INAUGURAL DISSERTATION

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3 INAUGURAL DISSERTATION submitted to the Combined Faculties for the Natural Sciences and for Mathematics of the Ruperto-Carola University of Heidelberg, Germany for the degree of Doctor of Natural Sciences Presented by Florian Herrmann Apotheker (Staatsexamen) born in Karlsruhe, Germany Oral examination:

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5 TCM Plants: DNA Barcoding, Cytotoxic and Trypanocidal Properties of Drugs and Their Active Constituents This work was carried out in the Department of Biology, Institute for Pharmacy and Molecular Biotechnology (IPMB), Im Neuenheimer Feld 364, 6912 Heidelberg at the Ruprecht-Karls-University of Heidelberg between February 26 and August 211. Head of division: Prof. Dr. Michael Wink Supervisor: Prof. Dr. Michael Wink Department of Biology, IPMB Ruprecht-Karls-University Heidelberg 1 st Referee: Prof. Dr. Michael Wink Department of Biology, IPMB Ruprecht-Karls-Universiität Heidelberg 2 nd Referee: Prof. Dr. Thomas Efferth Institute for Pharmacy and Biochemistry Johannes Gutenberg-Universität Mainz

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7 Publications F. Herrmann, R. Hamoud, F. Sporer, A. Tahrani, M. Wink: Carlina oxide a natural polyacetylene from Carlina acaulis (Asteraceae) with potent antitrypanosomal and antimicrobial properties! In press, Planta Medica; published online June 15, 211 DOI F. Herrmann, M. Wink: Synergistic interactions of saponins and monoterpenes in HeLa cells, Cos7 cells and in erythrocytes In press, Phytomedicine F. Herrmann, F. Sporer, A. Tahrani, M. Wink: Antitrypanosomal properties of Panax ginseng CA Meyer new possibilities for a remarkable traditional drug! Submitted, Phytotherapy Research F. Herrmann, M. Wink: Cytotoxicity of structurally diverse ginsenosides from Panax ginseng in HeLa cells is linked to membrane disturbances Submitted, Journal of Pharmacy and Pharmacology F Herrmann, M. R. Romero, A.G. Blazquez, D. Kaufmann, M. L. Ashour, S. Kahl, J.J.G. Marin, T. Efferth, M. Wink: Cytotoxicity, antiviral and antitrypanosomal screening of 82 plants from Chinese and European phytomedicine Submitted, Diversity F. Herrmann, M. Wink: Use of rbcl sequences for DNA barcoding and authentication of plant drugs used in Traditional Chinese Medicine Submitted, Zeitschrift für Naturforschung N.Z. Mamadalieva, F. Herrmann, M.Z. El-Readi, A. Tahrani, R. Hamoud, D. Egamberdieva, Sh.S. Azimova, M. Wink: Flavonoids in Scutellaria immaculata and S. ramosissima and their biological activities In press, Journal of Pharmacy and Pharmacology Equal distributed authors 3

8 T. Efferth, F. Herrmann, A. Tahrani, M. Wink: Cytotoxic activity towards cancer cells of arteanuine B, artemisitene, scopoletin and 1.8-cineole derived from Artemisia annua L. in comparison to artemisinin In press, Phytomedicine 211 DOI 1.116/j.phymed D. Hamdan, M. Z. El-Readi, A. Tahrani, F. Herrmann, D. Kaufmann, N. Farrag, A. El-Shazly, M. Wink: Chemical composition and biological activity of Citrus jambhiri Lush. Food Chemistry 211, 127: D. Hamdan, M. Z. El-Readi, A. Tahrani, F. Herrmann, D. Kaufmann, N. Farrag, A. El-Shazly, M. Wink: Secondary metabolites of ponderosa lemon (Citrus pyriformis Hassk) and their antioxidant, anti-inflammatory and cytotoxic activities In press, Zeitschrift für Naturforschung 211 S. Mulyaningsih, M. Youns, M. Z. El-Readi, M. L. Ashour, E. Nibret, F. Sporer, F. Herrmann, J. Reichling, M. Wink: Biological activity of the essential oil of Kadsura longipedunculata (Schisandraceae) and its major components Journal of Pharmacy and Pharmacology 21, 62:

