Xenopus oocyte K+ current. II. Adenylyl cyclase-linked receptors on follicle cells

Xenopus ovarian follicles consist of single large oocytes surrounded by a layer of small follicle cells that are coupled to the oocyte by gap junctions. Hyperpolarizing K+ currents can be detected in the oocytes of follicles stimulated with adenosine, isoproterenol, follicle-stimulating hormone (FSH), or microinjected adenosine 3',5'-cyclic monophosphate (cAMP). We show that cAMP accumulation can be detected in follicles incubated with the adenosine agonist 5'-N-ethylcarboxamidoadenosine (NECA), isoproterenol, or FSH, but only if forskolin and a phosphodiesterase inhibitor are also added. Treatment of follicles with collagenase has been reported to reduce, but usually not to eliminate, cAMP-activated K+ currents. In this study we show that collagenase treatment alone does not completely remove follicle cells or receptor-mediated cAMP accumulation measured in follicles. cAMP accumulation and cAMP-dependent K+ currents are both eliminated when the follicle cells are completely removed by a technique involving treatment of follicles with collagenase and hypertonic saline. Oocytes completely stripped of follicle cells fail to accumulate cAMP in response to receptor agonists and forskolin. Isolated follicle cells derived from single follicles (but without the oocyte present) accumulate cAMP in response to these drugs to an extent equivalent to the response seen in single intact follicles. Adenylyl cyclase-linked receptors of Xenopus follicles thus appear to be located exclusively on follicle cells. The data suggest that cAMP-dependent K+ currents, although measured in oocytes, may be generated in follicle cells which communicate with oocytes. Another possibility is that a high resting K+ conductance in follicle cells is communicated to oocytes via cAMP-sensitive gap junctions.