The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates.

Shin Matsubara,Akira Shiraishi,Tomohiro Osugi,Tsuyoshi Kawada,Honoo Satake

doi:10.7554/elife.49062

Shin Matsubara, Akira Shiraishi + Show 3 more

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https://doi.org/10.7554/elife.49062

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Abstract

Ascidians are the closest living relatives of vertebrates, and their study is important for understanding the evolutionary processes of oocyte maturation and ovulation. In this study, we first examined the ovulation of Ciona intestinalis Type A by monitoring follicle rupture in vitro, identifying a novel mechanism of neuropeptidergic regulation of oocyte maturation and ovulation. Ciona vasopressin family peptide (CiVP) directly upregulated the phosphorylation of extracellular signal-regulated kinase (CiErk1/2) via its receptor. CiVP ultimately activated a maturation-promoting factor, leading to oocyte maturation via germinal vesicle breakdown. CiErk1/2 also induced expression of matrix metalloproteinase (CiMMP2/9/13) in the oocyte, resulting in collagen degradation in the outer follicular cell layer and liberation of fertile oocytes from the ovary. This is the first demonstration of essential pathways regulating oocyte maturation and ovulation in ascidians and will facilitate investigations of the evolutionary process of peptidergic regulation of oocyte maturation and ovulation throughout the phylum Chordata.

Highlights

Oocyte maturation and ovulation are critical steps in the completion of female gametogenesis in the ovary and for subsequent fertilization and embryogenesis (Lane et al, 2014)
Time-lapse imaging revealed that follicle liberation followed the rupture of the outer follicular cell layer (Figure 1B and Video 1), and we defined this phenomenon as Ciona ovulation. Such rupture of outer follicular cells was observed in an isolated follicle following germinal vesicle breakdown (GVBD) (Figure 1C and Video 2). These results demonstrated that both oocyte maturation and ovulation can be studied in vitro using isolated immature/pre-ovulatory follicles
We focused on the two major maturation promoting factor (MPF) components, cyclin B (CcnB) and Cdc2 (Cdk1), given that oocyte maturation is triggered by activation of MPF in a wide variety of both vertebrates and invertebrates (Richani and Gilchrist, 2018; Nagahama and Yamashita, 2008; Kishimoto, 2018; Das and Arur, 2017; Fan and Sun, 2004)

Summary

Introduction

Oocyte maturation and ovulation are critical steps in the completion of female gametogenesis in the ovary and for subsequent fertilization and embryogenesis (Lane et al, 2014). Meiosis in animal oocytes is arrested at prophase of the first division (ProI). Hormonal stimulation triggers the resumption of meiosis in most vertebrates and invertebrates, and oocytes undergo nuclear maturation upon the onset of nuclear disassembly (i.e., germinal vesicle breakdown [GVBD]). Their meiosis is arrested again at a species-specific stage: metaphase of the first division (MetI, many invertebrates), metaphase of the second division (MetII, most vertebrates), or G1-phase (some echinoderms and coelenterates) until fertilization. The regulatory mechanisms underlying oocyte maturation and ovulation control the reproduction of the respective organisms and evolutionary processes across the animal kingdom

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