Native ion current coupled to purinergic activation via basal and mechanically induced ATP release in Xenopus follicles

Abstract

Xenopus follicle-enclosed oocytes are endowed with purinergic receptors located in the follicular cell membrane; their stimulation by ATP elicits an electrical response that includes generation of a fast inward current (F Cl) carried by Cl-. Here, it was found that mechanical stimulation of the follicle provoked a native electrical response named I mec. This was dependent on coupling between oocyte and follicular cells, because Imec was eliminated by enzymatic defolliculation or application of uncoupling drugs, such as heptanol or carbenoxolone. Moreover, the characteristics of Imec suggested that it corresponded with opening of the Cl- channel involved in FCl. For example, Imec showed cross-talk with the membrane mechanism that activates the FCl response and anionic selectivity similar to that displayed by FCl. Also like FCl, Imec was independent of extracellular or intracellular Ca2+. Furthermore, Imec was inhibited by superfusion with a purinergic antagonist, suramin, or by an enzyme that rapidly hydrolyzes ATP, apyrase. The response to mechanical stimulation was reconstituted in defolliculated oocytes expressing P2X channels as an ATP sensor. Recently, it has been shown that ATP release from the Xenopus oocyte is triggered by mechanical stimulation. Together, these observations seemed to indicate that Imec is activated through a mechanism that involves oocyte release of ATP that diffuses and activates purinergic receptors in follicular cells, with subsequent opening of FCl channels. Thus, Imec generation disclosed a paracrine communication system via ATP between the oocyte and its companion follicular cells that might be of physiological importance during the growth and development of the gamete. © 2008 Wiley-Liss, Inc.