Regulation of Female Folliculogenesis by Tsp1a in Nile Tilapia (Oreochromis niloticus)

<b> </b>TSP1 was reported to be involved in multiple biological processes including the activation of TGF-β signaling pathways and the regulation of angiogenesis during wound repair and tumor growth, while its role in ovarian folliculogenesis remains to be elucidated. In the present stud...

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Main Authors: Mimi Jie, He Ma, Li Zhou, Jiahong Wu, Minghui Li, Xingyong Liu, Deshou Wang
Format: Article
Language:English
Published: MDPI AG 2020-08-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/16/5893
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spelling doaj-372c751e4c82489cbfcd1e9e803771df2020-11-25T03:21:33ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-08-01215893589310.3390/ijms21165893Regulation of Female Folliculogenesis by Tsp1a in Nile Tilapia (Oreochromis niloticus)Mimi Jie0He Ma1Li Zhou2Jiahong Wu3Minghui Li4Xingyong Liu5Deshou Wang6Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing 400715, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, Fujian Province, ChinaKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing 400715, ChinaKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing 400715, ChinaKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing 400715, ChinaKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing 400715, ChinaKey Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Sciences, Southwest University, Chongqing 400715, China<b> </b>TSP1 was reported to be involved in multiple biological processes including the activation of TGF-β signaling pathways and the regulation of angiogenesis during wound repair and tumor growth, while its role in ovarian folliculogenesis remains to be elucidated. In the present study, Tsp1a was found to be expressed in the oogonia and granulosa cells of phase I to phase IV follicles in the ovaries of Nile tilapia by immunofluorescence. <i>tsp1a</i> homozygous mutants were generated by CRISPR/Cas9. Mutation of <i>tsp1a</i> resulted in increased oogonia, reduced secondary growth follicles and delayed ovary development. Expression of the cell proliferation marker PCNA was significantly up-regulated in the oogonia of the mutant ovaries. Furthermore, transcriptomic analysis revealed that expressions of DNA replication related genes were significantly up-regulated, while cAMP and MAPK signaling pathway genes which inhibit cell proliferation and promote cell differentiation were significantly down-regulated. In addition, aromatase (Cyp19a1a) expression and serum 17β-estradiol (E2) concentration were significantly decreased in the mutants. These results indicated that lacking <i>tsp1a</i> resulted in increased proliferation and inhibited differentiation of oogonia, which in turn, resulted in increased oogonia, reduced secondary growth follicles and decreased E2. Taken together, our results indicated that <i>tsp1a</i> was essential for ovarian folliculogenesis in Nile tilapia.https://www.mdpi.com/1422-0067/21/16/5893Nile tilapiathrombospondin1CRISPR/Cas9folliculogenesis
collection DOAJ
language English
format Article
sources DOAJ
author Mimi Jie
He Ma
Li Zhou
Jiahong Wu
Minghui Li
Xingyong Liu
Deshou Wang
spellingShingle Mimi Jie
He Ma
Li Zhou
Jiahong Wu
Minghui Li
Xingyong Liu
Deshou Wang
Regulation of Female Folliculogenesis by Tsp1a in Nile Tilapia (Oreochromis niloticus)
International Journal of Molecular Sciences
Nile tilapia
thrombospondin1
CRISPR/Cas9
folliculogenesis
author_facet Mimi Jie
He Ma
Li Zhou
Jiahong Wu
Minghui Li
Xingyong Liu
Deshou Wang
author_sort Mimi Jie
title Regulation of Female Folliculogenesis by Tsp1a in Nile Tilapia (Oreochromis niloticus)
title_short Regulation of Female Folliculogenesis by Tsp1a in Nile Tilapia (Oreochromis niloticus)
title_full Regulation of Female Folliculogenesis by Tsp1a in Nile Tilapia (Oreochromis niloticus)
title_fullStr Regulation of Female Folliculogenesis by Tsp1a in Nile Tilapia (Oreochromis niloticus)
title_full_unstemmed Regulation of Female Folliculogenesis by Tsp1a in Nile Tilapia (Oreochromis niloticus)
title_sort regulation of female folliculogenesis by tsp1a in nile tilapia (oreochromis niloticus)
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1661-6596
1422-0067
publishDate 2020-08-01
description <b> </b>TSP1 was reported to be involved in multiple biological processes including the activation of TGF-β signaling pathways and the regulation of angiogenesis during wound repair and tumor growth, while its role in ovarian folliculogenesis remains to be elucidated. In the present study, Tsp1a was found to be expressed in the oogonia and granulosa cells of phase I to phase IV follicles in the ovaries of Nile tilapia by immunofluorescence. <i>tsp1a</i> homozygous mutants were generated by CRISPR/Cas9. Mutation of <i>tsp1a</i> resulted in increased oogonia, reduced secondary growth follicles and delayed ovary development. Expression of the cell proliferation marker PCNA was significantly up-regulated in the oogonia of the mutant ovaries. Furthermore, transcriptomic analysis revealed that expressions of DNA replication related genes were significantly up-regulated, while cAMP and MAPK signaling pathway genes which inhibit cell proliferation and promote cell differentiation were significantly down-regulated. In addition, aromatase (Cyp19a1a) expression and serum 17β-estradiol (E2) concentration were significantly decreased in the mutants. These results indicated that lacking <i>tsp1a</i> resulted in increased proliferation and inhibited differentiation of oogonia, which in turn, resulted in increased oogonia, reduced secondary growth follicles and decreased E2. Taken together, our results indicated that <i>tsp1a</i> was essential for ovarian folliculogenesis in Nile tilapia.
topic Nile tilapia
thrombospondin1
CRISPR/Cas9
folliculogenesis
url https://www.mdpi.com/1422-0067/21/16/5893
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