Agonist‐activated Ca 2+ influx and Ca 2+ ‐dependent Cl − channels in Xenopus ovarian follicular cells: Functional heterogeneity within the cell monolayer

Xenopus follicles are endowed with specific receptors for ATP, ACh, and AII, transmitters proposed as follicular modulators of gamete growth and maturation in several species. Here, we studied ion‐current responses elicited by stimulation of these receptors and their activation mechanisms using the voltage‐clamp technique. All agonists elicited Cl − currents that depended on coupling between oocyte and follicular cells and on an increase in intracellular Ca 2+ concentration ([Ca 2+ ] i ), but they differed in their activation mechanisms and in the localization of the molecules involved. Both ATP and ACh generated fast Cl − (F Cl ) currents, while AII activated an oscillatory response; a robust Ca 2+ influx linked specifically to F Cl activation elicited an inward current (I iw,Ca ) which was carried mainly by Cl − ions, through channels with a sequence of permeability of SCN − > I − > Br − > Cl − . Like F Cl , I iw,Ca was not dependent on oocyte [Ca 2+ ] i ; instead both were eliminated by preventing [Ca 2+ ] i increase in the follicular cells, and also by U73122 and 2‐APB, drugs that inhibit the phospolipase C (PLC) pathway. The results indicated that F Cl and I iw,Ca were produced by the expected, PLC‐stimulated Ca 2+ ‐release and Ca 2+ ‐influx, respectively, and by the opening of I Cl(Ca) channels located in the follicular cells. Given their pharmacological characteristics and behavior in conditions of divalent cation deprivation, Ca 2+ ‐influx appeared to be driven through store‐operated, calcium‐like channels. The AII response, which is also known to require PLC activation, did not activate I iw,Ca and was strictly dependent on oocyte [Ca 2+ ] i increase; thus, ATP and ACh receptors seem to be expressed in a population of follicular cells different from that expressing AII receptors, which were coupled to the oocyte through distinct gap‐junction channels. J. Cell. Physiol. 227: 3457–3470, 2012. © 2011 Wiley Periodicals, Inc.