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Discovery of Antiprotozoal Compounds from Medicinal Plants

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Discovery of Antiprotozoal Compounds from Medicinal Plants Discovery of Antiprotozoal Compounds from Medicinal Plants Inauguraldissertation Zur Erlangung der Würde eines Doktors der Philosphie vorgelegt der Philosophisch-Naturwissenschaftlichen Fakultät der Universität Basel von Yoshie Adriana Hata-Uribe aus Bogota KOLUMBIEN Basel, 2014 Original document stored on the publication server of the University of Basel edoc.unibas.ch This work is licenced under the agreement „Attribution Non-Commercial No Derivatives – 3.0 Switzerland“ (CC BY-NC-ND 3.0 CH). The complete text may be reviewed here: creativecommons.org/licenses/by-nc-nd/3.0/ch/deed.en Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät auf Antrag von Prof. Dr. Matthias Hamburger Prof. Dr. Irmgard Merfort Prof. Dr. Reto Brun Basel, den 22.04.2014 Prof. Dr. Jörg Schibler Dekan 1 Namensnennung-Keine kommerzielle Nutzung-Keine Bearbeitung 3.0 Schweiz (CC BY-NC-ND 3.0 CH) Sie dürfen: Teilen — den Inhalt kopieren, verbreiten und zugänglich machen Unter den folgenden Bedingungen: Namensnennung — Sie müssen den Namen des Autors/Rechteinhabers in der von ihm festgelegten Weise nennen. Keine kommerzielle Nutzung — Sie dürfen diesen Inhalt nicht für kommerzielle Zwecke nutzen. Keine Bearbeitung erlaubt — Sie dürfen diesen Inhalt nicht bearbeiten, abwandeln oder in anderer Weise verändern. Wobei gilt: Verzichtserklärung — Jede der vorgenannten Bedingungen kann aufgehoben werden, sofern Sie die ausdrückliche Einwilligung des Rechteinhabers dazu erhalten. Public Domain (gemeinfreie oder nicht-schützbare Inhalte) — Soweit das Werk, der Inhalt oder irgendein Teil davon zur Public Domain der jeweiligen Rechtsordnung gehört, wird dieser Status von der Lizenz in keiner Weise berührt. Sonstige Rechte — Die Lizenz hat keinerlei Einfluss auf die folgenden Rechte: o Die Rechte, die jedermann wegen der Schranken des Urheberrechts oder aufgrund gesetzlicher Erlaubnisse zustehen (in einigen Ländern als grundsätzliche Doktrin des fair use bekannt); o Die Persönlichkeitsrechte des Urhebers; o Rechte anderer Personen, entweder am Lizenzgegenstand selber oder bezüglich seiner Verwendung, zum Beispiel für Werbung oder Privatsphärenschutz. Hinweis — Bei jeder Nutzung oder Verbreitung müssen Sie anderen alle Lizenzbedingungen mitteilen, die für diesen Inhalt gelten. Am einfachsten ist es, an entsprechender Stelle einen Link auf diese Seite einzubinden. Quelle: http://creativecommons.org/licenses/by-nc-nd/3.0/ch/ Datum: 12.11.2013 “…What the eyes perceive in herbs or stones or trees is not yet a remedy; the eyes see only the dross. But inside, under the dross, there the remedy lies hidden. First it must be cleaned from the dross, then it is there. This is alchemy, and this is the office of Vulcan; he is the apothecary and chemist of the medicine…” Paracelsus (1493 – 1541) TABLE OF CONTENTS LIST OF ABBREVIATIONS……………………………………………………….................................. 3 SUMMARY…………………………………………………………………………………………………. 4 ZUSAMMENFASSUNG………………………………………………………………………………….. 7 1. AIM OF THE WORK………………………………………………..…………………… 10 2. INTRODUCTION………………………………………………………………………… 13 2.1. Natural Products and Drug Discovery………………………………………………. 14 2.1.1. Historical background ……………………………………………………………. 14 2.1.2. Current Drug Discovery Process…………………………………………………. 24 2.1.3. Current State Natural Products…………………………………………………… 30 2.2. Drug Discovery for Neglected Tropical Diseases…………………………………….. 40 2.2.1. Neglected Tropical Diseases…………………………………………………. 40 2.2.2. Drug Discovery for Neglected Tropical Diseases………………..…………... 46 3. RESULTS AND DISCUSSION…………………………………………………………… 60 3.1 In Vitro Screening of Traditional South African Malaria Remedies Against Trypanosoma brucei rhodesiense, Trypanosoma cruzi, Leishmania donovani, and Plasmodium falciparum………………………………………………………………………. 61 3.2 Antiprotozoal Screening of 60 South African Plants, and the Identification of the Antitrypanosomal Germacranolides Schkuhrin I and II…………………………… 80 3.3 Antiprotozoal Isoflavan Quinones from Abrus precatorius ssp. africanus…………. 117 3.4 Antitrypanosomal Activity of Isoflavan Quinones from Abrus precatorius ………. 150 3.5 Antiprotozoal Compounds from Drypetes gerrardii ………………….……………. 192 3.6 Antiplasmodial and Antitrypanosomal Activity of Pyrethrins and Pyrethroids ... 247 3.7 Antitrypanosomal Sesquiterpene Lactones from Saussurea costus…………………. 263 4. CONCLUSION AND OUTLOOK …………………………………………………………. 271 ACKNOWLEDGMENTS…………………………………………………………………………….. 28 2 CURRICULUM VITAE………………………………………………………..……………………... 