9 Table of Contents Summary Summary (German) General Introduction Traditional Chinese Medicine Traditional Chinese Medicine Chinese herbal medicine Secondary metabolites Ecological function Biosynthesis Storage Classes of secondary metabolites Mode of action African Trypanosomiasis Epidemiology Classification Biology Control Targets References Use of rbcl sequences for DNA barcoding and authentication of plant drugs used in Traditional Chinese Medicine Abstract Introduction Material and Methods Results Discussion References Cytotoxicity, antitrypanosomal and antiviral screening of 82 plants from Chinese and European phytomedicine Abstract Introduction Material and Methods Results and Discussion References

10 4. Cytotoxicity of 12 structurally diverse ginsenosides from Panax ginseng in HeLa cells is linked to membrane disturbance Abstract Introduction Material and Methods Results Discussion References Antitrypanosomal properties of Panax ginseng CA Meyer new possibilities for a remarkable traditional drug! Abstract Introduction Material and Methods Results Discussion References Carlina oxide a natural polyacetylene from Carlina acaulis (Asteraceae) with potent antitrypanosomal and antimicrobial properties! Abstract Introduction Material and Methods Results Discussion References Synergistic Interactions of Saponins and Monoterpenes in HeLa cells, Cos7 Cells and in Erythrocytes Abstract Introduction Material and Methods Results Discussion References General conclusion and outlook Acknowledgements Appendix

11 Summary Our extensive screening of 82 herbal drugs used in traditional Chinese and European Phytomedicine revealed the great potential still hidden in this field of research. The correct authentication of plants used in research on traditional medicinal systems such as TCM is crucial before any serious research can be started. DNA barcoding offers a reliable, fast possibility to overcome this obstacle. Only one adulteration could be detected where Arctium lappa was wrongly labelled Fraxinus rhynchophylla. After screening 246 extracts of herbal drugs against a variety of targets such as trypanosomes, viruses and cancer cells we were able to select several highly promising plants for further research. We decided to focus our research on Panax ginseng, Araliaceae, a well known herbal medicine of international fame and a long history of traditional use. Our experiments revealed that ginsenosides, a highly variable group of saponins, disturb the biomembrane of cells, while the exact position of the sugar moieties and the resulting ability to be incorporated into the lipid bilayer of the cell membrane explain the great differences in their cytotoxicity. The membrane activity of the ginsenosides however was not responsible for the trypanocidal effect of ginseng revealed in our screening. Panaxynol, the major polyacetylene of ginseng was with an IC 5 concentration of.1 µg/ml and a selectivity index of 858 three times as selective against Trypanosoma brucei brucei as established antitrypanosomal drugs like suramin. We were able to discover with Carlina oxide isolated from Carlina acaulis, Asteraceae, a second polyacetylene highly selective in its cytotoxicity against T. b. brucei with an IC 5 of 1. µg/ ml and a selectivity index of 446. We suggest that the inhibition of the trypanothione reductase, essential for the resistance of the parasite against oxidative stress and unique to trypanosomes, is the primary principle of this selectivity. Our previous results obtained from the activity of ginsenosides had shown us the efficacy, but also the structure dependency of the membrane effects of saponins. With monoterpenes we have a second group of structurally completely different natural products that also target the biomembrane. The question arose if their omnipresence in phytomedicine and their application in combination would be more than just a coincidence. We combined several saponins with three monoterpenes and explored their effect on biomembranes modelled by erythrocytes and living cells. Astonishingly, the combination lowered the dosis necessary for haemolysis up to the factor, which was also confirmed in living cells. This revealed that monoterpenes and saponins are working together synergistically by enhancing their activity far above a simple additive effect. 7

