Rhipicephalus (Boophilus) Microplus and Rhipicephalus Appendiculatus Ticks and Determination of the Expression Profile of Bm86
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001-008 - Title page & table of contents 17x24 020810.pdf 1 2-8-2010 20:42:11 A contribution to the development of anti-tick vaccines A.M. Nijhof, 2010 PhD thesis Utrecht University, the Netherlands Printed by Atalanta Drukwerkbemiddeling, Houten ISBN 978-90-393-5376-9 001-008 - Title page & table of contents 17x24 020810.pdf 2 2-8-2010 20:42:11 A contribution to the development of anti-tick vaccines Een bijdrage aan de ontwikkeling van vaccins tegen teken (met een samenvatting in het Nederlands) Proefschrift ter verkrijging van de graad van doctor aan de Universiteit Utrecht op gezag van de rector magnificus, prof. dr. J.C. Stoof, ingevolge het besluit van het college voor promoties in het openbaar te verdedigen op dinsdag 7 september 2010 des middags te 12.45 uur door Ard Menzo Nijhof geboren op 24 maart 1978 te Zeist 001-008 - Title page & table of contents 17x24 020810.pdf 3 2-8-2010 20:42:11 Promotoren: Prof. dr. F. Jongejan Prof. dr. J.P.M. van Putten This research described in this thesis was financially supported by the Wellcome Trust under the 'Animal Health in the Developing World' initiative through project 075799 entitled 'Adapting recombinant anti-tick vaccines to livestock in Africa'. 001-008 - Title page & table of contents 17x24 020810.pdf 4 2-8-2010 20:42:11 In liefdevolle herinnering aan Bert Nijhof (1946-1998) 001-008 - Title page & table of contents 17x24 020810.pdf 5 2-8-2010 20:42:11 001-008 - Title page & table of contents 17x24 020810.pdf 6 2-8-2010 20:42:11 Table of contents Chapter 1 General introduction 9 Chapter 2 Gene silencing of the tick protective antigens, Bm86, Bm91 45 and subolesin, in the one-host tick Boophilus microplus by RNA interference Chapter 3 Evidence of the role of tick subolesin in gene expression 69 Chapter 4 Selection of reference genes for quantitative RT-PCR studies in 97 Rhipicephalus (Boophilus) microplus and Rhipicephalus appendiculatus ticks and determination of the expression profile of Bm86 Chapter 5 Bm86 orthologues and the novel ATAQ protein family with 125 multi Epidermal Growth Factor (EGF)-like domains from hard and soft ticks Chapter 6 Expression of recombinant Rhipicephalus (Boophilus) 153 microplus, R. annulatus and R. decoloratus Bm86 orthologs as secreted proteins in Pichia pastoris Chapter 7 Summarizing discussion 181 Summary in Dutch / Samenvatting 197 Acknowledgements 205 Curriculum Vitae 211 List of Publications 213 001-008 - Title page & table of contents 17x24 020810.pdf 7 2-8-2010 20:42:11 001-008 - Title page & table of contents 17x24 020810.pdf 8 2-8-2010 20:42:11 1 GENERAL INTRODUCTION 2 PhD thesis Nijhof - Title page chapter 1.pdf 1 26-7-2010 22:46:20 001-125 - Dissertatie Ard.pdf 10 21-7-2010 0:13:07 General introduction 1.1 Evolution, diversity and systematics of ticks Ricini e gramine oriuntur – Ticks originate from grass Aristotle, 350 BC. Historia Animalium The oldest tick fossils known to date are those that are entrapped in amber, an an- cient tree resin. When this sticky resin was exuded by a tree, insects and other small organisms were glued to its surface and became gradually engulfed by the flowing resin which could preserve them in fine detail. The majority of the tick inclusions in amber originate from Baltic (35-50 mya) and Dominican (15-40 mya) amber, but the oldest tick fossils of 90-100 million years of age were found in amber outcroppings in New Jersey and Burma (presently Myanmar) [1-3]. Carios jerseyi, the fossil found in New Jersey was identified as a soft tick, whereas the fossils found in Burmese amber belonged to two different genera of hard ticks, demonstrating that these lineages of ticks were well established by this time in the middle Cretaceous. The origin of ticks is thus pre-middle Cretaceous. Fossil tick specimens of a more recent origin include those found in Oligocene deposits (ca. 30 mya) [4] and in the ears of a frozen woolly rhinoceros from 2-5 mya [5]. Fossilized faeces or coprolites and mummies containing tick specimens of several thousand years old have been found in the Americas [6-8]. Of similar age is the drawing found in the Egyptian tomb of Antef from 1500 B.C. on which a hyena-like animal is depicted with round shapes resembling ticks in its ear, which may be the first drawing of ticks (Fig. 1) [9]. 