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Characterization of a novel species-specific 51-amino acid peptide, PEP51, as a caspase-3/7 activator in ovarian follicles of the ascidian, Ciona intestinalis Type A

Invertebrates lack hypothalamic-pituitary-gonadal axis, and have acquired species-specific regulatory systems for ovarian follicle development. Ascidians are marine invertebrates that are the phylogenetically closest living relatives to vertebrates, and we have thus far substantiated the molecular m...

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Autores principales: Sakai, Tsubasa, Yamamoto, Tatsuya, Watanabe, Takehiro, Hozumi, Akiko, Shiraishi, Akira, Osugi, Tomohiro, Matsubara, Shin, Kawada, Tsuyoshi, Sasakura, Yasunori, Takahashi, Toshio, Satake, Honoo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10570924/
https://www.ncbi.nlm.nih.gov/pubmed/37842312
http://dx.doi.org/10.3389/fendo.2023.1260600
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author Sakai, Tsubasa
Yamamoto, Tatsuya
Watanabe, Takehiro
Hozumi, Akiko
Shiraishi, Akira
Osugi, Tomohiro
Matsubara, Shin
Kawada, Tsuyoshi
Sasakura, Yasunori
Takahashi, Toshio
Satake, Honoo
author_facet Sakai, Tsubasa
Yamamoto, Tatsuya
Watanabe, Takehiro
Hozumi, Akiko
Shiraishi, Akira
Osugi, Tomohiro
Matsubara, Shin
Kawada, Tsuyoshi
Sasakura, Yasunori
Takahashi, Toshio
Satake, Honoo
author_sort Sakai, Tsubasa
collection PubMed
description Invertebrates lack hypothalamic-pituitary-gonadal axis, and have acquired species-specific regulatory systems for ovarian follicle development. Ascidians are marine invertebrates that are the phylogenetically closest living relatives to vertebrates, and we have thus far substantiated the molecular mechanisms underlying neuropeptidergic follicle development of the cosmopolitan species, Ciona intestinalis Type A. However, no ovarian factor has so far been identified in Ciona. In the present study, we identified a novel Ciona-specific peptide, termed PEP51, in the ovary. Immunohistochemical analysis demonstrated the specific expression of PEP51 in oocyte-associated accessory cells, test cells, of post-vitellogenic (stage III) follicles. Immunoelectron microscopy revealed that PEP51 was localized in the cytosol of test cells in early stage III follicles, which lack secretory granules. These results indicate that PEP51 acts as an intracellular factor within test cells rather than as a secretory peptide. Confocal laser microscopy verified that activation of caspase-3/7, the canonical apoptosis marker, was detected in most PEP51-positive test cells of early stage III. This colocalization of PEP51 and the apoptosis marker was consistent with immunoelectron microscopy observations demonstrating that a few normal (PEP51-negative) test cells reside in the aggregates of PEP51-positive apoptotic test cells of early stage III follicles. Furthermore, transfection of the PEP51 gene into COS-7 cells and HEK293MSR cells resulted in activation of caspase-3/7, providing evidence that PEP51 induces apoptotic signaling. Collectively, these results showed the existence of species-specific ovarian peptide-driven cell metabolism in Ciona follicle development. Consistent with the phylogenetic position of Ciona as the closest sister group of vertebrates, the present study sheds new light on the molecular and functional diversity of the regulatory systems of follicle development in the Chordata.
