Regulation of oocyte maturation: communication in the rat cumulus-oocyte complex

This study was undertaken to analyse the time relationships between breakdown of communication in the cumulus-oocyte complex and reinitiation of meiosis in the oocyte. In addition the possibility was examined that under conditions of established communication, cAMP is transferred from the cumulus cells to the oocyte. Coupling in the cumulus-oocyte complex and maturation of the oocyte were examined, both in vitro in follicles exposed to LH and in vivo following injection of the hormone to immature, pregnant mare's serum gonadotrophin-primed rats. Transfer analysis was performed by determination of cAMP content in cumulus-enclosed as compared to cumulus-free oocytes incubated with forskolin. It was discovered that after 1 h of culture in the presence of LH, coupling in the cumulus-oocyte complexes had decreased to 45% of its initial level, while only 10% of the oocytes had resumed meiosis by this time. The decrease in coupling in cumulus-oocyte complexes in vivo was 20% by 2 h after administration of the hormone, with all the oocytes being immature at this time. Cyclic AMP determinations revealed that cumulus-enclosed oocytes contained concentrations of cAMP three-fold higher than cumulus-free oocytes incubated under similar conditions. This study demonstrates that, in the rat, (i) a decrease in coupling precedes reinitiation of meiosis and (ii) in the presence of established communication, cAMP is transferred from the cumulus cells to the oocyte. These findings suggest that a decrease in communication can serve as the signal for oocyte maturation, possibly by preventing transfer of cAMP from the cumulus cells to the oocyte.