12 Summary (German) Wir untersuchten in einem umfangreichen Screening 82 Pflanzendrogen der traditionellen Chinesischen und Europäischen Phytomedizin. Dabei bildet die korrekte Identifizierung der zu testenden Arten die entscheidende Voraussetzung für jegliche weiterführende Untersuchung. Wir benutzten erfolgreich DNA Barcoding zur Identifizierung und fanden nur eine einzige Verfälschung: Arctium lappa war fälschlicherweise als Fraxinus rhynchophylla ausgegeben worden. Durch unser umfangreiches Screening von 246 Extrakten gegen Trypanosomen, Viren und Krebszellen gelang es uns, mehrere vielversprechende Pflanzen für weiterführende Untersuchungen auszuwählen. Besonders interessant erschien uns dabei Panax ginseng, Araliaceae, eine bemerkenswerte Heilpflanze mit langer Geschichte. Die Wirkung von Ginseng wird üblicherweise den Ginsenosiden, einer speziellen Gruppe von Saponinen, zugeschrieben. Dementsprechend untersuchten wir die Wirkung von 12 Ginsenosiden und konnten feststellen, dass die Position der Zuckergruppe am Molekül hauptverantwortlich für die großen Unterschiede in ihrer zytotoxischen Wirkung auf Zellmembranen ist. Eine Erklärung für die im Screening beobachtete Wirkung der Ginsengextrakte gegenüber Trypanosomen lieferten diese Ergebnisse jedoch nicht. Bei näherer Untersuchung der Hexanextrakte konnten wir feststellen, dass Panaxynol, das Hauptpolyacetylen von Ginseng Trypanosoma brucei brucei gegenüber hoch selektiv ist (IC 5 1. µg/ ml). Der Selektivitätsindex war mit 858 dreimal höher als der gängiger Arzneistoffe wie Suramin. Mit Carlinaoxid aus Carlina acaulis, Asteraceae, konnten wir ein weiteres gegenüber Trypanosomen hochselektives Polyacetylen entdecken (IC 5 1. µg/ ml bei einem Selektivitätsindex von 446). Als Wirkungsmechanismus für beide Polyacetylene schlagen wir die Hemmung der Trypanothionreduktase vor; dieses Enzym kommt nur in Trypanosomen vor und ist unverzichtbar für deren Schutz vor oxidativem Stress. Die Membranaktivität der Ginsenoside veranlasste uns, die Wirkung von Saponinen in der Phytomedizin näher zu untersuchen. Besonders auffällig ist dabei, dass Saponindrogen oft mit Monoterpendrogen in Erkältungstees kombiniert werden. Da sich beide Stoffgruppen strukturell stark unterscheiden, aber trotzdem denselben Angriffspunkt, die Biomembran, besitzen, wollten wir wissen, ob diese Kombination die Wirkung verstärken würde. Wir kombinierten mehrere Saponine mit Monoterpenen und untersuchten ihre Wirkung auf kernlose Erythrozyten und lebende Zellen. Erstaunlicherweise senkte diese Kombination die für Hämolyse nötige Dosis an Saponin um den Faktor, was sich auch in lebenden Zellen bestätigte. Dies zeigt, dass Monoterpene und Saponine ihre Aktivität weit über einen additiven Effekt hinaus synergistisch verstärken. 8