283 2 LIST OF ABBREVIATIONS WHO World Health Organization DDT Dichlorodiphenyltrichloroethane NMR Nuclear Magnetic Resonance DHA Dihydroartemisinin TCTP Malarial translationally controlled tumor protein ACT Artemisinin-based combinations treatment DDD Drug discovery and development PK Pharmacokinetics SAR Structure-activity relationship ADME Absorption, distribution, metabolism, and excretion NPs Natural products NCES New chemical entities HTS High throughput screening NMR Nuclear magnetic resonance HPLC High performance liquid chromatography RP Reverse Phase UV Ultraviolet MS Mass spectrometry ESI Electrospray ionization APCI Atmospheric pressure chemical ionization API Atmospheric pressure ionization TOF Time-of-flight GABA Gamma-aminobutyric acid PDA Photodiode array detector ELSD Evaporative light scattering detector SPE Solid phase extraction COSY Correlated spectroscopy NOESY Nuclear overhouser enhancement spectroscopy HETCOR Heteronuclear correlation ROESY Rotating frame overhauser enhancement spectroscopy TOCSY Total correlation spectroscopy HSQC Heteronuclear single quantum coherence HMBC Heteronuclear multiple bond correlation AC Absolute configuration ECD Electronic circular dichroism PEGs Pulsed-field gradients NTD Neglected tropical diseases HAT Human African Trypanosomiasis DALYs Disability-adjusted life years BBB blood-brain barrier DNDi Drugs for neglected diseases initiative TDR The special program for research and training in tropical diseases (WHO) CNS Central nervous system PSA Polar surface area IC50 Inhibitory Concentration 50 SI Selectivity index 3 SUMMARY Tropical parasitic diseases such as malaria, human African trypanosomiasis, chagas disease, and leishmaniasis affect hundreds of millions of people worldwide and have devastating consequences. Current drugs available to treat these diseases have serious drawbacks. New drugs are urgently needed. Natural products (NPs) play a dominant role in drug discovery for the treatment of human diseases. Particularly, quinine and artemisinin have their origin in nature and have inspired successful drugs for malaria treatment. In a medium throughput screening, a total of 507 extracts from South African plants were assayed for their antiprotozoal activity against Plasmodium falciparum, Trypanosoma brucei rhodesiense, Trypanosoma cruzi and Leishmania donovani. Extracts from Abrus precatorius L. ssp. africanus Verdc. (Fabaceae) and Drypetes gerrardii Hutch. var. gerrardii (Putranjivaceae) inhibited at least one of the parasites at a test concentration considered relevant. With the aim of identifying the compounds responsible for these activities, a HPLC-based activity profiling approach followed by dereplication was applied. Targeted isolation of promising compounds was achieved by a combination of chromatography techniques. Structure elucidation was achieved by HR-ESI-MS and NMR (1H, 13C, COSY, HMBC, HSQC, and NOESY spectroscopy). Absolute configuration was determined by comparison of electronic circular dichroism (ECD) spectra with calculated ECD data. HPLC-based activity profiling of A. precatorius allowed the identification of abruquinones, a series of isoflavan quinones, as responsible for the trypanocidal activity of the crude extract. A total of ten abruquinones were isolated. Among these were five new compounds, and one compound was reported for the first time as natural product. Abruquinone B, I, A, D, K, and L showed remarkable inhibition (0.16 ± 0.060, 0.28 ± 0.051, 0.02 ± 0.003, 0.01 ± 0.001, 0.11 ± 0.053, and 0.02 ± 0.053, respectively) and notable selectivity, expressed as selectivity indices (SIs) which were calculated from cytotoxicity data in L-6 cells (51, 74, 1379, 668, 508, and 374, respectively). These results warrant in vivo assessment of abruquinones. Abruquinones are promising hits due to their strong and selective in vitro inhibition of T. b. rhodesiense, their good compliance with Lipinski’s “rule-of-5” and other molecular properties, as well as their predicted low/moderate toxic potential. Therefore, further studies are necessary to guarantee a botanical or chemical source, and to assess in vivo efficacy. Two different extracts of D. gerrardii showed antiprotozoal activity, and the active constituents were tracked and isolated by HPLC-based activity profiling. The CH2Cl2/MeOH (1:1) stems extract inhibited L. donovani and P. falciparum. The major compound, a new phenanthrenone, showed good in vitro activity 4 (IC50 of 0.9 ± 0.3 µM) and selectivity (SI of 68) against P. falciparum. Based on these promising results, in-vivo studies were conducted. However, the compound was not able to reduce parasitemia in the P. berghei mouse model. A phenanthrenone heterodimer was also isolated and showed in vitro antiplasmodial activity (IC50 of 2.04 ± 0.15 µM and SI of 31). Furthermore, the CH2Cl2/MeOH (1:1) leaves extract displayed trypanocidal properties, and the known saponin putranoside A was isolated and tested against T. b. rhodesiense, (IC50 of 18.0 ± 3.8 µM and a SI of 4). The phenanthrenone was the most active and
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