Agonist-activated Ca2+ Influx and Ca2+ -Dependent Cl- Channels in Xenopus Ovarian Follicular Cells: Functional Heterogeneity Within the Cell Monolayer

J Cell Physiol. 2012 Oct;227(10):3457-70. doi: 10.1002/jcp.24046.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / metabolism
  • Adenosine Triphosphate / metabolism
  • Animals
  • Calcium / metabolism*
  • Chloride Channels / metabolism*
  • Chlorides / metabolism*
  • Female
  • Gap Junctions / metabolism*
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism
  • Ion Transport / physiology
  • Oocytes / metabolism
  • Ovarian Follicle / metabolism*
  • Receptors, Cholinergic / metabolism
  • Xenopus laevis

Substances

  • Chloride Channels
  • Chlorides
  • Inositol 1,4,5-Trisphosphate Receptors
  • Receptors, Cholinergic
  • Adenosine Triphosphate
  • Acetylcholine
  • Calcium