Abstract
The physiological success of fluid-secreting tissues relies on a regulated interplay between Ca(2+)-activated Cl(-) and K(+) channels. Parotid acinar cells express two types of Ca(2+)-activated K(+) channels: intermediate conductance IK1 channels and maxi-K channels. The IK1 channel is encoded by the K(Ca)3.1 gene, and the K(Ca)1.1 gene is a likely candidate for the maxi-K channel. To confirm the genetic identity of the maxi-K channel and to probe its specific roles, we studied parotid glands in mice with the K(Ca)1.1 gene ablated. Parotid acinar cells from these animals lacked maxi-K channels, confirming their genetic identity. The stimulated parotid gland fluid secretion rate was normal, but the sodium and potassium content of the secreted fluid was altered. In addition, we found that the regulatory volume decrease in acinar cells was substantially impaired in K(Ca)1.1-null animals. We examined fluid secretion from animals with both K(+) channel genes deleted. The secretion rate was severely reduced, and the ion content of the secreted fluid was significantly changed. We measured the membrane potentials of acinar cells from wild-type mice and from animals with either or both K(+) channel genes ablated. They revealed that the observed functional effects on fluid secretion reflected alterations in cell membrane voltage. Our findings show that the maxi-K channels are critical for the regulatory volume decrease in these cells and that they play an important role in the sodium uptake and potassium secretion process in the ducts of these fluid-secreting salivary glands.
Highlights
For the fluid secretion process to be sustained, an apical cell driving force for ClϪ efflux must be maintained
Ca2ϩ-activated Kϩ Channels in Parotid Acinar Cells—As described in the Introduction, parotid acinar cells express two types of Ca2ϩ-activated Kϩ channels: the time- and voltageindependent IK1 channel and a maxi-K channel that is gated by voltage as well as by Ca2ϩ
These findings clearly identify the IK1 channel with the KCa3.1 gene
Summary
Mouse Strains—Several strains of mice were used, including three with one or more Ca2ϩ-activated Kϩ channel genes deleted. The measured relevant junction potential in these recordings was Ͻ4 mV, sufficiently small that no correction to membrane voltage was made. Parotid acinar cell membrane potentials were measured at room temperature (20 –22 °C) with the current clamp mode of an Axopatch 200B amplifier using a Digidata 1320A digitizer running Clampex 9.2 (Axon Instruments); Clampfit 9.2 was used for analysis. These experiments utilized the perforated patch technique [20] with an external solution containing 150 mM NaCl, 5 mM KCl, 2 mM CaCl2, 1 mM MgCl2, 10 mM glucose, and 10 mM HEPES (pH 7.2). These are reported below or in the figure legends as appropriate
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