13 1. General Introduction 1.1 Traditional Chinese Medicine Traditional Chinese Medicine Traditional Chinese Medicine is as old as China itself. The beginnings of acupuncture and Fig. 1: Shi si jing fa hui (Expression of the Fourteen Meridians) Tokyo : Suharaya Heisuke kanko, Kyoho gan herbal medicine seem to date back to even before the Shang Dynasty (c. 16 to 145 BC) [1-4]. Our main knowledge besides historical descriptions from later dynasties such as the Shiji by Sima Qian is based on oracle bones with an archaic form of Chinese characters and bronze vessels. Basic Chinese imperial ideas such as the legitimization of the ruler by the Mandate of Heaven or ancestor worship date to this period [2-4]. The philosophical concept of the TCM theory however developed during the Han Dynasty (22 BC to 22 AD) [1,5]. The Han Dynasty is generally regarded as the period when classical Chinese culture became consolidated. Confucianism was adopted as state philosophy, and the country made great advances in many areas of the arts and sciences. Military expansion enabled the Han Dynasty to form trade links across the Silk Road to the west [2-4]. In this climate of progress medicine could also flourish and changed from local traditions to a theoretical concept that was accepted all over China. Confucianism was essential for this development by creating the ideological framework the different local adaptations could be fitted into [1]. The famous Huangdi Neijing, commonly regarded as the beginning of TCM, dates to the second century BC [1]. From then, the medicinal theory developed continuously until the system we know today was created. This development is always linked to individual, outstanding physicians, such as Hua Tuo, who lived during the late Han Dynasty and introduced surgery, or Sun Simiao who wrote the first Chinese encyclopedia of medicine during the Tang Dynasty (618 to 97 AD) [1]. Li Shizhen wrote the essential book on the Chinese herbal medicine, the

14 Compendium of Materia Medica (Bencao Gangmu) during the Ming Dynasty (1368 to 1644 AD) [1]. TCM experienced a revival in simplified form under Mao who wanted the system standardized to overcome the catastrophic healthcare situation in the countryside. Based on this, the modern TCM developed and became increasingly popular in the west. Theoretical concept of TCM Contrary to western medicine, TCM has a holistic approach to illness and medical treatment. The main concept is to balance the different functions of the body [5]. According to TCM, all aspects of the human body are linked, which can be exemplified by the pulse or tongue diagnosis used to draw conclusions about the general state of health of the patient [6]. An illness is commonly regarded as a disturbance of the harmony, which can be diagnosed in various ways [5]. Due to the holistic approach, the treatment also has to be a holistic one. Rather than to treat the symptoms or a specific illness, the concept seeks to restore the harmony and thus to treat the roots of the illness. To understand TCM, it is necessary to know some of the basic principles. The concept of dualism, commonly refered to as yin and yang is crucial for TCM [5,6]. Yin and yang, the two aspects of everything, are the basis of all treatment. Stemming from this are the qi, the five elements, and the meridians [5,6]. Qi is often explained as life energy, but has a far broader application in Chinese philosophy. The five elements are closely linked to the organs of the body and are essential for the general diagnosis. The meridian system, on the other hand, is used in the treatment and detailed analysis of the health disorder (Fig. 1). Disturbances of the flow of qi, the life energy, can be diagnosed in this way. The theoretical basis of acupuncture can be found here as well [5]. From the western point of view the complex theoretical system of TCM is a way to discribe symptoms. The resulting treatment is based on long evidence based experimental knowledge integrated into the philosophical world view of the Chinese cultural tradition. Major methods of treatment Acupuncture is the best known aspect of TCM and is increasingly used in the west as well to treat pain related health problems [6]. Patients are treated by insertion of needles into the body on the meridian points. It is often combined with moxibustion, the burning of Artemisia closely above the meridian points. Two variations exist either the moxa (Artemisia spec.) is 1

15 held above the meridian points and burned or it is added on top of an acupuncture needle and then ignited. Another common method to treat health problems is the cupping (Ba Guan) [6]. Several glass cups are placed on top of specific body parts, commonly the back. Due to an applied vacuum, the cups form pressure on the skin. The physician can diagnose the health problem from the effect on the skin. It is also used to treat muscle pain and back ache, and is partly related to massage techniques. The Tui Na massage is another method to restore the undisturbed flow of qi in the body and thus forms an important part in the holistic treatment traditionally applied in TCM [6] Chinese herbal medicine Chinese herbal medicine is integrated into the theoretical concept of TCM by sorting the herbs according to attributed properties such as cooling, heating, etc [7-11]. According to the theoretical concept, they are used to counterbalance deficiencies caused by diseases. Diseases causing a lack of heat thus are treated with herbs that possess heating properties to restore the balance in the human body [5,6,9]. However, we should not regard it as so simple since the long historical use and the huge number of herbs used in TCM allows a very individualized and specific treatment (Fig. 2). The combination of 1 or more herbs per formulation gives the physician the Fig. 2: Chinese herbal medicine store in Beijing, 26 possibility to individualize the treatment in a way not possible in western medicine [9]. Behind the theoretical concept of TCM thus is a solid phytotherapy based on thousands of years of experience. The large area of China combines various climatic zones from tropics over deserts to high altitudes, providing the basis for an especially rich flora [2]. Consequently TCM uses a huge number of medicinal plants that by far exceeds those used in European phytotherapy [7-11]. Currently, 4773 herbs are officially recognised for treatment in TCM, not to mention locally used plants that are not part of the Chinese pharmacopoeia [8]. 11