11 001-125 - Dissertatie Ard.pdf 11 21-7-2010 0:13:07 Chapter 1 Figure 1. Fragment from the drawing of hyena-like animal discovered in the Egyp- tian tomb of Antef, dating from the time of Thutmose III (eighteenth dynasty), about 1500 B.C. In literature, the first appearance of ticks is probably made in Homer’s Odyssey (ca. 800 B.C.). Upon his return home twenty years after leaving for the Trojan War Odysseus is recognized - despite being disguised as a beggar - by his faithful dog Argos who is overgrown with ticks. The dog wags its tail and then dies in peace. Another Greek, the philosopher Aristotle, was the first to explicitly describe the bloodsucking habit of ticks in one of Aesop’s fables. In this tale the fox is trapped in a gully while trying to cross a river and suffered for a long time, in particular from the large number of ticks she had on her. A passing hedgehog took pity and offered to take the ticks of her which is refused by the fox. When asked why, the fox replied ‘These ticks have already had their fill of me, and they are taking only a little blood. But if you take these away, others will come and in hunger drink up the rest of my blood’ (Rhetoric 2.20) [10, 11]. Aristotle, in his Historia Animal- ium, also mentions that dogs, cows, sheep and goats have ticks, but claims that donkeys are free of them [11]. 12 001-125 - Dissertatie Ard.pdf 12 21-7-2010 0:13:08 General introduction The Swedish botanist Karl Linnaeus (1707-1778), founder of modern biological nomenclature, included the first binominal classification and description of three tick species which are nowadays known as Ixodes ricinus, Hyalomma aegyptium and Amblyomma americanum in his Systema Naturae [12]. More descriptions of new tick species followed, most numerously by men such as Carl Ludwig Koch (1778-1857), Louis-Georges Neumann (1846-1930), Paul Schulze (1887-1949), Glen M. Kohls (1905-1986) and Harry Hoogstraal (1917-1986). Approximately 879 different tick species have been described to date [13] which can be found throughout the terrestrial world from regions as high as 15,000 feet altitude in the Himalaya mountain range [14] to dark abandoned and bat-inhabited mines and from the coldness of the Antarctic peninsula [15] to the heat of Africa’s deserts. Ticks are classified as members of the Arachnida class, sharing the subclass Acari together with mites. A distinguishing feature between the arachnids and insects is the presence of four pair of legs in adult arachnids compared to three pair of legs in insects. Ticks are further divided into three families: the Argasidae or soft ticks, the Ixodidae or hard ticks and the Nuttalliellidae. A hard sclerotized shield or scu- tum found on the anterior dorsal surface of hard ticks is absent in soft ticks and forms a striking difference between these two families. Other anatomical differ- ences include the aspect of the outer body wall or integument which is leathery in soft ticks while smooth with fine grooves in hard ticks, and the position of the mouthparts. These are located ventrally in soft ticks and anterior in hard ticks, making them always visible from a dorsal aspect in ticks of the latter family (Fig. 2). The sole representative of the monotypic Nuttalliellidae family, the illustrious Nuttalliella namaqua of which very few specimens have been recorded, has fea- tures characteristic of both soft and hard ticks [16, 17]. The hard ticks form the largest family with approximately 692 species divided over 12 genera while the soft ticks comprise 4 genera with 186 species. The hard ticks can be further divided in two lines: the Prostriata and the Metastriata. The Prostriata is regarded as the most primitive line and consist of the Ixodes genus only. The majority of the 245 species which make up this genus are nest- or bur- row-dwelling (nidicolous) parasites. Ixodes adults can copulate both on and off the host in contrast to Metastriata adults which mate only on the host. The Metas- triata can be further divided into four subfamilies: the Bothriocrotoninae, a small group of five species of the Bothriocroton genus indigenous to Australia, the Am- blyomminae containing ticks of the Amblyomma genus, the Haemaphysalinae containing ticks of the Haemaphysalis genus and the Rhipicephalinae containing ticks of the Anomalohimalaya, Cosmiomma, Dermacentor, Hyalomma, Margaro- 13 001-125 - Dissertatie Ard.pdf 13 21-7-2010 0:13:08 Chapter 1 pus, Nosomma, Rhipicentor and Rhipicephalus genera [18]. The latter includes ticks of the economically important Boophilus genus since these were syn- onymized with Rhipicephalus following phylogenetic analyses [19]. Boophilus (from Latin bos = ox and Greek philein = loving) was retained as a subgenus, but the suggested synonymization is controversial and not universally accepted [20]. Carios is the largest soft tick genus with 89 species, followed by the Argas, Orni- thodoros and Otobius genera. Figure 2. Top panel: dorsal (left) and ventral (right) view of an Ixodes ricinus fe- male, representative of a hard tick species. Bottom panel: dorsal (left) and ventral (right) view of an Ornithodoros savignyi female, representative of a soft tick spe- cies.