Abstract
Large-conductance calcium (Ca2+)-activated potassium (K+) (BK) channel activation is important for feedback control of Ca2+ influx and cell excitability during spontaneous muscle contraction. To characterize endogenously expressed BK channels and evaluate the functional relevance of Ca2+ sources leading to BK activity, patch-clamp electrophysiology was performed on cricket oviduct myocytes to obtain single-channel recordings. The single-channel conductance of BK channels was 120 pS, with increased activity resulting from membrane depolarization or increased intracellular Ca2+ concentration. Extracellular application of tetraethylammonium (TEA) and iberiotoxin (IbTX) suppressed single-channel current amplitude. These results indicate that BK channels are endogenously expressed in cricket oviduct myocytes. Ca2+ release from internal Ca2+ stores and Ca2+ influx via the plasma membrane, which affect BK activity, were investigated. Extracellular Ca2+ removal nullified BK activity. Administration of ryanodine and caffeine reduced BK activity. Administration of L-type Ca2+ channel activity regulators (Bay K 8644 and nifedipine) increased and decreased BK activity, respectively. Finally, the proximity between the L-type Ca2+ channel and BK was investigated. Administration of Bay K 8644 to the microscopic area within the pipette increased BK activity. However, this increase was not observed at a sustained depolarizing potential. These results show that BK channels are endogenously expressed in cricket oviduct myocytes and that BK activity is regulated by L-type Ca2+ channel activity and Ca2+ release from Ca2+ stores. Together, these results show that functional coupling between L-type Ca2+ and BK channels may underlie the molecular basis of spontaneous rhythmic contraction.
Highlights
The calcium (Ca2+)-activated potassium (K+) (BK) channel has a large single-channel conductance (∼100–300 pS), the nickname “Big K” [1, 2]
BK channels primarily function as negative-feedback regulators of membrane potential and [Ca2+]i, which are important in many physiological processes
We investigated the proximity of BK and L-type Ca2+ channels within the microdomain by administering Bay K 8644 through a patch pipette and observing the effect on BK activity on the patch membrane
Summary
The calcium (Ca2+)-activated potassium (K+) (BK) channel has a large single-channel conductance (∼100–300 pS) (or MaxiK), the nickname “Big K” [1, 2]. The BK channel α-subunit plays a central role in channel function. BK channels are expressed in nerves and muscles, and in endocrine, cardiovascular, digestive, urinary, and reproductive organs [1, 2, 5, 6]. BK channel activity is regulated by membrane depolarization and increased intracellular Ca2+. BK channel activation results in membrane repolarization and voltage-gated Ca2+ channel closure, reducing Ca2+ entry into cells. BK channels primarily function as negative-feedback regulators of membrane potential and [Ca2+]i, which are important in many physiological processes. BK activity is involved in action potential intervals, duration, firing frequency, neurotransmitter release, endocrine secretion, smooth muscle contraction, and control of epithelial cell potassium release in nerves [6,7,8,9,10]. The BK channels are functionally involved in movement disorders, circadian rhythms, learning and memory, hearing, vision, cardiovascular function, airway control, urination, glucose
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