Ultrastructural changes in follicle cell-oocyte associations during development and maturation of the ovarian follicle in Atlantic croaker.

Full-grown ovarian follicles of the marine teleost Atlantic croaker (Micropogonias undulatus) are unresponsive to steroidal maturation-inducing substance (MIS). However, responsiveness to MIS (maturational competence) can be induced in vivo or in vitro by brief stimulation with gonadotropin (e.g., human chorionic gonadotropin, hCG). The objective of this study was to examine ultrastructural changes in follicle cell-oocyte associations related to the acquisition of maturational competence and maturation in croaker ovarian follicles. Ultrathin sections of lanthanum-infiltrated samples were observed by transmission electron microscopy at various points during follicular development and hormone-induced maturation: vitellogenic oocytes (< 350 microns), full-grown oocytes (350-400 microns), hCG-stimulated (maturationally competent) oocytes, hCG/MIS-stimulated (early-maturation, hydrating) oocytes, and ovulated oocytes. In general, prior to ovulation, oocyte microvilli made contact with granulosa cells, and gap junction-like structures were seen at these points of contact. Midvitellogenic follicles (< 350 microns) had relatively high levels of follicle cell-oocyte associations and gap junctional contacts, but by late vitellogenesis (350-400 microns) these levels had declined markedly. However, high levels of intercellular associations and gap junctional contacts were reestablished upon induction of maturational competence with hCG, and these levels remained high in early-maturation oocytes. These changes seemed to be mainly due to alterations in oocyte microvilli length and surface contact with granulosa cells rather than to alterations in the numbers of microvilli. However, retraction and disappearance of microvilli occurred during ovulation. Therefore, the appearance of maturational competence coincided with the reestablishment of heterocellular gap junctional contacts in full-grown follicles. One function of these contacts may be to allow transfer of maturational signals between the granulosa cells and the oocyte during the early stages of follicular maturation.