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Copyright Undertaking Copyright Undertaking This thesis is protected by copyright, with all rights reserved. By reading and using the thesis, the reader understands and agrees to the following terms: 1. The reader will abide by the rules and legal ordinances governing copyright regarding the use of the thesis. 2. The reader will use the thesis for the purpose of research or private study only and not for distribution or further reproduction or any other purpose. 3. The reader agrees to indemnify and hold the University harmless from and against any loss, damage, cost, liability or expenses arising from copyright infringement or unauthorized usage. IMPORTANT If you have reasons to believe that any materials in this thesis are deemed not suitable to be distributed in this form, or a copyright owner having difficulty with the material being included in our database, please contact [email protected] providing details. 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Pao Yue-kong Library, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong http://www.lib.polyu.edu.hk CHARACTERIZATION OF THE TISSUE-SELECTIVITY OF TRADITIONAL CHINESE MEDICINE (TCM)-DERIVED PHYTOESTROGEN AND THE POSSIBLE MECHANISMS INVOLVED ZHOU LIPING Ph.D The Hong Kong Polytechnic University 2017 The Hong Kong Polytechnic University Department of Applied Biology and Chemical Technology Characterization of the Tissue-selectivity of Traditional Chinese Medicine (TCM)-derived Phytoestrogen and the Possible Mechanisms Involved ZHOU Liping A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy September 2016 I Certificate Originality I hereby declare that this thesis is my own work and that, to the best of my knowledge and belief, it reproduces no material previously published or written, nor material that has been accepted for the award of any other degree or diploma, except where due acknowledgement has been made in the text. (Signed) ZHOU Liping (Name of student) II Abstract Icariin is the most abundant flavonoid in Herba Epemedii (HEP), a commonly used Chinese herb for treatment of bone disease, that has been reported to exert estrogenic effects. Danggui Buxue Tang (DBT), consisting of Radix Astragali and Radix Angelicae Sinensis, is the most popular traditional Chinese Medicine (TCM) decoction prescribed for management of menopausal symptoms in China and its chemical composition has been well characterized. Recent studies found that DBT may contain phytoestrogens and majority of the activities of DBT are mediated by these phytoestrogens. This study aimed to investigate the estrogenic effects of icariin and DBT in different estrogen-sensitive tissues and the possible mechanisms involved. In the first part of my study, the tissue-selectivity of icariin was evaluated by using mature ovariectomized (OVX) Sprague Dawley rats and four estrogen-responsive cell lines (human breast cancer MCF-7 cell, human endometrial Ishikawa cell, human neuroblastoma SH-SY5Y cell and human osteosarcoma MG-63 cell). Upon treatment for 12 weeks, icariin dose-dependently increased the bone mineral density (BMD) and improved the trabecular bone properties at distal femur, proximal tibia and lumbar spine in OVX rats. Moreover, icariin reversed the changes in mRNA expression of tyrosine hydroxylase (TH) and dopamine transporter (DAT) in striatum of OVX rats III but did not induce estrogenic responses in uterus and breast. In addition, icariin significantly stimulated cell proliferation or differentiation but failed to induce the expression of estrogen-responsive genes and estrogen response element-dependent luciferase activities in MCF-7, Ishikawa cell, SH-SY5Y cell and MG-63 cell. These results indicate that icariin did not induce estrogen-dependent transcriptional events in these cell lines. In the second part of my study, the tissue-selectivity of DBT was investigated using both mature OVX rats and estrogen receptor (ER)-positive cell lines. The results showed that DBT reversed the decrease in estradiol level as well as the accompanying increase in follicle-stimulating hormone (FSH) and luteinizing hormone (LH) level in rats induced by ovariectomy. In addition, DBT increased BMD and improved micro-architecture of both long bone and vertebra in OVX rats. DBT also up-regulated mRNA expression of TH and suppressed mRNA expression of DAT in striatum of OVX rats without inducing estrogenic responses in uterus and breast tissue of OVX rats. Our in vitro studies showed that DBT directly stimulated cell proliferation and differentiation as well as ERE luciferase activities in MCF-7, Ishikawa cell, SH-SY5Y cell and MG-63 cell, suggesting the direct estrogenic effects of DBT. Co-treatment of DBT-treated MG-63 cells with ICI182,780 (ER antagonist, 10-6M), U0126 (mitogen-activated protein kinase MAPK inhibitor, 10-6M) and IV LY294002 (phosphoinositide 3-kinase PI3K inhibitor, 10-6M) completely or partially blocked the stimulating effects of DBT on cell proliferation and cell differentiation. These results indicate that ER, MAPK and PI3K