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Dissertation Sadrine Tchoukou BIOACTIVITY OF PLANTS SECONDARY METABOLITES Estrogenic, cytotoxic and anabolic effects on estrogen target organs of an extract of Erythrina excelsa and Ecdysterone A thesis presented to: The Institute of Cardiovascular Research and Sports Medicine Department of Molecular and Cellular Sports Medicine German Sport University Cologne In partial fulfillment of the requirements for the degree PhD in Natural Sciences by: Sadrine Tchoukouegno Ngueu From Bamenyam, Cameroon Members of the jury: - Prof. Dr. Patrick Diel (First referee) - Prof. Dr. Günter Vollmer (Second referee) - Prof. Dr. Wilhelm Schänzer - Dr. Frank Hülsemann Date of defence: 05.09.2013 Gedruckt mit Unterstützung des Deutschen Akademischen Austauschdienstes (DAAD) Versicherung gem. § 7 Abs. 2 Nr. 4 Hierdurch versichere ich: Ich habe diese Arbeit selbständig und nur unter Benutzung der angegebenen Quellen und technischen Hilfen angefertigt; sie hat noch keiner anderen Stelle zur Prüfung vorgelegen. Wörtlich übernommene Textstellen, auch Einzelsätze oder Teile davon, sind als Zitate kenntlich gemacht worden. …………………………………… Sadrine Tchoukouegno Ngueu Erklärung gem. § 7 Abs. 2 Nr. 5 Hierdurch erkläre ich, dass ich die Leitlinien guter wissenschaftlicher Praxis der DeutschenSporthochschule Köln in der aktuellen Fassung eingehalten habe. …………………………………… Sadrine Tchoukouegno Ngueu I dedicate this work to: God almighty and to Jesus Christ my Lord and Savior in whom I trust. My lovely husband Olivier Ndiapi for his endless support through happy and difficult times. These 4 years away from each other were challenging but your support was always an encouragement to me. Acknowledgements Acknowledgements I would not have completed this work without the help and support of several persons. Foremost, special thanks go to my supervisor Prof.Dr. Patrick Diel who did not only give me his support throughout the completion of my thesis work, but also supported me with the DAAD scholarship application procedure. I extend my thanks to Prof. Guenter Vollmer for his helpful pieces of advice regarding my work and who, during these years, wrote letters of recommandation that helped extend my scholarship. I am also grateful to Prof. Dr. Maria Paar who guided me through my first chromatographic separation. I thank the German academic service exchange (DAAD) for granting me the scholarship. I had the opportunity to work in a team composed of persons from different horizons and experiences which was very helpful not only for my academic advancement, but also contributed to build certain traits of my character. I think of my colleagues Jonas Hengevoß, Xiao Juan Hu, Sephanie Mosler, Felix Kluxen, Nora Zoth, Almut Molzberger, Carmen Weigt, Tina Blei, Dennis Mueller, and Martina Velders. I specially thank Felix Kluxen not only for the helpful tips in the lab, but also for his availability and patience towards me during my first days in Germany. My gratitude also goes to our technical assistant crew composed of Anika Voß, Ute Laudenbach-Leschowski, Ghilav Mojgan, and Bianca Collins who were always available to assist me in the pratical aspects of laboratory work. Special thanks go to Ute Laudenbach for her support in all aspects of animal experiments. I would also like to acknowledge the support of my former Master degree supervisor, Prof. Njamen Dieudonne, during my scholarship application process and during my PhD thesis work. M.Sc. Sadrine Tchoukouegno Ngueu vi Acknowledgements Special thanks to Maria Halabalaki (School of pharmacy, University of Athens) for her support in my work and for granting me the opportunity to carry out an internship in the pharmacognosy laboratory of the University of Athens. I will not forget Job Tchoumtchoua who has been more than a friend to me. Thank you for the long discussions over the phone and for introducing and supervising me in your lab in Athens. I thank Raoul Kempkes of the Biochemistry department for his technical support in the use of the flow cytometer. Finally, I thank my family for their continuous support in the course of my education. I think also of my late parents and my late elder brother who took me as he his own child and guided me throughout my studies. M.Sc. Sadrine Tchoukouegno Ngueu vii Zusammenfassung Zusammenfassung Heilpflanzen dienen als primäre Gesundheitsversorgung in den meisten asiatischen und afrikanischen Ländern. In westlich geprägten Ländern in denen hauptsächlich auf naturwissenschaftlichen Grundsätzen basierende Medizin praktiziert wird, werden Stoffe aus pflanzlicher Herkunft entweder direkt als Kräuterformulierungen oder als Ergänzung zu bestehenden Therapien verwendet. Daneben können Pflanzen mit aktiven Wirkstoffen auch Teil der Ernährung sein. Es besteht die allgemeine Überzeugung, dass pflanzliche