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      Ovarian Innervation Coupling With Vascularity: The Role of Electro-Acupuncture in Follicular Maturation in a Rat Model of Polycystic Ovary Syndrome

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          Abstract

          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.

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          A new rat model exhibiting both ovarian and metabolic characteristics of polycystic ovary syndrome.

          Malin Lönn, Elisabet Stener-Victorin, Agneta Holmäng … (2007)
          Polycystic ovary syndrome (PCOS) is a complex endocrine and metabolic disorder associated with ovulatory dysfunction, hyperandrogenism, abdominal obesity, and insulin resistance. However, its etiology is unclear, and its management is often unsatisfactory or requires a diversified approach. Here, we describe a new rat PCOS model, the first to exhibit both ovarian and metabolic characteristics of the syndrome. Female rats received the nonaromatizable androgen dihydrotestosterone (DHT) or the aromatase inhibitor letrozole by continuous administration, beginning before puberty, to activate androgen receptors. Adult DHT rats had irregular cycles, polycystic ovaries characterized by cysts formed from atretic follicles, and a diminished granulosa layer. They also displayed metabolic features, including increased body weight, increased body fat, and enlarged mesenteric adipocytes, as well as elevated leptin levels and insulin resistance. All letrozole rats were anovulatory and developed polycystic ovaries with structural changes strikingly similar to those in human PCOS. Our findings suggest that the formation of a "hyperplastic" theca interna reflects the inclusion of luteinized granulosa cells in the cyst wall rather than true hyperplasia. We conclude that the letrozole model is suitable for studies of the ovarian features of human PCOS, while the DHT model is suitable for studies of both ovarian and metabolic features of the syndrome.
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            Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin.

            Yoh-suke Mukouyama, Donghun Shin, Stefan Britsch … (2002)
            Nerves and blood vessels are branched structures, but whether their branching patterns are established independently or coordinately is not clear. Here we show that arteries, but not veins, are specifically aligned with peripheral nerves in embryonic mouse limb skin. Mutations that eliminate peripheral sensory nerves or Schwann cells prevent proper arteriogenesis, while those that disorganize the nerves maintain the alignment of arteries with misrouted axons. In vitro, sensory neurons or Schwann cells can induce arterial marker expression in isolated embryonic endothelial cells, and VEGF(164/120) is necessary and sufficient to mediate this induction. These data suggest that peripheral nerves provide a template that determines the organotypic pattern of blood vessel branching and arterial differentiation in the skin, via local secretion of VEGF.
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              Blood vessels and nerves: common signals, pathways and diseases.

              Peter Carmeliet (2003)
              Both blood vessels and nerves are vital channels to and from tissues. Recent genetic insights show that they have much more in common than was originally anticipated. They use similar signals and principles to differentiate, grow and navigate towards their targets. Moreover, the vascular and nervous systems cross-talk and, when dysregulated, this contributes to medically important diseases. The realization that both systems use common genetic pathways should not only form links between vascular biology and neuroscience, but also promises to accelerate the discovery of new mechanistic insights and therapeutic opportunities.
              Article 0 comments Cited 112 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Journal
                Journal ID (nlm-ta): Front Physiol
                Journal ID (iso-abbrev): Front Physiol
                Journal ID (publisher-id): Front. Physiol.
                Title: Frontiers in Physiology
                Publisher: Frontiers Media S.A.
                ISSN (Electronic): 1664-042X
                Publication date (Electronic): 29 May 2020
                Publication date Collection: 2020
                Volume: 11
                Electronic Location Identifier: 474
                Affiliations
                [1] 1Department 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, China
                [2] 2Department of Obstetrics and Gynecology, Shanghai Medical School, Fudan University , Shanghai, China
                [3] 3Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Fudan University , Shanghai, China
                [4] 4Department of Obstetrics and Gynecology, Shuguang Hospital Affiliated to Shanghai University of Traditional Chinese Medicine , Shanghai, China
                Author notes

                Edited by: Artur Mayerhofer, Ludwig Maximilian University of Munich, Germany

                Reviewed by: Hernan E. Lara, University of Chile, Chile; Cecily Vauna Bishop, Oregon Health & Science University, United States

                *Correspondence: Yi Feng, fengyi17@ 123456fudan.edu.cn

                This article was submitted to Reproduction, a section of the journal Frontiers in Physiology

                Article
                DOI: 10.3389/fphys.2020.00474
                PMC ID: 7273926
                PubMed ID: 32547407
                SO-VID: 090892e9-d7fd-4ef8-ac14-4aaf2b3cbef7
                Copyright © Copyright © 2020 Tong, Liu, Xu, Shi, Hu, Ma, Cui, Lu, Pei, Xu, Zhang, Li and Feng.
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                Date received : 16 January 2020
                Date accepted : 17 April 2020
                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 54, Pages: 14, Words: 0
                Categories
                Subject: Physiology
                Subject: Original Research

                ScienceOpen disciplines: Anatomy & Physiology
                Keywords: electro-acupuncture,ovarian innervation,follicular maturation,neurovascular coupling,cubic three-dimensional tissue clearing
                Data availability:
                ScienceOpen disciplines: Anatomy & Physiology
                Keywords: electro-acupuncture, ovarian innervation, follicular maturation, neurovascular coupling, cubic three-dimensional tissue clearing

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