Osmo-dependent Cl- currents activated by cyclic AMP in follicle-enclosed Xenopus oocytes

The role of adenosine 3',5'-cyclic monophosphate (cAMP) in generating the osmo-dependent slow inward membrane currents (S(in)) elicited by activation of follicle stimulating hormone (FSH) or acetylcholine (ACh) receptors was studied in voltage-clamped, follicle-enclosed oocytes of Xenopus laevis (follicles). Forskolin (FSK) also generated S(in) currents, and in low concentrations it potentiated the S(in) currents elicited by FSH but not those elicited by ACh. Moreover, intra-oocyte injections of cAMP elicited similar slow inward currents (cAMP-S(in)) that: (i) were carried mainly by chloride ions; (ii) were abolished by defolliculating the oocytes; and (iii) were dependent on the osmolarity of the external medium. Compared with the Ca(2+)-dependent chloride channels that are located in the oocyte membrane; the cAMP-activated S(in) channels were less permeable to I- and Br-, and their current-voltage relation did not rectify strongly at negative potentials. Generation of cAMP-S(in) desensitized the FSH-S(in) currents, but did not have effects on both the S(in) and the fast chloride current (F(in)) specifically elicited by ACh. Furthermore, follicular phospholipase C activation through stimulation of angiotensin II (AII) receptors failed to generate the current responses elicited by ACh. We conclude that cAMP acts as a potent second messenger in generating the osmo-dependent Cl- currents elicited by FSH but not those elicited by ACh. The mechanisms underlying the ACh responses remain unknown. The osmo-dependent chloride channels activated by cAMP may play a role in the control of volume of the follicular cells-oocyte complex.