Secretion of cumulus expansion enabling factor by mouse oocytes: relationship to oocyte growth and competence to resume meiosis.

Fully grown mouse oocytes secrete a factor that enables the surrounding cumulus cells to undergo cumulus expansion upon stimulation of the cumulus cells with follicle-stimulating hormone in vitro. The secretion of the enabling factor by the oocytes is developmentally regulated; it is normally secreted in significant amounts only by oocytes that are competent of undergoing spontaneous germinal vesicle breakdown (GVB) and resuming the first meiotic division. The objective of this study was to determine the relationship, if any, among secretion of this factor, oocyte growth, and the competence to undergo GVB. Three experimental systems were used to assess these relationships. First, 20 to 25% of the oocytes isolated from the small antral follicles of mutant hypogonadal mice were GVB-incompetent even though they had achieved a size typical of GVB-competent oocytes. These large GVB-incompetent oocytes secreted almost as much cumulus expansion enabling factor as the GVB-competent oocytes. Second, GVB-incompetent oocytes cultured under conditions that promote the acquisition of GVB competence but not oocyte growth acquired the ability to secrete the cumulus expansion enabling factor. Third, the precocious activation of maturation promoting factor (MPF) in GVB-incompetent oocytes by okadaic acid did not stimulate the secretion of cumulus expansion enabling factor. It is concluded that the secretion of cumulus expansion enabling factor by oocytes is (1) independent of oocyte growth, (2) independent of competence to undergo GVB, and (3) not induced by the precocious activation of MPF. Thus, although the secretion of the enabling factor normally coincides with the time of acquisition of competence to undergo GVB, the ability to secrete the enabling factor is independent of oocyte maturation. Nevertheless, factors that promote the oocyte's program that leads to competence to undergo GVB probably also promote the ability to secrete the enabling factor.