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Development of Transient Outward Currents Coupled With Ca²⁺-Induced Ca²⁺ Release Mediates Oscillatory Membrane Potential in Ascidian Muscle Cells

¹Department of Life Sciences, Graduate School of Arts and Sciences, University of Tokyo, Meguro-ku, 153-8902 Tokyo; ²Molecular Neurobiology Section, Neuroscience Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, 305-8566 Ibaraki; ³Division of Biophysics and Neurobiology, Department of Molecular Physiology, National Institute for Physiological Sciences; and ⁴Section of Developmental Neurophysiology, Center for Integrative Bioscience, Okazaki National Research Institutes, Myodaiji, Okazaki 444-8585 Aichi, Japan

Submitted 16 January 2004; accepted in final form 30 March 2004

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 Ca²⁺-induced Ca²⁺ 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 Ca²⁺-activated K⁺ channel inhibitors. We found a 60-pS single channel conductance that was activated by local Ca²⁺ 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.

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