Abstract
During oocyte development, meiosis arrests in prophase of the first division for a remarkably prolonged period firstly during oocyte growth, and then when awaiting the appropriate hormonal signals for egg release. This prophase arrest is finally unlocked when locally produced maturation initiation hormones (MIHs) trigger entry into M-phase. Here, we assess the current knowledge of the successive cellular and molecular mechanisms responsible for keeping meiotic progression on hold. We focus on two model organisms, the amphibian Xenopus laevis, and the hydrozoan jellyfish Clytia hemisphaerica. Conserved mechanisms govern the initial meiotic programme of the oocyte prior to oocyte growth and also, much later, the onset of mitotic divisions, via activation of two key kinase systems: Cdk1-Cyclin B/Gwl (MPF) for M-phase activation and Mos-MAPkinase to orchestrate polar body formation and cytostatic (CSF) arrest. In contrast, maintenance of the prophase state of the fully-grown oocyte is assured by highly specific mechanisms, reflecting enormous variation between species in MIHs, MIH receptors and their immediate downstream signalling response. Convergence of multiple signalling pathway components to promote MPF activation in some oocytes, including Xenopus, is likely a heritage of the complex evolutionary history of spawning regulation, but also helps ensure a robust and reliable mechanism for gamete production.
Highlights
Successful embryonic development following fertilisation in all animals critically depends on the quality of the gametes
After female jellyfish bud from the colony and start to feed and grow, small developing gonads first can be recognised within one week, as Nanos/Piwi-expressing cells positioned at the sites of gonad formation on the four radial canals embark on oogenesis
We outline here recent advances in Xenopus and Clytia in the understanding of the oocyte receptors that respond to maturation initiation hormones (MIHs) stimuli upstream of cAMP, and of the PKA substrates that link this to maturation promoting factor (MPF) activation
Summary
Successful embryonic development following fertilisation in all animals critically depends on the quality of the gametes. The first meiotic division arrests for prolonged periods at the diplotene stage, which depending on species can last days, weeks, months or years During this long-lasting arrest, the oocytes grow enormously, accumulating all the molecular reserves required for the early embryonic development. For example, hormonal readouts of stress and nutritional balance converge to regulate the production of gonadotropins along the Hypothalamic–Pituitary–Gonadal axis, culminating with release of Luteinising Hormone (LH) from the pituitary to stimulate the oocyte follicle cells [6] Local signals from these follicle cells (or equivalent cells in other animals) act on the oocyte to trigger meiotic maturation. Fully-grown oocytes develop a responsiveness to specialised MIH signals that initiates the maturation process only when the physiological and environmental conditions are favourable
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