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Dynamic regulation of semaphorin 7A and adhesion receptors in ovarian follicle remodeling and ovulation

The ovarian follicle is a complex structure that protects and helps in the maturation of the oocyte, and then releases it through the controlled molecular and structural remodeling process of ovulation. The progesterone receptor (PGR) has been shown to be essential in regulating ovulation-related ge...

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Autores principales: Emery, Alaknanda, Dunning, Kylie R., Dinh, Doan T., Akison, Lisa K., Robker, Rebecca L., Russell, Darryl L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10628455/
https://www.ncbi.nlm.nih.gov/pubmed/37941899
http://dx.doi.org/10.3389/fcell.2023.1261038
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author Emery, Alaknanda
Dunning, Kylie R.
Dinh, Doan T.
Akison, Lisa K.
Robker, Rebecca L.
Russell, Darryl L.
author_facet Emery, Alaknanda
Dunning, Kylie R.
Dinh, Doan T.
Akison, Lisa K.
Robker, Rebecca L.
Russell, Darryl L.
author_sort Emery, Alaknanda
collection PubMed
description The ovarian follicle is a complex structure that protects and helps in the maturation of the oocyte, and then releases it through the controlled molecular and structural remodeling process of ovulation. The progesterone receptor (PGR) has been shown to be essential in regulating ovulation-related gene expression changes. In this study, we found disrupted expression of the cellular adhesion receptor gene Sema7A in the granulosa cells of PGR(−/−) mice during ovulation. We subsequently found that expression of Sema7A in preovulatory follicles is promoted by gonadotropins and hypoxia, establishing an asymmetrical pattern with the SEMA7A protein enriched at the apex of large antral follicles. Sema7A expression was downregulated through a PGR-dependent mechanism in the periovulatory period, the abundance of SEMA7A protein was reduced, and the asymmetric pattern became more homogeneous after an ovulatory stimulus. Receptors for Sema7A can either repel or promote intercellular adhesion. During ovulation, striking inverse regulation of repulsive Plxnc1 and adhesive Itga5/Itgb1 receptors likely contributes to dramatic tissue remodeling. The adhesive receptor Itga5 was significantly increased in periovulatory granulosa cells and cumulus–oocyte complexes (COCs), and functional assays showed that periovulatory granulosa cells and COCs acquire increased adhesive phenotypes, while Sema7A repels granulosa cell contact. These findings suggest that the regulation of Sema7A and its associated receptors, along with the modulation of integrin α5, may be critical in establishing the multilaminar ovarian follicle structure and facilitating the remodeling and apical release of the cumulus–oocyte complex during ovulation.
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spelling pubmed-106284552023-11-08 Dynamic regulation of semaphorin 7A and adhesion receptors in ovarian follicle remodeling and ovulation Emery, Alaknanda Dunning, Kylie R. Dinh, Doan T. Akison, Lisa K. Robker, Rebecca L. Russell, Darryl L. Front Cell Dev Biol Cell and Developmental Biology The ovarian follicle is a complex structure that protects and helps in the maturation of the oocyte, and then releases it through the controlled molecular and structural remodeling process of ovulation. The progesterone receptor (PGR) has been shown to be essential in regulating ovulation-related gene expression changes. In this study, we found disrupted expression of the cellular adhesion receptor gene Sema7A in the granulosa cells of PGR(−/−) mice during ovulation. We subsequently found that expression of Sema7A in preovulatory follicles is promoted by gonadotropins and hypoxia, establishing an asymmetrical pattern with the SEMA7A protein enriched at the apex of large antral follicles. Sema7A expression was downregulated through a PGR-dependent mechanism in the periovulatory period, the abundance of SEMA7A protein was reduced, and the asymmetric pattern became more homogeneous after an ovulatory stimulus. Receptors for Sema7A can either repel or promote intercellular adhesion. During ovulation, striking inverse regulation of repulsive Plxnc1 and adhesive Itga5/Itgb1 receptors likely contributes to dramatic tissue remodeling. The adhesive receptor Itga5 was significantly increased in periovulatory granulosa cells and cumulus–oocyte complexes (COCs), and functional assays showed that periovulatory granulosa cells and COCs acquire increased adhesive phenotypes, while Sema7A repels granulosa cell contact. These findings suggest that the regulation of Sema7A and its associated receptors, along with the modulation of integrin α5, may be critical in establishing the multilaminar ovarian follicle structure and facilitating the remodeling and apical release of the cumulus–oocyte complex during ovulation. Frontiers Media S.A. 2023-10-24 /pmc/articles/PMC10628455/ /pubmed/37941899 http://dx.doi.org/10.3389/fcell.2023.1261038 Text en Copyright © 2023 Emery, Dunning, Dinh, Akison, Robker and Russell. 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 Cell and Developmental Biology
Emery, Alaknanda
Dunning, Kylie R.
Dinh, Doan T.
Akison, Lisa K.
Robker, Rebecca L.
Russell, Darryl L.
Dynamic regulation of semaphorin 7A and adhesion receptors in ovarian follicle remodeling and ovulation
title Dynamic regulation of semaphorin 7A and adhesion receptors in ovarian follicle remodeling and ovulation
title_full Dynamic regulation of semaphorin 7A and adhesion receptors in ovarian follicle remodeling and ovulation
title_fullStr Dynamic regulation of semaphorin 7A and adhesion receptors in ovarian follicle remodeling and ovulation
title_full_unstemmed Dynamic regulation of semaphorin 7A and adhesion receptors in ovarian follicle remodeling and ovulation
title_short Dynamic regulation of semaphorin 7A and adhesion receptors in ovarian follicle remodeling and ovulation
title_sort dynamic regulation of semaphorin 7a and adhesion receptors in ovarian follicle remodeling and ovulation
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10628455/
https://www.ncbi.nlm.nih.gov/pubmed/37941899
http://dx.doi.org/10.3389/fcell.2023.1261038
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