Silent Calcium Channels in Skeletal Muscle Fibers of the Crustacean Atya lanipes

Silent Calcium Channels in Skeletal Muscle Fibers of the Crustacean Atya lanipes The superficial (tonic) abdominal flexor muscles of Atya lanipes do not generate Ca2+ action potentials when depolarized and have no detectable inward Ca2+ current. These fibers, however, are strictly dependent on Ca2+ influx for contraction, suggesting that they depend on Ca2+-induced Ca2+ release for contractile activation. The nature of the communication between Ca2+ channels in the sarcolemmal/tubular membrane and Ca2+ release channels in the sarcoplasmic reticulum in this crustacean muscle was investigated. The effects of dihydropyridines on tension generation and the passive electrical response were examined in current-clamped fibers: Bay K 8644 enhanced tension about 100% but did not alter the passive electrical response; nifedipine inhibited tension by about 70%. Sr2+ and Ba2+ action potentials could be elicited in Ca2+-free solutions. The spikes generated by these divalent cations were abolished by nifedipine. As the Sr2+ or Ba2+ concentrations were increased, the amplitudes of the action potentials and their maximum rate of rise, V max , increased and tended towards saturation. Three-microelectrode voltage-clamp experiments showed that even at high (138 mm) extracellular Ca2+ concentration the channels were silent, i.e., no inward Ca2+ current was detected. In Ca2+-free solutions, inward currents carried by 138 mm Sr2+ or Ba2+ were observed. The currents activated at voltages above −40 mV and peaked at about 0 mV. This voltage-activation profile and the sensitivity of the channels to dihydropyridines indicate that they resemble L-type Ca2+ channels. Peak inward current density values were low, ca.−33 μA/cm2 for Sr2+ and −14 μA/cm2 for Ba2+, suggesting that Ca2+ channels are present at a very low density. It is concluded that Ca2+-induced Ca2+ release in this crustacean muscle operates with an unusually high gain: Ca2+ influx through the silent Ca2+ channels is too low to generate a macroscopic inward current, but increases sufficiently the local concentration of Ca2+ in the immediate vicinity of the sarcoplasmic reticulum Ca2+ release channels to trigger the highly amplified release of Ca2+ required for tension generation. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The Journal of Membrane Biology Springer Journals

Silent Calcium Channels in Skeletal Muscle Fibers of the Crustacean Atya lanipes

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Publisher
Springer-Verlag
Copyright
Copyright © Inc. by 2000 Springer-Verlag New York
Subject
Life Sciences; Biochemistry, general; Human Physiology
ISSN
0022-2631
eISSN
1432-1424
D.O.I.
10.1007/s002320001002
Publisher site
See Article on Publisher Site

Abstract

The superficial (tonic) abdominal flexor muscles of Atya lanipes do not generate Ca2+ action potentials when depolarized and have no detectable inward Ca2+ current. These fibers, however, are strictly dependent on Ca2+ influx for contraction, suggesting that they depend on Ca2+-induced Ca2+ release for contractile activation. The nature of the communication between Ca2+ channels in the sarcolemmal/tubular membrane and Ca2+ release channels in the sarcoplasmic reticulum in this crustacean muscle was investigated. The effects of dihydropyridines on tension generation and the passive electrical response were examined in current-clamped fibers: Bay K 8644 enhanced tension about 100% but did not alter the passive electrical response; nifedipine inhibited tension by about 70%. Sr2+ and Ba2+ action potentials could be elicited in Ca2+-free solutions. The spikes generated by these divalent cations were abolished by nifedipine. As the Sr2+ or Ba2+ concentrations were increased, the amplitudes of the action potentials and their maximum rate of rise, V max , increased and tended towards saturation. Three-microelectrode voltage-clamp experiments showed that even at high (138 mm) extracellular Ca2+ concentration the channels were silent, i.e., no inward Ca2+ current was detected. In Ca2+-free solutions, inward currents carried by 138 mm Sr2+ or Ba2+ were observed. The currents activated at voltages above −40 mV and peaked at about 0 mV. This voltage-activation profile and the sensitivity of the channels to dihydropyridines indicate that they resemble L-type Ca2+ channels. Peak inward current density values were low, ca.−33 μA/cm2 for Sr2+ and −14 μA/cm2 for Ba2+, suggesting that Ca2+ channels are present at a very low density. It is concluded that Ca2+-induced Ca2+ release in this crustacean muscle operates with an unusually high gain: Ca2+ influx through the silent Ca2+ channels is too low to generate a macroscopic inward current, but increases sufficiently the local concentration of Ca2+ in the immediate vicinity of the sarcoplasmic reticulum Ca2+ release channels to trigger the highly amplified release of Ca2+ required for tension generation.

Journal

The Journal of Membrane BiologySpringer Journals

Published: Jan 1, 2000

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