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The effects of endogenous FSH and its receptor on oogenesis and folliculogenesis in female Alligator sinensis

BACKGROUND: The precise mechanisms of hormone action responsible for the full course of events modulating folliculogenesis in crocodilian have not been determined, although histological features have been identified. RESULTS: The Alligator sinensis ovarian morphological characteristics observed at 1...

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Autores principales: Nie, Haitao, Xu, Yunlu, Zhang, Yuqian, Wen, Yue, Zhan, Jixiang, Xia, Yong, Zhou, Yongkang, Wang, Renping, Wu, Xiaobing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10318752/
https://www.ncbi.nlm.nih.gov/pubmed/37403129
http://dx.doi.org/10.1186/s40850-023-00170-z
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author Nie, Haitao
Xu, Yunlu
Zhang, Yuqian
Wen, Yue
Zhan, Jixiang
Xia, Yong
Zhou, Yongkang
Wang, Renping
Wu, Xiaobing
author_facet Nie, Haitao
Xu, Yunlu
Zhang, Yuqian
Wen, Yue
Zhan, Jixiang
Xia, Yong
Zhou, Yongkang
Wang, Renping
Wu, Xiaobing
author_sort Nie, Haitao
collection PubMed
description BACKGROUND: The precise mechanisms of hormone action responsible for the full course of events modulating folliculogenesis in crocodilian have not been determined, although histological features have been identified. RESULTS: The Alligator sinensis ovarian morphological characteristics observed at 1, 15, 30, 60, 90, and 300 days post hatching(dph) revealed that the dynamic changes in germ cells varied in different meiotic and developmental stages, confirming that the processes of folliculogenesis were protracted and asynchronous. The presence of endogenous follicle-stimulating hormone(FSH) mRNA and protein expression within the cerebrum at 1 dph, in parallel with the increase in germ cells within the germ cell nests(Nest) from 1 dph to 15 dph, suggested that endocrine regulation of the pituitary-gonad axis is an early event in oogonia division. Furthermore, the endogenous expression of FSH showed a trend of negative feedback augmentation accompanied by the exhaustion of maternal yolk E(2) observed at 15 dph. Such significant elevation of endogenous FSH levels was observed to be related to pivotal events in the transition from mitosis to meiosis, as reflected by the proportion of oogonia during premeiosis interphase, with endogenous FSH levels reaching a peak at the earliest time step of 1 dph. In addition, the simultaneous upregulation of premeiotic marker STRA8 mRNA expression and the increase in endogenous FSH further verified the above speculation. The strongly FSHr-positive label in the oocytes within Pre-previtellogenic follicles was synchronized with the significant elevation of ovarian cAMP detected at 300 dph, which suggested that diplotene arrest maintenance during early vitellogenesis might be FSH dependent. In addition, preferential selection in asynchronous meiotic initiation has been supposed to act on somatic supportive cells and not directly on germ cells via regulation of FSH that in turn affects downstream estrogen levels. This suggestion was verified by the reciprocal stimulating effect of FSH and E(2) on the accelerated meiotic marker SYCP3 and by the inhibited cell apoptosis demonstrated in ovarian cell culture in vitro. CONCLUSION: The corresponding results contribute an expansion of the understanding of physiological processes and shed some light on the specific factors responsible for gonadotropin function in the early folliculogenesis of crocodilians. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-023-00170-z.
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spelling pubmed-103187522023-07-05 The effects of endogenous FSH and its receptor on oogenesis and folliculogenesis in female Alligator sinensis Nie, Haitao Xu, Yunlu Zhang, Yuqian Wen, Yue Zhan, Jixiang Xia, Yong Zhou, Yongkang Wang, Renping Wu, Xiaobing BMC Zool Research Article BACKGROUND: The precise mechanisms of hormone action responsible for the full course of events modulating folliculogenesis in crocodilian have not been determined, although histological features have been identified. RESULTS: The Alligator sinensis ovarian morphological characteristics observed at 1, 15, 30, 60, 90, and 300 days post hatching(dph) revealed that the dynamic changes in germ cells varied in different meiotic and developmental stages, confirming that the processes of folliculogenesis were protracted and asynchronous. The presence of endogenous follicle-stimulating hormone(FSH) mRNA and protein expression within the cerebrum at 1 dph, in parallel with the increase in germ cells within the germ cell nests(Nest) from 1 dph to 15 dph, suggested that endocrine regulation of the pituitary-gonad axis is an early event in oogonia division. Furthermore, the endogenous expression of FSH showed a trend of negative feedback augmentation accompanied by the exhaustion of maternal yolk E(2) observed at 15 dph. Such significant elevation of endogenous FSH levels was observed to be related to pivotal events in the transition from mitosis to meiosis, as reflected by the proportion of oogonia during premeiosis interphase, with endogenous FSH levels reaching a peak at the earliest time step of 1 dph. In addition, the simultaneous upregulation of premeiotic marker STRA8 mRNA expression and the increase in endogenous FSH further verified the above speculation. The strongly FSHr-positive label in the oocytes within Pre-previtellogenic follicles was synchronized with the significant elevation of ovarian cAMP detected at 300 dph, which suggested that diplotene arrest maintenance during early vitellogenesis might be FSH dependent. In addition, preferential selection in asynchronous meiotic initiation has been supposed to act on somatic supportive cells and not directly on germ cells via regulation of FSH that in turn affects downstream estrogen levels. This suggestion was verified by the reciprocal stimulating effect of FSH and E(2) on the accelerated meiotic marker SYCP3 and by the inhibited cell apoptosis demonstrated in ovarian cell culture in vitro. CONCLUSION: The corresponding results contribute an expansion of the understanding of physiological processes and shed some light on the specific factors responsible for gonadotropin function in the early folliculogenesis of crocodilians. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-023-00170-z. BioMed Central 2023-07-04 /pmc/articles/PMC10318752/ /pubmed/37403129 http://dx.doi.org/10.1186/s40850-023-00170-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Nie, Haitao
Xu, Yunlu
Zhang, Yuqian
Wen, Yue
Zhan, Jixiang
Xia, Yong
Zhou, Yongkang
Wang, Renping
Wu, Xiaobing
The effects of endogenous FSH and its receptor on oogenesis and folliculogenesis in female Alligator sinensis
title The effects of endogenous FSH and its receptor on oogenesis and folliculogenesis in female Alligator sinensis
title_full The effects of endogenous FSH and its receptor on oogenesis and folliculogenesis in female Alligator sinensis
title_fullStr The effects of endogenous FSH and its receptor on oogenesis and folliculogenesis in female Alligator sinensis
title_full_unstemmed The effects of endogenous FSH and its receptor on oogenesis and folliculogenesis in female Alligator sinensis
title_short The effects of endogenous FSH and its receptor on oogenesis and folliculogenesis in female Alligator sinensis
title_sort effects of endogenous fsh and its receptor on oogenesis and folliculogenesis in female alligator sinensis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10318752/
https://www.ncbi.nlm.nih.gov/pubmed/37403129
http://dx.doi.org/10.1186/s40850-023-00170-z
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