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

  1. Shin Matsubara
  2. Akira Shiraishi
  3. Tomohiro Osugi
  4. Tsuyoshi Kawada
  5. Honoo Satake  Is a corresponding author
  1. Suntory Foundation for Life Sciences, Japan

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.

Data availability

All data generated or analyzed in this study are included in the manuscript and supporting files. Accession numbers of RNA-seq data in this study are described in Table 1 and Table 2. All RNA seq-data are provided in Supplementary file 1 and 4.

Article and author information

Author details

  1. Shin Matsubara

    Bioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Akira Shiraishi

    Bioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Tomohiro Osugi

    Bioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6987-9576
  4. Tsuyoshi Kawada

    Bioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Honoo Satake

    Bioorganic Research Institute, Suntory Foundation for Life Sciences, Kyoto, Japan
    For correspondence
    satake@sunbor.or.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1165-3624

Funding

Japan Society for the Promotion of Science (JP16K07430)

  • Honoo Satake

Japan Society for the Promotion of Science (JP16K18581)

  • Shin Matsubara

Japan Society for the Promotion of Science (JP17J10624)

  • Shin Matsubara

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Yukiko M Yamashita, University of Michigan, United States

Version history

  1. Received: June 5, 2019
  2. Accepted: September 26, 2019
  3. Accepted Manuscript published: October 1, 2019 (version 1)
  4. Version of Record published: October 10, 2019 (version 2)

Copyright

© 2019, Matsubara et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Shin Matsubara
  2. Akira Shiraishi
  3. Tomohiro Osugi
  4. Tsuyoshi Kawada
  5. Honoo Satake
(2019)
The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates
eLife 8:e49062.
https://doi.org/10.7554/eLife.49062

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

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