Regulation of development in the fully grown mouse oocyte: chromosome-mediated temporal and spatial differentiation of the cytoplasm and plasma membrane.

The relationship between nuclear maturation and the differentiation of the cytoplasm and plasma membrane during resumption of arrested meiosis was investigated by culture of GV-and MII-stage mouse oocytes in the presence and absence of nocodazole. Culture in the presence of nocodazole was associated with dispersal of MI and MII chromosomes throughout the subplasmalemmal cytoplasm. A progression of cortical (thickening of actin filaments) and plasma membrane changes (denudation of microvilli, reduction in cell surface glycoproteins, formation of chromosome-containing evaginations) that normally occurs in proximity to chromosomes associated with intact MI or MII spindles took place only in those regions of the cortical cytoplasm containing the dispersed subplasmalemmal chromosomes. The dispersion and migration of the chromosomes occurred in an apparently random fashion. Fluorescent probe analysis of normal and treated oocytes indicated a stage-specific association between the spatial distribution of chromosomes and mitochondria. Transfer of individual bivalent chromosomes to untreated oocytes at different stages of maturation and to cytoplasts derived from oocytes anucleated prior to GVB demonstrated the necessity of chromosomes for cytoplasmic and plasma membrane differentiation, and that the capacity of the cytoplasm and plasma membrane to differentiate in response to the presence of a chromosome is acquired prior to GVB.