Development of transient outward currents coupled with Ca2+-induced Ca2+ release mediates oscillatory membrane potential in ascidian muscle cells.
Isolated ascidian Halocynthia roretzi blastomeres of the muscle lineage exhibit muscle cell-like excitability on differentiation despite the arrest of cell cleavage early in development. This characteristic provides a unique opportunity to track changes in ion channel expression during muscle cell differentiation. Here, we show that the intrinsic membrane property of ascidian cleavage-arrested muscle-type cells becomes oscillatory by expressing transient outward currents (I(to)) activated by Ca(2+)-induced Ca(2+) release (CICR) in a maturation-dependent manner. In current-clamp mode, most day 4 (72 h after fertilization) cleavage-arrested muscle cells exhibited an oscillatory membrane potential of -20 mV at 15 Hz, whereas most day 3 (48 h after fertilization) cells exhibited a spiking pattern. In voltage-clamp mode, the day 4 cells exhibited prominent transient outward currents that were not present in day 3 cells. I(to) was abolished by the application of 10 mM caffeine, implying that CICR was involved in I(to) activation. I(to) was based on K(+) efflux and sensitive to tetraethylammonium and some Ca(2+)-activated K(+) channel inhibitors. We found a 60-pS single channel conductance that was activated by local Ca(2+) release in ascidian muscle cell. Voltage-clamp recording with an oscillatory waveform as a command pulse showed that CICR-activated K(+) currents were activated during the falling phase of the membrane potential oscillation. These results suggest that developmental expression of CICR-activated K(+) current plays a role in the maturation of larval locomotion by modifying the intrinsic membrane excitability of muscle cells.
Nakajo
Koichi
K
Department of Life Sciences, Graduate School of Arts and Sciences, University of Tokyo, Meguro-ku, 153-8902 Tokyo, Japan. knakajo@nips.ac.jp
Okamura
Yasushi
Y
D000200:Action Potentials; D000818:Animals; D002110:Caffeine / Q000494:pharmacology; D002118:Calcium / Q000378:metabolism / Q000502:physiology*; D016922:Cellular Senescence; D004553:Electric Conductivity; D007425:Intracellular Membranes / Q000378:metabolism; D007814:Larva; D008564:Membrane Potentials / Q000502:physiology; D032342:Muscle Cells / Q000502:physiology*; D009991:Oscillometry; D015221:Potassium Channels / Q000187:drug effects / Q000502:physiology; D011930:Reaction Time; D013268:Stimulation, Chemical; D013550:Swimming; D013997:Time Factors; D014561:Urochordata / Q000235:genetics / Q000502:physiology*
D015221:Potassium Channels; D002110:Caffeine; D002118:Calcium