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spelling pubmed-105709242023-10-14 Characterization of a novel species-specific 51-amino acid peptide, PEP51, as a caspase-3/7 activator in ovarian follicles of the ascidian, Ciona intestinalis Type A Sakai, Tsubasa Yamamoto, Tatsuya Watanabe, Takehiro Hozumi, Akiko Shiraishi, Akira Osugi, Tomohiro Matsubara, Shin Kawada, Tsuyoshi Sasakura, Yasunori Takahashi, Toshio Satake, Honoo Front Endocrinol (Lausanne) Endocrinology Invertebrates lack hypothalamic-pituitary-gonadal axis, and have acquired species-specific regulatory systems for ovarian follicle development. Ascidians are marine invertebrates that are the phylogenetically closest living relatives to vertebrates, and we have thus far substantiated the molecular mechanisms underlying neuropeptidergic follicle development of the cosmopolitan species, Ciona intestinalis Type A. However, no ovarian factor has so far been identified in Ciona. In the present study, we identified a novel Ciona-specific peptide, termed PEP51, in the ovary. Immunohistochemical analysis demonstrated the specific expression of PEP51 in oocyte-associated accessory cells, test cells, of post-vitellogenic (stage III) follicles. Immunoelectron microscopy revealed that PEP51 was localized in the cytosol of test cells in early stage III follicles, which lack secretory granules. These results indicate that PEP51 acts as an intracellular factor within test cells rather than as a secretory peptide. Confocal laser microscopy verified that activation of caspase-3/7, the canonical apoptosis marker, was detected in most PEP51-positive test cells of early stage III. This colocalization of PEP51 and the apoptosis marker was consistent with immunoelectron microscopy observations demonstrating that a few normal (PEP51-negative) test cells reside in the aggregates of PEP51-positive apoptotic test cells of early stage III follicles. Furthermore, transfection of the PEP51 gene into COS-7 cells and HEK293MSR cells resulted in activation of caspase-3/7, providing evidence that PEP51 induces apoptotic signaling. Collectively, these results showed the existence of species-specific ovarian peptide-driven cell metabolism in Ciona follicle development. Consistent with the phylogenetic position of Ciona as the closest sister group of vertebrates, the present study sheds new light on the molecular and functional diversity of the regulatory systems of follicle development in the Chordata. Frontiers Media S.A. 2023-09-29 /pmc/articles/PMC10570924/ /pubmed/37842312 http://dx.doi.org/10.3389/fendo.2023.1260600 Text en Copyright © 2023 Sakai, Yamamoto, Watanabe, Hozumi, Shiraishi, Osugi, Matsubara, Kawada, Sasakura, Takahashi and Satake https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Endocrinology
Sakai, Tsubasa
Yamamoto, Tatsuya
Watanabe, Takehiro
Hozumi, Akiko
Shiraishi, Akira
Osugi, Tomohiro
Matsubara, Shin
Kawada, Tsuyoshi
Sasakura, Yasunori
Takahashi, Toshio
Satake, Honoo
Characterization of a novel species-specific 51-amino acid peptide, PEP51, as a caspase-3/7 activator in ovarian follicles of the ascidian, Ciona intestinalis Type A
title Characterization of a novel species-specific 51-amino acid peptide, PEP51, as a caspase-3/7 activator in ovarian follicles of the ascidian, Ciona intestinalis Type A
title_full Characterization of a novel species-specific 51-amino acid peptide, PEP51, as a caspase-3/7 activator in ovarian follicles of the ascidian, Ciona intestinalis Type A
title_fullStr Characterization of a novel species-specific 51-amino acid peptide, PEP51, as a caspase-3/7 activator in ovarian follicles of the ascidian, Ciona intestinalis Type A
title_full_unstemmed Characterization of a novel species-specific 51-amino acid peptide, PEP51, as a caspase-3/7 activator in ovarian follicles of the ascidian, Ciona intestinalis Type A
title_short Characterization of a novel species-specific 51-amino acid peptide, PEP51, as a caspase-3/7 activator in ovarian follicles of the ascidian, Ciona intestinalis Type A
title_sort characterization of a novel species-specific 51-amino acid peptide, pep51, as a caspase-3/7 activator in ovarian follicles of the ascidian, ciona intestinalis type a
topic Endocrinology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10570924/
https://www.ncbi.nlm.nih.gov/pubmed/37842312
http://dx.doi.org/10.3389/fendo.2023.1260600
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