pathways might be involved in mediating the actions of DBT in bone cells. It is also of concern to determine if the use of herbal medicine will be safe for postmenopausal women who are simultaneously prescribed with selective estrogen receptor modulators (SERMs) such as tamoxifen and raloxifene for treatment of breast cancer and osteoporosis as many of their activities are mediated by the same receptors. In the third part of my study, the potential interactions between DBT and SERMs (tamoxifen and raloxifene) were thereby investigated. Upon co-treatment for three months, DBT did not alter the estrogenic effects of tamoxifen and raloxifene in the uterus, breast tissues, brain and bone of OVX rats. In addition, DBT at 0.1mg/ml did not interact with the estrogenic effects of SERMs in MCF-7 cells. However, DBT at 0.5mg/ml antagonized the effects of tamoxifen on cell proliferation in MCF-7 cell and enhanced the stimulating effects of tamoxifen and raloxifene on cell proliferation of SH-SY5Y cell as well as the alkaline phosphatase (ALP) activity in Ishikawa and MG-63 cells. These results suggest that DBT does not interact with western drugs (tamoxifen and raloxifene) in estrogen-sensitive tissues in vivo while the in vitro interactive effects appear to be dose-dependent and tissue-specific. This discrepancy V between in vivo and in vitro studies might be due to the fact that DBT applied in the cells was without biological activation and such concentrations are too high to be achieved in vivo. In conclusion, both icariin and DBT selectively exerted protective effects in bone and brain without causing side effects in uterus and breast in vivo. Our study provide evidence to support our hypothesis that phytoestrogens derived from TCM selectively exert estrogenic effects in estrogen-sensitive tissues and might be useful for the management of postmenopausal syndromes. VI List of Publications 1. LP Zhou#, KW Tsim, MS Wong. Danggui Buxue Tang decoction (DBT) protects rats against ovariectomy-induced osteoporosis by suppressing bone turnover. The 11th International Postgraduate symposium on Chinese Medicine. 2015. Hong Kong 2. M.X. Ho#, L.P Zhou, M.S. Wong. Icariin Exerts Anabolic Effects on Osteoblasts via Rapid Estrogen Receptor α Signaling Pathways. Annual Meeting of American Society of Bone and Mineral Research. 2015. Seattle, USA. 3. Zhou LP#, Poon CCW, Tsim KWK, MS Wong. A Phytoestrogen-rich DBT formula modulated hypothalamic-pituitary-ovary axis in mature ovariectomized rats. ENDO 2016, Annual Meeting of the Endocrine Society. 2016. Boston, USA. 4. Zhou LP#, Dong XL, Cao SS, Tsim KWK, MS Wong. Danggui Buxue Tang Decoction (DBT), a phytoestrogen-rich formula, increased bone mineral density and improved bone properties in mature ovariectomized rats. ENDO 2016, Annual Meeting of the Endocrine Society. 2016. Boston, USA. 5. Zhang Y#, Zhou LP, Ho MX, Wong KC, MS Wong. 8-prenylgenistein, a derivative of genistein, exerted osteoprotective effects without uterotrophic activity. ENDO 2016, Annual Meeting of the Endocrine Society. 2016. Boston, USA. 6. Dong F, Dong X, Zhou L, Xiao H, Ho PY, Wong MS, Wang Y. 2016 Doxorubicin-loaded biodegradable self-assembly zein nanoparticle and its anti-cancer effect: Preparation, in vitro evaluation, and cellular uptake. Colloids Surf B Biointerfaces.140:324-31. 7. Zhang Yan, Zhou Li-Ping, Ho Mingxian, Li Xiao-Pi, Zhao Yong-Jian, Mok Kam-Wah, Qiu Zuo-Cheng, Shi Qi, Wang Yong-Jun, Wong Man-Sau. VII 8-Prenylgenistein, a prenylated genistein derivative, exerted tissue selective osteoprotective effects in ovariectomized mice. (Submitted) 8. Protective effects of Danggui Buxue Tang (DBT), a phytoestrogen-containing Traditional Chinese Medicine, against osteoporosis in ovariectomy rats and possible involvement of ER, MAPK and PI3K pathway. (in preparation) 9. A phytoestrogen rich DBT formula modulates circulating levels of reproductive hormones in mature ovariectomized rats and exerts direct estrogenic actions in estrogen sensitive cells. (in preparation) 10. Ginsenoside Rg1 improves the spatial learning and memory ability of Aß25-35-induced AD mice possibly via ER and IGF-IR pathways. (in preparation) VIII Acknowledgement Three years ago, I went to The Hong Kong Polytechnic University to pursue my study as a PhD student. It is one of the most important and brave decisions I have made. Yes, it is full of challenges and tortures while it is also a period of harvest. Thanks to all the help from my surroundings, I managed to finish my study. At the end of my PhD study, I would like to take this opportunity to express my gratitude to those who helped during my three years’ study. My deepest gratitude goes first and foremost to my supervisor, Professor Wong Man Sau. I appreciate her constant encouragement and invaluable advices throughout my PhD study. Without her professional guidance and generous support, I would never have been able to finish my study. Her enthusiastic attitude towards science and her high work efficiency will be the goals for all my life.
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