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Perivascular cells support folliculogenesis in the developing ovary

Supporting cells of the ovary, termed granulosa cells, are essential for ovarian differentiation and oogenesis by providing a nurturing environment for oocyte maintenance and maturation. Granulosa cells are specified in the fetal and perinatal ovary, and sufficient numbers of granulosa cells are cri...

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Autores principales: Li, Shu-Yun, Bhandary, Bidur, Gu, Xiaowei, DeFalco, Tony
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9564831/
https://www.ncbi.nlm.nih.gov/pubmed/36194632
http://dx.doi.org/10.1073/pnas.2213026119
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author Li, Shu-Yun
Bhandary, Bidur
Gu, Xiaowei
DeFalco, Tony
author_facet Li, Shu-Yun
Bhandary, Bidur
Gu, Xiaowei
DeFalco, Tony
author_sort Li, Shu-Yun
collection PubMed
description Supporting cells of the ovary, termed granulosa cells, are essential for ovarian differentiation and oogenesis by providing a nurturing environment for oocyte maintenance and maturation. Granulosa cells are specified in the fetal and perinatal ovary, and sufficient numbers of granulosa cells are critical for the establishment of follicles and the oocyte reserve. Identifying the cellular source from which granulosa cells and their progenitors are derived is an integral part of efforts to understand basic ovarian biology and the etiology of female infertility. In particular, the contribution of mesenchymal cells, especially perivascular cells, to ovarian development is poorly understood but is likely to be a source of new information regarding ovarian function. Here we have identified a cell population in the fetal ovary, which is a Nestin-expressing perivascular cell type. Using lineage tracing and ex vivo organ culture methods, we determined that perivascular cells are multipotent progenitors that contribute to granulosa, thecal, and pericyte cell lineages in the ovary. Maintenance of these progenitors is dependent on ovarian vasculature, likely reliant on endothelial–mesenchymal Notch signaling interactions. Depletion of Nestin(+) progenitors resulted in a disruption of granulosa cell specification and in an increased number of germ cell cysts that fail to break down, leading to polyovular ovarian follicles. These findings highlight a cell population in the ovary and uncover a key role for vasculature in ovarian differentiation, which may lead to insights into the origins of female gonad dysgenesis and infertility.
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spelling pubmed-95648312023-04-04 Perivascular cells support folliculogenesis in the developing ovary Li, Shu-Yun Bhandary, Bidur Gu, Xiaowei DeFalco, Tony Proc Natl Acad Sci U S A Biological Sciences Supporting cells of the ovary, termed granulosa cells, are essential for ovarian differentiation and oogenesis by providing a nurturing environment for oocyte maintenance and maturation. Granulosa cells are specified in the fetal and perinatal ovary, and sufficient numbers of granulosa cells are critical for the establishment of follicles and the oocyte reserve. Identifying the cellular source from which granulosa cells and their progenitors are derived is an integral part of efforts to understand basic ovarian biology and the etiology of female infertility. In particular, the contribution of mesenchymal cells, especially perivascular cells, to ovarian development is poorly understood but is likely to be a source of new information regarding ovarian function. Here we have identified a cell population in the fetal ovary, which is a Nestin-expressing perivascular cell type. Using lineage tracing and ex vivo organ culture methods, we determined that perivascular cells are multipotent progenitors that contribute to granulosa, thecal, and pericyte cell lineages in the ovary. Maintenance of these progenitors is dependent on ovarian vasculature, likely reliant on endothelial–mesenchymal Notch signaling interactions. Depletion of Nestin(+) progenitors resulted in a disruption of granulosa cell specification and in an increased number of germ cell cysts that fail to break down, leading to polyovular ovarian follicles. These findings highlight a cell population in the ovary and uncover a key role for vasculature in ovarian differentiation, which may lead to insights into the origins of female gonad dysgenesis and infertility. National Academy of Sciences 2022-10-04 2022-10-11 /pmc/articles/PMC9564831/ /pubmed/36194632 http://dx.doi.org/10.1073/pnas.2213026119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Li, Shu-Yun
Bhandary, Bidur
Gu, Xiaowei
DeFalco, Tony
Perivascular cells support folliculogenesis in the developing ovary
title Perivascular cells support folliculogenesis in the developing ovary
title_full Perivascular cells support folliculogenesis in the developing ovary
title_fullStr Perivascular cells support folliculogenesis in the developing ovary
title_full_unstemmed Perivascular cells support folliculogenesis in the developing ovary
title_short Perivascular cells support folliculogenesis in the developing ovary
title_sort perivascular cells support folliculogenesis in the developing ovary
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9564831/
https://www.ncbi.nlm.nih.gov/pubmed/36194632
http://dx.doi.org/10.1073/pnas.2213026119
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