Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary Syndrome
Low-frequency electro-acupuncture (EA) has been shown to restore ovulation in patients with polycystic ovary syndrome (PCOS), and previous animal experiments showed that EA improves ovarian blood flow and angiogenesis. We performed EA for 4 weeks in dihydrotestosterone (DHT)-induced PCOS-like rats a...
| Main Authors: | , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2020-05-01
|
| Series: | Frontiers in Physiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fphys.2020.00474/full |
| _version_ | 1818310700005588992 |
|---|---|
| author | Xiaoyu Tong Yanjun Liu Yanjun Liu Xiaoqing Xu Jiemei Shi Wei Hu Tong Ma Peng Cui Wenhan Lu Zhenle Pei Mingzhen Xu Feifei Zhang Feifei Zhang Xin Li Xin Li Yi Feng |
| author_facet | Xiaoyu Tong Yanjun Liu Yanjun Liu Xiaoqing Xu Jiemei Shi Wei Hu Tong Ma Peng Cui Wenhan Lu Zhenle Pei Mingzhen Xu Feifei Zhang Feifei Zhang Xin Li Xin Li Yi Feng |
| author_sort | Xiaoyu Tong |
| collection | DOAJ |
| description | Low-frequency electro-acupuncture (EA) has been shown to restore ovulation in patients with polycystic ovary syndrome (PCOS), and previous animal experiments showed that EA improves ovarian blood flow and angiogenesis. We performed EA for 4 weeks in dihydrotestosterone (DHT)-induced PCOS-like rats and investigated the three-dimensional (3D) ovarian innervation to determine the role of innervation in folliculogenesis and vascularity. Ovarian tissues were made transparent following the CUBIC 3D tissue-clearing protocol and were immunostained using antibodies against platelet endothelial cell adhesion molecule-1 and tyrosine hydroxylase to visualize the ovarian vasculature and innervation, respectively. This was followed by 3D imaging using lightsheet microscopy and analysis using the Imaris software. In control rats, ovarian innervation increased with age, and the neuronal branching started from the ovarian hilum and reached the individual follicles at different follicle stages. At the individual follicle level, each follicle was mainly innervated by one neuronal fiber. Compared with control rats, ovaries from DHT-treated PCOS-like rats had more antral follicles and fewer preovulatory follicles and corpora lutea. Furthermore, PCOS ovaries showed decreased innervation of blood vessels near the hilum and the surrounding individual antral follicles. EA in PCOS-like rats led to increased numbers of preovulatory follicles and corpora lutea together with increased innervation of blood vessels near the hilum. To determine the role of ovarian innervation, we further performed unilateral sectioning of the superior ovarian nerve (SON) in PCOS + EA rats and found that the left sectioned ovary had fewer preovulatory follicles and corpora lutea compared with those in the right non-sectioned ovary. In conclusion, ovarian innervation likely played an important role in folliculogenesis, and EA might restore PCOS pathophysiology by regulating ovarian innervation, at least partially mediated through the SON. |
| first_indexed | 2024-12-13T07:50:13Z |
| format | Article |
| id | doaj.art-e3af3e81a656496786e88bf244cd4791 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-13T07:50:13Z |
| publishDate | 2020-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-e3af3e81a656496786e88bf244cd47912022-12-21T23:54:42ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-05-011110.3389/fphys.2020.00474526285Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary SyndromeXiaoyu Tong0Yanjun Liu1Yanjun Liu2Xiaoqing Xu3Jiemei Shi4Wei Hu5Tong Ma6Peng Cui7Wenhan Lu8Zhenle Pei9Mingzhen Xu10Feifei Zhang11Feifei Zhang12Xin Li13Xin Li14Yi Feng15Department of Integrative Medicine and Neurobiology, School of Basic Medical Sciences, Institutes of Brain Science, Brain Science Collaborative Innovation Center, State Key Laboratory of Medical Neurobiology, Fudan Institutes of Integrative Medicine, Fudan University, Shanghai, ChinaDepartment of Obstetrics and Gynecology, Shanghai Medical School, Fudan University, Shanghai, ChinaShanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Fudan University, Shanghai, ChinaDepartment of Integrative Medicine and Neurobiology, School of Basic Medical Sciences, Institutes of Brain Science, Brain Science Collaborative Innovation Center, State Key Laboratory of Medical Neurobiology, Fudan Institutes of Integrative Medicine, Fudan University, Shanghai, ChinaDepartment of Integrative Medicine and Neurobiology, School of Basic Medical Sciences, Institutes of Brain Science, Brain Science Collaborative Innovation Center, State Key Laboratory of Medical Neurobiology, Fudan Institutes of Integrative Medicine, Fudan University, Shanghai, ChinaDepartment of Integrative Medicine and Neurobiology, School of Basic Medical Sciences, Institutes of Brain Science, Brain Science Collaborative Innovation Center, State Key Laboratory of Medical Neurobiology, Fudan Institutes of Integrative Medicine, Fudan University, Shanghai, ChinaDepartment of Integrative Medicine and Neurobiology, School of Basic Medical Sciences, Institutes of Brain Science, Brain Science Collaborative Innovation Center, State Key Laboratory of Medical Neurobiology, Fudan Institutes of Integrative Medicine, Fudan University, Shanghai, ChinaDepartment of Obstetrics and Gynecology, Shuguang Hospital Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai, ChinaDepartment of Integrative Medicine and Neurobiology, School of Basic Medical Sciences, Institutes of Brain Science, Brain Science Collaborative Innovation Center, State Key Laboratory of Medical Neurobiology, Fudan Institutes of Integrative Medicine, Fudan University, Shanghai, ChinaDepartment of Integrative Medicine