Meiosis and oogenesis

Abstract

Molecular Biology of the CellVol. 23, No. 6 ASCB Annual Meeting HighlightsFree AccessMeiosis and oogenesisMarie-Hélène VerlhacMarie-Hélène VerlhacSearch for more papers by this authorPublished Online:13 Oct 2017https://doi.org/10.1091/mbc.e11-12-0982AboutSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail A minisymposium at the 2011 meeting of the American Society for Cell Biology presented recent advances in the field of meiosis and oogenesis (Figure 1).FIGURE 1: Scheme of meiosis in mouse oocytes. Homologous chromosome pairing, synapsis, and recombination take place in prophase I. Oocyte: light gray; maternal and paternal chromosomes: blue and violet; nucleus: dark gray; nuclear envelope breakdown: dotted line; spindle: green.How does the follicle coordinate meiosis progression?The ovarian follicle is an integrated system in which follicular cells regulate oocyte progression into meiosis. Oocytes are large cells that divide asymmetrically to preserve stores for future embryonic development. To do this, they must coordinate asymmetric spindle positioning with cell cycle progression and chromosome segregation. In mammals, the luteinizing hormone signaling induces a drop in cyclic guanosine monophosphate (cGMP) levels in the granulosa cells surrounding the oocyte. As discussed by Laurinda Jaffe, this drop in cGMP is due to a decrease in guanylyl cyclase-B activity in these cells. As a consequence, the phosphodiesterase PDE3A activity is no longer inhibited in oocytes, leading to a drop in cAMP levels and thus triggering a drop in protein kinase A activity and subsequent activation of cyclin B/cyclin-dependent kinase 1 (CDK1), a prerequisite for meiotic resumption. Takeo Kishimoto presented evidence that robust meiotic resumption in starfish oocytes not only requires cyclin B/CDK1 activation but also depends on Greatwall kinase activity.How does F-actin control chromosome positioning?Starfish oocytes gather their condensing chromosomes, dispersed in an 80-μm-wide nucleus, using an F-actin fishnet, which contracts isotropically (as described by Péter Lénárt). At nuclear envelope breakdown, this mesh is anchored to the animal pole at which the centrosomes reside, which provides directionality to the general motion of chromosomes. Furthermore, chromosomes at the border of the meshwork induce larger patches of F-actin in a RanGTP-dependent manner, reminiscent of the effect of chromatin on the cortex in mouse oocytes. This actin mesh delivers chromosomes that are beyond the reach of microtubules to the centrosomes for spindle assembly and asymmetric division. Similarly, Marie-Emilie Terret presented evidence that the coordination between two F-actin meshworks in mouse oocytes allows positioning of the first meiotic spindle to the cortex at the end of meiosis I. Indeed, an Arp2/3-dependent thickening of the cortex occurs in meiosis I; this is essential for first meiotic spindle migration. These cortical filaments create a border between cytoplasmic and cortical F-actin. Therefore, in both starfish and mouse, a contractile F-actin meshwork delivers chromosomes to the cortex. In starfish, it is anchored on remnants of the nuclear envelope, such that its contractions do not deform the plasma membrane. In mouse oocytes, it is anchored to the cortex, and cortical thickening thus acts as a barrier protecting the plasma membrane from intracellular F-actin contractions.Is there loading of cohesin after S-phase during the arrest in prophase I?Female gamete formation, which in mammals starts in the embryo and ends during adulthood, necessitates adaptations specific to a process extending over a prolonged period. Recent studies in mouse have suggested that sister chromatid cohesion is lost in aging females and that there is no turnover of cohesins during the growth phase, potentially explaining the increased error rate of chromosome segregation in human oocytes. Both Sharon Bickel and Aaron Severson provided compelling evidence that cohesins can be reloaded after the last round of DNA replication in prophase I of meiosis. Severson showed that in nematodes, cohesin complexes that associate with two new kleisin subunits (COH-3 and COH-4) load onto chromosomes after premeiotic DNA replication is complete and are triggered to establish sister chromatid cohesion by the Spo11-induced DNA double-strand breaks that initiate crossover recombination. Sharon Bickel showed that the acetyltransferase Drosophila homologue of Eco1 (Deco), which is necessary for cohesion establishment during S-phase, is also required during meiotic prophase for maintenance of chiasmata. Loss of Deco after meiotic S phase results in loss of chiasma maintenance and increased levels of nondisjunction. Bickel's work suggests that two pathways could promote increased incidence of errors in aging females: progressive loss of cohesion and loss of cohesion reloading during prophase I.FOOTNOTESDOI: 10.1091/mbc.E11-12-0982FiguresReferencesRelatedDetails Vol. 23, No. 6 March 15, 2012965-1140 Metrics Downloads & Citations Downloads: 180 History Information© 2012 Verlhac. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0).PDF download