Heilmittel aufgrund ihres natürlichen Ursprungs sicher sind. Daher werden sie oft im Rahmen selbsttherapeutischer Maßnahmen verwendet und sind in Deutschland auch nicht rezeptpflichtig. Diese Arbeit beschäftigt sich mit der Bioaktivität, Wirkungen aber auch potentiellen Nebenwirkungen derartiger pflanzlicher Heilmittel. Hierbei stehen Extrakte aus Erythrina excelsa sowie die Substanz Ecdysterone im Mittelpunkt des Interesses. Erythrina excelsa ist eine Pflanze die in der kamerunischen traditionellen Medizin zur Behandlung von Wechseljahrsbeschwerden und gynäkologische Tumoren Anwendung findet. Ob Erythrina excelsa allerdings wirklich pharmakologisch aktive Substanzen enthält, die derartige Wirkungen erzielen können, wurde bisher noch nicht untersucht. Ecdysterone (Ecdy) ist ein Inhaltsstoff von verschiedenen Pflanzen, die in der chinesischen, ayurvedischen und russischen traditionellen Medizin zur Behandlung unterschiedlichster Beschwerden verwendet werden. Für Ecdy konnte eine anabole Wirkung in vitro und in vivo gezeigt werden. Obwohl die zugrunde liegenden Mechanismen noch nicht aufgeklärt sind, wird es intensiv als Nahrungsergänzungsmittel zur Steigerung des Muskelaufbaus beworben und auch von Bodybuildern verwendet. Ein Missbrauch zum Doping in anderen Sportarten wird befürchtet. Die Ziele dieser Arbeit waren zum einen die Bioaktivität von Extrakten von Erythrina excelsa, die in Bezug zur traditionellen Anwendung in der Naturmedizin stehen, sowie die biologisch aktiven Inhaltsstoffe in den Extrakten näher zu charakterisieren. Zum anderen sollten die Mechanismen der anabolen Wirkung von Ecdysterone untersucht werden. M.Sc. Sadrine Tchoukouegno Ngueu viii Zusammenfassung Mittels Yeast Estrogen Screen (YES), uterotrophen Assay und des MTT-Assay konnte gezeigt werden, dass ein Äthanolextrakt von E. excelsa östrogene/anti- östrogene und zytotoxische Effekte aufweist. Eine dreitägige subkutane Verabreichung des Extraktes in einer Dosis von 50 mg/kg KG/Tag an ovariektomierten Wistar Ratten führte zu signifikanten östrogenen Wirkungen auf morphometrische Parameter der Gebärmutter (Feuchtgewicht und epithelialen Höhen) und auf die Expression von Östrogen-abhängigen Genen in der Gebärmutter (C3 und Clusterin) und in der Leber (CaBP9K und IGFBP-1). Bei einer Dosis von 100 mg/kg KG/Tag zeigte der Extrakt unerwartet auf die beschriebenen biologischen Endpunkte eine anti-östrogene Wirkung. Eine fünftägige Behandlung von Estrogenrezeptor (ER) -positiven MCF-7 Brustkrebszellen mit dem Extrakt führte zu einem biphasischen Profil: Bei niedrigen Konzentrationen kam es zu einem leichten Anstieg der Zellviabilität, bei höheren Konzentrationen dagegen zu einer Induktion von Zelltod. Dagegen wurde bei der Behandlung von ER negativen HT-29 Zellen Zytotoxizität bei allen getesteten Konzentrationen beobachtet. Um die Wirkstoffe des Extraktes näher zu charakterisieren, wurde eine Vakuum Flüssigchromatographie Fraktionierung durchgeführt. Biologisch aktive Fraktionen wurden mittels des YES Assays identifiziert und die biologische Wirkung dieser Fraktion auf Proliferation und Apotose von MCF-7-Brustkrebs-Zellen mittels Durchflusszytometrie, Genexpressionsanalyse und Immunhistochemie untersucht. Die Dichloromethan- Methanol (50:50 v/v) Fraktion (F4), die in Bezug auf östrogene und zytotoxische Wirkung die aktivste Fraktion war, zeigte eine nicht-monotone Konzentrations- Wirkungs-Kurve auf den Zellzyklus, die Proliferation und Apoptose von MCF-7 Brustkrebszellen. Bei niedrigen Konzentrationen und in Abwesenheit von E2, förderte F4 Östrogenrezenptor- abhängig die Proliferation von MCF-7 Zellen (Hochregulation von Cyclin D1 und Herunterregulation des Bax/Bcl-2-mRNA Verhältnisses). Interessanterweise wirkte F4 in den gleichen Konzentrationen bei Anwesenheit von E2, als Antagonist und verhinderte ein E2-induziertes Zellwachstum. Bei höheren Konzentrationen modulierte F4 den Zellzyklus zugunsten einer gesteigerten Apoptose (Erhöhung des Caspase-gespaltenen Zytokeratin 18, Hochregulation des Bax/Bcl-2 Verhältnisses und Herunterregulation von Cyclin-D1-mRNA). In Zusammenarbeit mit der Arbeitsgruppe von Dr. Halabalaki von der Abteilung für Pharmakognosie und Naturstoffchemie der Universität von Athen wurde eine weitere M.Sc. Sadrine Tchoukouegno Ngueu ix Zusammenfassung Charakterisierung des Extraktes mittels LC-HRMS und LC-HRMS/MS Analyse durchgeführt um die im Extrakt enthaltenen Isoflavonoide zu identifizieren. Diese Analyse zeigte, dass Pyran- und Prenyl-Isoflavonoidderivate die charakteristischen chemischen Stoffe des Extrakts sind was auch die beobachtete Kombination der biologischen Eigenschaften des Extraktes erklären könnte. Im zweiten Teil dieser Arbeit wurden die anabolen Wirkmechanismen von Ecdysterone, Erythrina excelsa Extrakt und Genistein
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