Epithelium and/or theca are required for ATP-elicited K+ current in follicle-enclosed Xenopus oocytes

The Xenopus follicular cell membrane is endowed with ATP-sensitive K+ channels, which are operated by various transmitters. These generate the ionic response named I-K,I-cAMP via a mechanism that involves intracellular cAMP synthesis. It is known that opening these K+ channels favors oocyte maturation. Follicle stimulation by adenosine (Ado) or ATP consistently generates a strong I-K,I-cAMP via activation of P1 and P3 purinergic receptors; however, ATP can also inhibit I-K,I-cAmp, apparently acting on a third receptor type. Here, we show that I-K,I-cAMP might be elicited by ATP released within the follicle, and that current activation by ATP was entirely dependent on the presence of epithelial and/or theca layers. Morphological studies confirmed that removal of epithelium/theca in these follicles (e.t.r.) was complete, and activation of fast Cl- (F-in) currents by ATP in e.t.r. follicles confirmed that communication between oocyte and follicular cells remained unchanged. Thus, dependence on epithelium/theca was specific for ATIP-elicited K+ current. Using UTP and betagamma-MeATP as specific purinergic agents for I-K,I-cAMP inhibition and activation, respectively, it was found that inhibition of I-K,I-cAMp elicited by ATP or UTP was robustly present in e.t.r. follicles but was absent or strongly decreased in whole follicles (w.f.). Accordingly, this indicated that in w.f., epithelium and/or theca downregulated the I-K,I-cAMP inhibition evoked by ATP, and that this control mechanism was absent in e.t.r. follicles. We suggest that this notable action on follicular cells involves one or both of two mechanisms, a paracrine transmitter released from epithelial and/or theca layers and action of ecto-ATPases. (C) 2004 Wiley-Liss, Inc.