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

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...

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Main Authors: Shin Matsubara, Akira Shiraishi, Tomohiro Osugi, Tsuyoshi Kawada, Honoo Satake
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/49062
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author Shin Matsubara
Akira Shiraishi
Tomohiro Osugi
Tsuyoshi Kawada
Honoo Satake
author_facet Shin Matsubara
Akira Shiraishi
Tomohiro Osugi
Tsuyoshi Kawada
Honoo Satake
author_sort Shin Matsubara
collection DOAJ
description 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.
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spelling doaj.art-e65d0aef59354dcaab66c9d53f66235d2022-12-22T03:52:08ZengeLife Sciences Publications LtdeLife2050-084X2019-10-01810.7554/eLife.49062The regulation of oocyte maturation and ovulation in the closest sister group of vertebratesShin Matsubara0https://orcid.org/0000-0002-7794-534XAkira Shiraishi1https://orcid.org/0000-0003-3456-3074Tomohiro Osugi2https://orcid.org/0000-0001-6987-9576Tsuyoshi Kawada3Honoo Satake4https://orcid.org/0000-0003-1165-3624Bioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, Japan; Research Fellow of Japan Society for the Promotion of Science, Tokyo, JapanBioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, JapanBioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, JapanBioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, JapanBioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, JapanAscidians 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.https://elifesciences.org/articles/49062ovulationfolliclematurationvasopressin
spellingShingle Shin Matsubara
Akira Shiraishi
Tomohiro Osugi
Tsuyoshi Kawada
Honoo Satake
The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
eLife
ovulation
follicle
maturation
vasopressin
title The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
title_full The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
title_fullStr The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
title_full_unstemmed The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
title_short The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
title_sort regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
topic ovulation
follicle
maturation
vasopressin
url https://elifesciences.org/articles/49062
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