Bisphenol A (BPA) Directly Activates the G Protein-Coupled Estrogen Receptor 1 and Triggers the Metabolic Disruption in the Gonadal Tissue of <i>Apostichopus japonicus</i>

The sea cucumber, <i>Apostichopus japonicus,</i> is a marine benthic organism that feeds on small benthic particulate matter and is easily affected by pollutants. Bisphenol A (BPA, 4,4′-isopropylidenediphenol) has been identified as an endocrine disruptor. It is ubiquitously detectable i...

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Main Authors: Jieyi Yuan, Jingwen Yang, Xiuwen Xu, Zexianghua Wang, Zhijing Jiang, Zhiqing Ye, Yucheng Ren, Qing Wang, Tianming Wang
Format: Article
Language:English
Published: MDPI AG 2023-05-01
Series:Biology
Subjects:
Online Access:https://www.mdpi.com/2079-7737/12/6/798
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author Jieyi Yuan
Jingwen Yang
Xiuwen Xu
Zexianghua Wang
Zhijing Jiang
Zhiqing Ye
Yucheng Ren
Qing Wang
Tianming Wang
author_facet Jieyi Yuan
Jingwen Yang
Xiuwen Xu
Zexianghua Wang
Zhijing Jiang
Zhiqing Ye
Yucheng Ren
Qing Wang
Tianming Wang
author_sort Jieyi Yuan
collection DOAJ
description The sea cucumber, <i>Apostichopus japonicus,</i> is a marine benthic organism that feeds on small benthic particulate matter and is easily affected by pollutants. Bisphenol A (BPA, 4,4′-isopropylidenediphenol) has been identified as an endocrine disruptor. It is ubiquitously detectable in oceans and affects a variety of marine animals. It functions as an estrogen analog and typically causes reproductive toxicity by interfering with the endocrine system. To comparatively analyze the reproductive effects of estradiol (E<sub>2</sub>) and BPA on sea cucumbers, we identified a G protein-coupled estrogen receptor 1 (GPER1) in <i>A. japonicus</i> and investigated its effects on reproduction. The results showed that BPA and E<sub>2</sub> exposure activated <i>A. japonicus</i> AjGPER1, thereby mediating the mitogen-activated protein kinase signaling pathways. High-level expression of <i>AjGPER1</i> in the ovarian tissue was confirmed by qPCR. Furthermore, metabolic changes were induced by 100 nM (22.83 μg/L) BPA exposure in the ovarian tissue, leading to a notable increase in the activities of trehalase and phosphofructokinase. Overall, our findings suggest that AjGPER1 is directly activated by BPA and affects sea cucumber reproduction by disrupting ovarian tissue metabolism, suggesting that marine pollutants pose a threat to the conservation of sea cucumber resources.
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spelling doaj.art-2504a106b4534615b51a7ff330e376552023-11-18T09:22:43ZengMDPI AGBiology2079-77372023-05-0112679810.3390/biology12060798Bisphenol A (BPA) Directly Activates the G Protein-Coupled Estrogen Receptor 1 and Triggers the Metabolic Disruption in the Gonadal Tissue of <i>Apostichopus japonicus</i>Jieyi Yuan0Jingwen Yang1Xiuwen Xu2Zexianghua Wang3Zhijing Jiang4Zhiqing Ye5Yucheng Ren6Qing Wang7Tianming Wang8National Engineering Research Center of Marine Facilities Aquaculture, Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, ChinaResearch and Development Center for Efficient Utilization of Coastal Bioresources, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai 264003, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Marine Science and Technology College, Zhejiang Ocean University, Zhoushan 316022, ChinaThe sea cucumber, <i>Apostichopus japonicus,</i> is a marine benthic organism that feeds on small benthic particulate matter and is easily affected by pollutants. Bisphenol A (BPA, 4,4′-isopropylidenediphenol) has been identified as an endocrine disruptor. It is ubiquitously detectable in oceans and affects a variety of marine animals. It functions as an estrogen analog and typically causes reproductive toxicity by interfering with the endocrine system. To comparatively analyze the reproductive effects of estradiol (E<sub>2</sub>) and BPA on sea cucumbers, we identified a G protein-coupled estrogen receptor 1 (GPER1) in <i>A. japonicus</i> and investigated its effects on reproduction. The results showed that BPA and E<sub>2</sub> exposure activated <i>A. japonicus</i> AjGPER1, thereby mediating the mitogen-activated protein kinase signaling pathways. High-level expression of <i>AjGPER1</i> in the ovarian tissue was confirmed by qPCR. Furthermore, metabolic changes were induced by 100 nM (22.83 μg/L) BPA exposure in the ovarian tissue, leading to a notable increase in the activities of trehalase and phosphofructokinase. Overall, our findings suggest that AjGPER1 is directly activated by BPA and affects sea cucumber reproduction by disrupting ovarian tissue metabolism, suggesting that marine pollutants pose a threat to the conservation of sea cucumber resources.https://www.mdpi.com/2079-7737/12/6/798<i>Apostichopus japonicus</i>reproductionestradiol receptorBisphenol A (BPA)metabolic disruption
spellingShingle Jieyi Yuan
Jingwen Yang
Xiuwen Xu
Zexianghua Wang
Zhijing Jiang
Zhiqing Ye
Yucheng Ren
Qing Wang
Tianming Wang
Bisphenol A (BPA) Directly Activates the G Protein-Coupled Estrogen Receptor 1 and Triggers the Metabolic Disruption in the Gonadal Tissue of <i>Apostichopus japonicus</i>
Biology
<i>Apostichopus japonicus</i>
reproduction
estradiol receptor
Bisphenol A (BPA)
metabolic disruption
title Bisphenol A (BPA) Directly Activates the G Protein-Coupled Estrogen Receptor 1 and Triggers the Metabolic Disruption in the Gonadal Tissue of <i>Apostichopus japonicus</i>
title_full Bisphenol A (BPA) Directly Activates the G Protein-Coupled Estrogen Receptor 1 and Triggers the Metabolic Disruption in the Gonadal Tissue of <i>Apostichopus japonicus</i>
title_fullStr Bisphenol A (BPA) Directly Activates the G Protein-Coupled Estrogen Receptor 1 and Triggers the Metabolic Disruption in the Gonadal Tissue of <i>Apostichopus japonicus</i>
title_full_unstemmed Bisphenol A (BPA) Directly Activates the G Protein-Coupled Estrogen Receptor 1 and Triggers the Metabolic Disruption in the Gonadal Tissue of <i>Apostichopus japonicus</i>
title_short Bisphenol A (BPA) Directly Activates the G Protein-Coupled Estrogen Receptor 1 and Triggers the Metabolic Disruption in the Gonadal Tissue of <i>Apostichopus japonicus</i>
title_sort bisphenol a bpa directly activates the g protein coupled estrogen receptor 1 and triggers the metabolic disruption in the gonadal tissue of i apostichopus japonicus i
topic <i>Apostichopus japonicus</i>
reproduction
estradiol receptor
Bisphenol A (BPA)
metabolic disruption
url https://www.mdpi.com/2079-7737/12/6/798
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