Intermediate Conductance Ca-activated Potassium Channels Are Activated by Functional Coupling with Stretch-activated Nonselective Cation Channels in Cricket Myocytes

Overview

Journal Front Insect Sci

Date 2024 Mar 12

PMID 38468799

Authors

Tomohiro Numata

Kaori Sato-Numata

Masami Yoshino

Affiliations

Soon will be listed here.

Abstract

Cooperative gating of localized ion channels ranges from fine-tuning excitation-contraction coupling in muscle cells to controlling pace-making activity in the heart. Membrane deformation resulting from muscle contraction activates stretch-activated (SA) cation channels. The subsequent Ca influx activates spatially localized Ca-sensitive K channels to fine-tune spontaneous muscle contraction. To characterize endogenously expressed intermediate conductance Ca-activated potassium (IK) channels and assess the functional relevance of the extracellular Ca source leading to IK channel activity, we performed patch-clamp techniques on cricket oviduct myocytes and recorded single-channel data. In this study, we first investigated the identification of IK channels that could be distinguished from endogenously expressed large-conductance Ca-activated potassium (BK) channels by adding extracellular Ba. The single-channel conductance of the IK channel was 62 pS, and its activity increased with increasing intracellular Ca concentration but was not voltage-dependent. These results indicated that IK channels are endogenously expressed in cricket oviduct myocytes. Second, the Ca influx pathway that activates the IK channel was investigated. The absence of extracellular Ca or the presence of Gd abolished the activity of IK channels. Finally, we investigated the proximity between SA and IK channels. The removal of extracellular Ca, administration of Ca to the microscopic region in a pipette, and application of membrane stretching stimulation increased SA channel activity, followed by IK channel activity. Membrane stretch-induced SA and IK channel activity were positively correlated. However, the emergence of IK channel activity and its increase in response to membrane mechanical stretch was not observed without Ca in the pipette. These results strongly suggest that IK channels are endogenously expressed in cricket oviduct myocytes and that IK channel activity is regulated by neighboring SA channel activity. In conclusion, functional coupling between SA and IK channels may underlie the molecular basis of spontaneous rhythmic contractions.

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