Hormonal regulation of meiotic maturation in the hamster oocyte involves a cytoskeleton-mediated process

Maturation of the mammalian oocyte involves hormone-induced meiotic cell cycle progression from prophase I to metaphase II and extrusion of the first polar body (PB). In this study, the effects of gonadotrophins on meiotic cell cycle progression in cultured hamster oocytes were analyzed with respect to changes in cumulus cell-oocyte interactions and the oocyte cytoskeleton. Cumulus-oocyte complexes were obtained from large antral follicles (> or = 700 microns in diameter) of eCG-primed animals and were cultured in the presence or absence of gonadotropins alone (FSH, hCG, LH) or in combination (FSH + hCG or FSH + LH). Oocytes were analyzed using conventional, digital, and confocal fluorescence microscopy to monitor chromatin, actin, and tubulin organization under different culture conditions. Most oocytes (83%) cultured with FSH alone progressed to and arrested at metaphase II and extruded the first PB; in contrast, meiotic progression and PB extrusion were impaired (45-85%) in all other groups. The presence of cumulus cells associated with the oocyte was found necessary for progression to metaphase I and for first PB emission. Completion of meiotic maturation in the presence of FSH alone was correlated with enhanced cortical actin polymerization in the oocyte and the retraction of actin-containing transzonal cumulus processes. The results demonstrate that gonadotropins exert specific effects on meiotic progression, PB emission, cumulus-oocyte interactions, and oocyte cytoskeletal organization during in vitro maturation of hamster oocytes, indicating that the hormonal control of meiosis involves cytoskeletal changes in both the somatic and germ cells.