Cionin, a vertebrate cholecystokinin/gastrin homolog, induces ovulation in the ascidian Ciona intestinalis type A
Abstract Cionin is a homolog of vertebrate cholecystokinin/gastrin that has been identified in the ascidian Ciona intestinalis type A. The phylogenetic position of ascidians as the closest living relatives of vertebrates suggests that cionin can provide clues to the evolution of endocrine/neuroendoc...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2021-05-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-021-90295-3 |
| _version_ | 1818400693887696896 |
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| author | Tomohiro Osugi Natsuko Miyasaka Akira Shiraishi Shin Matsubara Honoo Satake |
| author_facet | Tomohiro Osugi Natsuko Miyasaka Akira Shiraishi Shin Matsubara Honoo Satake |
| author_sort | Tomohiro Osugi |
| collection | DOAJ |
| description | Abstract Cionin is a homolog of vertebrate cholecystokinin/gastrin that has been identified in the ascidian Ciona intestinalis type A. The phylogenetic position of ascidians as the closest living relatives of vertebrates suggests that cionin can provide clues to the evolution of endocrine/neuroendocrine systems throughout chordates. Here, we show the biological role of cionin in the regulation of ovulation. In situ hybridization demonstrated that the mRNA of the cionin receptor, Cior2, was expressed specifically in the inner follicular cells of pre-ovulatory follicles in the Ciona ovary. Cionin was found to significantly stimulate ovulation after 24-h incubation. Transcriptome and subsequent Real-time PCR analyses confirmed that the expression levels of receptor tyrosine kinase (RTK) signaling genes and a matrix metalloproteinase (MMP) gene were significantly elevated in the cionin-treated follicles. Of particular interest is that an RTK inhibitor and MMP inhibitor markedly suppressed the stimulatory effect of cionin on ovulation. Furthermore, inhibition of RTK signaling reduced the MMP gene expression in the cionin-treated follicles. These results provide evidence that cionin induces ovulation by stimulating MMP gene expression via the RTK signaling pathway. This is the first report on the endogenous roles of cionin and the induction of ovulation by cholecystokinin/gastrin family peptides in an organism. |
| first_indexed | 2024-12-14T07:40:38Z |
| format | Article |
| id | doaj.art-ac4e618fa9304bbca129af9abc9d436e |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-14T07:40:38Z |
| publishDate | 2021-05-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-ac4e618fa9304bbca129af9abc9d436e2022-12-21T23:11:02ZengNature PortfolioScientific Reports2045-23222021-05-0111111210.1038/s41598-021-90295-3Cionin, a vertebrate cholecystokinin/gastrin homolog, induces ovulation in the ascidian Ciona intestinalis type ATomohiro Osugi0Natsuko Miyasaka1Akira Shiraishi2Shin Matsubara3Honoo Satake4Division of Integrative Biomolecular Function, Suntory Foundation for Life SciencesBioorganic Research InstituteDivision of Integrative Biomolecular Function, Suntory Foundation for Life SciencesBioorganic Research InstituteDivision of Integrative Biomolecular Function, Suntory Foundation for Life SciencesBioorganic Research InstituteDivision of Integrative Biomolecular Function, Suntory Foundation for Life SciencesBioorganic Research InstituteDivision of Integrative Biomolecular Function, Suntory Foundation for Life SciencesBioorganic Research InstituteAbstract Cionin is a homolog of vertebrate cholecystokinin/gastrin that has been identified in the ascidian Ciona intestinalis type A. The phylogenetic position of ascidians as the closest living relatives of vertebrates suggests that cionin can provide clues to the evolution of endocrine/neuroendocrine systems throughout chordates. Here, we show the biological role of cionin in the regulation of ovulation. In situ hybridization demonstrated that the mRNA of the cionin receptor, Cior2, was expressed specifically in the inner follicular cells of pre-ovulatory follicles in the Ciona ovary. Cionin was found to significantly stimulate ovulation after 24-h incubation. Transcriptome and subsequent Real-time PCR analyses confirmed that the expression levels of receptor tyrosine kinase (RTK) signaling genes and a matrix metalloproteinase (MMP) gene were significantly elevated in the cionin-treated follicles. Of particular interest is that an RTK inhibitor and MMP inhibitor markedly suppressed the stimulatory effect of cionin on ovulation. Furthermore, inhibition of RTK signaling reduced the MMP gene expression in the cionin-treated follicles. These results provide evidence that cionin induces ovulation by stimulating MMP gene expression via the RTK signaling pathway. This is the first report on the endogenous roles of cionin and the induction of ovulation by cholecystokinin/gastrin family peptides in an organism.https://doi.org/10.1038/s41598-021-90295-3 |
| spellingShingle | Tomohiro Osugi Natsuko Miyasaka Akira Shiraishi Shin Matsubara Honoo Satake Cionin, a vertebrate cholecystokinin/gastrin homolog, induces ovulation in the ascidian Ciona intestinalis type A Scientific Reports |
| title | Cionin, a vertebrate cholecystokinin/gastrin homolog, induces ovulation in the ascidian Ciona intestinalis type A |
| title_full | Cionin, a vertebrate cholecystokinin/gastrin homolog, induces ovulation in the ascidian Ciona intestinalis type A |
| title_fullStr | Cionin, a vertebrate cholecystokinin/gastrin homolog, induces ovulation in the ascidian Ciona intestinalis type A |
| title_full_unstemmed | Cionin, a vertebrate cholecystokinin/gastrin homolog, induces ovulation in the ascidian Ciona intestinalis type A |
| title_short | Cionin, a vertebrate cholecystokinin/gastrin homolog, induces ovulation in the ascidian Ciona intestinalis type A |
| title_sort | cionin a vertebrate cholecystokinin gastrin homolog induces ovulation in the ascidian ciona intestinalis type a |
| url | https://doi.org/10.1038/s41598-021-90295-3 |
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