16 1.2 Secondary metabolites Ecological function Lacking the ability to avoid predators by flight or fight and lacking an immune system to fight microbes, plants developed two other methods to survive during 5 million years of evolution. One is the physical protection by bark or thorns, the other, secondary metabolites [12-18]. They are present in one form or another in all plants and form the most effective yet often unspecific defence system imaginable. So far more than different substances have been identified that can be grouped in nitrogen-containing (alkaloids, amines, nonprotein amino acids, peptides, etc) and nitrogen-free (terpenes, phenolics, saponins, polacetylenes, etc) molecules [12]. They are synthesized in specific pathways and stored in specifically for this task developed compartments and cells. Due to their complexity, they form a highly effective defence system against herbivores, fungi, bacteria and even viruses. Additionally, they are also used in the struggle between plants for ecological advantages by attracting animals for pollination or by hindering the growth of competing plants for light or water [12]. Especially rich in secondary metabolites are usually those parts vital for reproduction such as seeds, flowers, etc [12] Biosynthesis Contrary to the huge variability of natural products, the pathways used for their biosynthesis are few. Precursors are usually products of the primary metabolic pathways such as glucose or amino acids. These primary metabolites are the basis for the secondary metabolism. Here, the primary metabolites are transformed into secondary metabolites such as terpenes, saponins, alkaloids or tannins. Especially three pathways are essential for all plants: The glycolysis, the Krebs cycle and the Shikimate pathway. They are not only essential for the common processes in the cells such as respiration but also transform the primary metabolites into secondary metabolites. The different classes of secondary metabolites can generally be attributed to different pathways. While terpenes, saponins or fatty acids are among the products of the glycolysis, alkaloids are either products of the Krebs cycle or the Shikimate pathway. The Shikimate pathway is also involved in the production of flavonoids and tannins [19-25] Storage Secondary metabolites usually need to be transported from their place of origin to the storage compartments. This transportation can occur within the cell or via the xylem and phloem to specific storage cells in remote parts of the plant. 12

17 Hydrophilic secondary metabolites are mainly stored in the vacuole but also in laticifers and cell walls [19,26-32]. Most alkaloids, saponins and flavonoids are commonly found in the vacuole, while several specific alkaloids are concentrated in the laticifers. Tannins are usually found in the vacuoles and cell walls. One peculiar feature is that many hydrophilic molecules such as saponins are stored as prodrugs and are only activated once the cell is hurt. The disruption of the cell compartments leads to the release of enzymes that activate the molecules to their final form. Lipophilic secondary metabolites can be stored in specific oil cells, the cuticle, resin ducts or simply in the plastid membranes [19,26,33]. Oil cells are a specific defence mechanism rich in terpenoids. Closely related is the storage of waxes and terpenoids in the cuticle. Resin ducts and plastid membranes also contain terpenoids and even lipophilic flavonoids Classes of secondary metabolites Alkaloids are the most variable group of secondary metabolites [14-17,34-38]. They usually interact with specific target proteins such as ion channels, receptors or enzymes. Similarities to neurotransmitters like acetylcholine or noradrenalin enable them to modify neuronal signal transduction [15,34,39-45]. Non-protein amino acids are analogues of the protein amino acids. They can be incorporated into proteins by enzymes instead of common amino acids, resulting in the malfunction of vital processes [34,46]. Cyanogenic glucosides are in the vacuole stored prodrugs that are activated by the rupture of the cell. β-glucosidases cleave the sugar off the molecule which is hydrolyzed into hydrocyanic acid (HCN) and an aldehyde. HCN is extremely reactive and blocks the mitochondrial respiration [34,4,47-5]. Glucosynolates are also stored as prodrugs and only activated by cell damage. They are cleaved into mustard oil by myrosinase and interact with biomembranes, enzymes or DNA [34,48-5]. Terpenes are a group of highly variable lipophilic molecules that interact with biomembranes and the lipophilic core of proteins. Their membrane activity is rather unspecific, resulting in an increase of membrane fluidity [34,5]. Saponins also target the biomembrane [34,5,51]. They are glycosides of triterpenes or steroids and appear as mono- and bidesmosidic molecules. Bidesmosidic saponins are prodrugs that need enzymatic activation prior to be able to interact with biomembranes. Monodesmosidic saponins are amphiphilic molecules that interact with the lipid bilayer and 13

