509-34
PMID: 8010750
-
Local calcium transients triggered by single L-type calcium channel currents in cardiac cells.
Science. 1995 May 19;268(5213):1042-5
PMID: 7754383
-
Imaging elementary events of calcium release in skeletal muscle cells.
Science. 1995 Sep 22;269(5231):1723-6
PMID: 7569901
-
Calcium inactivation of calcium release in frog cut muscle fibers that contain millimolar EGTA or Fura-2.
J Gen Physiol. 1995 Aug;106(2):337-88
PMID: 8537819
-
Two mechanisms of quantized calcium release in skeletal muscle.
Nature. 1996 Feb 1;379(6564):455-8
PMID: 8559251
-
Sarcomeric calcium sparks activated by fiber depolarization and by cytosolic Ca2+ in skeletal muscle.
Cell Calcium. 1996 Aug;20(2):123-8
PMID: 8889203
-
Factors shaping the confocal image of the calcium spark in cardiac muscle cells.
Biophys J. 1996 Dec;71(6):2942-57
PMID: 8968567
-
Repriming and activation alter the frequency of stereotyped discrete Ca2+ release events in frog skeletal muscle.
J Physiol. 1996 Dec 15;497 ( Pt 3):581-8
PMID: 9003545
-
Charge movement and mechanical repriming in skeletal muscle.
J Physiol. 1976 Jan;254(2):361-88
PMID: 1082510