and Neurobiology, School of Basic Medical Sciences, Institutes of Brain Science, Brain Science Collaborative Innovation Center, State Key Laboratory of Medical Neurobiology, Fudan Institutes of Integrative Medicine, Fudan University, Shanghai, ChinaDepartment of Integrative Medicine and Neurobiology, School of Basic Medical Sciences, Institutes of Brain Science, Brain Science Collaborative Innovation Center, State Key Laboratory of Medical Neurobiology, Fudan Institutes of Integrative Medicine, Fudan University, Shanghai, ChinaDepartment of Obstetrics and Gynecology, Shanghai Medical School, Fudan University, Shanghai, ChinaShanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Fudan University, Shanghai, ChinaDepartment of Obstetrics and Gynecology, Shanghai Medical School, Fudan University, Shanghai, ChinaShanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Fudan University, Shanghai, ChinaDepartment of Integrative Medicine and Neurobiology, School of Basic Medical Sciences, Institutes of Brain Science, Brain Science Collaborative Innovation Center, State Key Laboratory of Medical Neurobiology, Fudan Institutes of Integrative Medicine, Fudan University, Shanghai, ChinaLow-frequency electro-acupuncture (EA) has been shown to restore ovulation in patients with polycystic ovary syndrome (PCOS), and previous animal experiments showed that EA improves ovarian blood flow and angiogenesis. We performed EA for 4 weeks in dihydrotestosterone (DHT)-induced PCOS-like rats and investigated the three-dimensional (3D) ovarian innervation to determine the role of innervation in folliculogenesis and vascularity. Ovarian tissues were made transparent following the CUBIC 3D tissue-clearing protocol and were immunostained using antibodies against platelet endothelial cell adhesion molecule-1 and tyrosine hydroxylase to visualize the ovarian vasculature and innervation, respectively. This was followed by 3D imaging using lightsheet microscopy and analysis using the Imaris software. In control rats, ovarian innervation increased with age, and the neuronal branching started from the ovarian hilum and reached the individual follicles at different follicle stages. At the individual follicle level, each follicle was mainly innervated by one neuronal fiber. Compared with control rats, ovaries from DHT-treated PCOS-like rats had more antral follicles and fewer preovulatory follicles and corpora lutea. Furthermore, PCOS ovaries showed decreased innervation of blood vessels near the hilum and the surrounding individual antral follicles. EA in PCOS-like rats led to increased numbers of preovulatory follicles and corpora lutea together with increased innervation of blood vessels near the hilum. To determine the role of ovarian innervation, we further performed unilateral sectioning of the superior ovarian nerve (SON) in PCOS + EA rats and found that the left sectioned ovary had fewer preovulatory follicles and corpora lutea compared with those in the right non-sectioned ovary. In conclusion, ovarian innervation likely played an important role in folliculogenesis, and EA might restore PCOS pathophysiology by regulating ovarian innervation, at least partially mediated through the SON.https://www.frontiersin.org/article/10.3389/fphys.2020.00474/fullelectro-acupunctureovarian innervationfollicular maturationneurovascular couplingCUBIC three-dimensional tissue clearing |
| spellingShingle | Xiaoyu Tong Yanjun Liu Yanjun Liu Xiaoqing Xu Jiemei Shi Wei Hu Tong Ma Peng Cui Wenhan Lu Zhenle Pei Mingzhen Xu Feifei Zhang Feifei Zhang Xin Li Xin Li Yi Feng Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary Syndrome Frontiers in Physiology electro-acupuncture ovarian innervation follicular maturation neurovascular coupling CUBIC three-dimensional tissue clearing |
| title | Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary Syndrome |
| title_full | Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary Syndrome |
| title_fullStr | Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary Syndrome |
| title_full_unstemmed | Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary Syndrome |
| title_short | Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary Syndrome |
| title_sort | ovarian innervation coupling with vascularity the role of electro acupuncture in follicular maturation in a rat model of polycystic ovary syndrome |
| topic | electro-acupuncture ovarian innervation follicular maturation neurovascular coupling CUBIC three-dimensional tissue clearing |
| url | https://www.frontiersin.org/article/10.3389/fphys.2020.00474/full |
| work_keys_str_mv | AT xiaoyutong ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT yanjunliu ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT yanjunliu ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT xiaoqingxu ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT jiemeishi ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT weihu ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT tongma ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT pengcui ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT wenhanlu ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT zhenlepei ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT mingzhenxu ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT feifeizhang ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT feifeizhang ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT xinli ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT xinli ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome AT yifeng ovarianinnervationcouplingwithvascularitytheroleofelectroacupunctureinfollicularmaturationinaratmodelofpolycysticovarysyndrome |