18 proteins of the biomembrane. One subgroup of the saponins is the cardiac glycosides that target the Na + -K + -ATPase. Flavonoids and polyphenols are phydrophilic molecules that interact with proteins via phenolic hydroxyl groups. While flavonoids are sometimes target specific and interact with enzymes, the polyphenols with more phenolic hydroxygroups are usually much less specific and interact with all proteins present [14,34,5,52,53]. Fig. 3: Targets for secondary metabolites in animal cells after Wink 28 [14] Mode of action The animal cell offers a wide range of targets for secondary metabolites (Fig. 3). The principal ones are proteins, the biomembrane and nucleic acids. Proteins are responsible for almost all processes in the cell. They act as receptors, ion channels, regulatory molecules such as transcription factors or signal molecules, transporters, catalytic enzymes and structural molecules. Their functionality depends on their three dimensional structure any conformational change usually modifies the activity of the protein [19,34]. Most secondary metabolites interact with proteins unselectively (Fig. 4). Fig. 4: Unspecific interaction of polyphenols with proteins after Wink 28 [14] 14

19 They are not specific for certain proteins but interact with all proteins by forming covalent or ionic bonds with free amino-, SH- or OH-groups. Molecules with epoxide or aldehyde groups bind to amino groups, while molecules with double or triple bonds interact with free SHgroups and epoxides. The Hydroxylgroups of polyphenols dissociate under physiological conditions into O - ions that form hydrogen and ionic bonds with electronegative atoms and Fig. 5: Interaction of saponins [1], mono- [2,3] and sesquiterpenes [4] with the biomembrane of animal cells after Wink and Schimmer 29 [34] alkaloids work this way [19,34,35,4]. positively charged side chains of the amino acids. The presence of several polyphenols leads to interactions that are strong enough to inactivate proteins [19,34]. Besides the unselective interaction of polyphenols a lot of secondary metabolites interact quite specifically with enzymes and receptors. They bind to the active binding site of the molecule due to structural similarities to endogenous ligands. There, they either activate or inactivate proteins and disturb for example the signal transduction of vital processes. This effect can be either reversible or, in worst case, irreversible. Many neurotoxic The biomembrane (Fig. 5) is the second major target of secondary metabolites [19,34]. Contrary to many interactions with proteins is the interference with the biomembrane purely unspecific. Monodesmosidic saponins are amphiphilic molecules whose lipophilic part integrates into the biomembrane while the hydrophilic part interacts with proteins or sugars on the membrane surface. Thus the fluidity of the lipid bilayer is enhanced while the Fig. 6: Intercalation of planar natural products into the DNA after Wink 28 [14] conformation of proteins is disturbed. Additionally the interactions with cholesterol in the lipid bilayer influence the microstructure of the biomembrane which also leads to conformational changes of receptors on the surface. Monoterpenes interact with the same target by integrating into the lipid bilayer and the lipophilic core of membrane proteins. Their interaction is 15

