Silent calcium channels in skeletal muscle fibers of the crustacean Atya lanipes.
The superficial (tonic) abdominal flexor muscles of Atya lanipes do not generate Ca(2+) action potentials when depolarized and have no detectable inward Ca(2+) current. These fibers, however, are strictly dependent on Ca(2+) influx for contraction, suggesting that they depend on Ca(2+)-induced Ca(2+) release for contractile activation. The nature of the communication between Ca(2+) channels in the sarcolemmal/tubular membrane and Ca(2+) 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%. Sr(2+) and Ba(2+) action potentials could be elicited in Ca(2+)-free solutions. The spikes generated by these divalent cations were abolished by nifedipine. As the Sr(2+) or Ba(2+) 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 Ca(2+) concentration the channels were silent, i.e., no inward Ca(2+) current was detected. In Ca(2+)-free solutions, inward currents carried by 138 mm Sr(2+) or Ba(2+) 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 Ca(2+) channels. Peak inward current density values were low, ca. -33 microA/cm(2) for Sr(2+) and -14 microA/cm(2) for Ba(2+), suggesting that Ca(2+) channels are present at a very low density. It is concluded that Ca(2+)-induced Ca(2+) release in this crustacean muscle operates with an unusually high gain: Ca(2+) influx through the silent Ca(2+) channels is too low to generate a macroscopic inward current, but increases sufficiently the local concentration of Ca(2+) in the immediate vicinity of the sarcoplasmic reticulum Ca(2+) release channels to trigger the highly amplified release of Ca(2+) required for tension generation.
Monterrubio
J
J
Institute of Neurobiology and Department of Physiology, University of Puerto Rico, Medical Sciences Campus, 201 Boulevard del Valle, San Juan, PR 00901, USA.
Lizardi
L
L
Zuazaga
C
C
D001498:3-Pyridinecarboxylic acid, 1,4-dihydro-2,6-dimethyl-5-nitro-4-(2-(trifluoromethyl)phenyl)-, Methyl ester / Q000494:pharmacology; D000818:Animals; D001464:Barium / Q000494:pharmacology; D002104:Cadmium / Q000494:pharmacology; D015220:Calcium Channels / Q000502:physiology*; D002413:Cations, Divalent / Q000494:pharmacology; D003445:Crustacea; D004558:Electric Stimulation; D066298:In Vitro Techniques; D009119:Muscle Contraction / Q000187:drug effects / Q000502:physiology*; D018485:Muscle Fibers, Skeletal / Q000187:drug effects / Q000502:physiology*; D018482:Muscle, Skeletal / Q000502:physiology*; D018408:Patch-Clamp Techniques; D013324:Strontium / Q000494:pharmacology
D015220:Calcium Channels; D002413:Cations, Divalent; D002104:Cadmium; D001464:Barium; D001498:3-Pyridinecarboxylic acid, 1,4-dihydro-2,6-dimethyl-5-nitro-4-(2-(trifluoromethyl)phenyl)-, Methyl ester; D013324:Strontium