20 usually even less specific than that of saponins. They simply increase the membrane fluidity which results in leakage and eventually the rupture of the biomembrane. The third major target of secondary metabolites is nucleic acids such as DNA (Fig. 6) and RNA [15,19,34,41,44,45]. Several natural products interfere with proteins necessary for the replication of DNA and mrna. However, there exist also natural products that interact with the DNA directly. Epoxides and aldehydes like pyrrolizidine alkaloids or furanocoumarins bind covalently to functional groups of the DNA bases. Planar molecules with aromatic rings like the alkaloids berberine, emetine, quinidine or furanocumarins intercalate into the DNA by fitting between adenine-thymine or guanine-cytosine base pairs. There, they can cross-link DNA strands; a disturbed replication leads to apoptosis, mutations and even cancer. 16

21 1.3 African Trypanosomiasis Epidemiology African trypanosomiasis or sleeping sickness is a parasitic disease found in most sub-saharan countries. Human trypanosomiasis is caused by the protozoon Trypanosoma brucei rhodesiense and T. b. gambiense, while T. b. brucei, T. congolense, T. simiae and T. vivax are responsible for the cattle disease nagana [54-56]. T. b. gambiense is responsible for the chronic form of sleeping sickness with 9% of the cases. It occurs in west and central Africa, while T. b. rhodesiense, found in eastern and southern Africa, represents less than 1% of the cases and causes the acute form of the disease [57]. African trypanosomiasis is responsible for severe health and economic problems. After being nearly extinct in the middle of the 2 th century, it has been increasing since the independence of the African countries due to several reasons. The development of resistances against the commonly used drugs together with a decentralisation of the measures taken to fight African trypanosomiasis is among the reasons to explain this unfortunate trend. Nowadays, African trypanosomiasis is endemic again to 36 countries with 6 million people threatened by its consequences. Estimations of the WHO speak of 3 to 5 cases of human trypanosomiasis per year, while at least 46 million cattle are exposed to nagana, the cattle version of the disease [58-6] Classification The different trypanosome species with Trypanosoma Domain Eukaryota brucei and Trypanosoma cruzi as famous representatives Kingdom Excavata form part of the order of the Trypanosomatida, a group of Phylum Euglenozoa Class Kinetoplastida exclusively parasitic, single-cell uniflagellates. The Order Trypanosomatida Trypanosomatida are an order of the class of the Genera Trypanosoma Kinetoplastida, which consists mainly of parasitic, single-cell flagellates. Kinetoplastida can be separated into uniflagellates (Trypanosomastida) and biflagellates (Bodonida). The Kinetoplastida are part of the phylum Euglenozoa. Euglenozoa, which are separated into Kinetoplastida and Euglenida are unicellular organisms. While Euglenida often contain chloroplasts Kinetoplastida mostly are parasitic organisms. Euglenozoa are part of the kingdom of Excavata, one of the six kingdoms of the Eukaryota [61]. 17

22 1.3.3 Biology Human African trypanosomiasis and nagana are transmitted to their mammalian hosts by the tsetse fly (Glossina species) [54]. Accordingly, the occurrence of sleeping sickness is limited to the distribution of the tsetse fly. They inhabit most of mid-continental Africa between the Sahara and the Kalahari deserts. Tsetse flies are usually separated into savannah flies, forest flies and riverine flies based on their usual habitat and behaviour [62]. Only high altitudes and deserts are free of them. The name tsetse derives from Tswana, a language spoken in southern Africa and simply means fly [63]. Fig. 7: Life cycle of Trypanosoma brucei after CDC [64] Life Cycle The life cycle of African trypanosomiasis includes a Tsetse fly stage and a human stage (Fig. 7). By taking a blood meal, the infected tsetse fly injects the metacyclic trypomastigotes into the host. Now the human stage starts with the transformation of the metacyclic trypomastigotes into bloodstream trypomastigotes. These are distributed in the human body and multiply by binary fission. At first they occur mostly in the blood and the lymphatic system. After crossing the blood-brain barrier, they invade the central nervous system and 18

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