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Glossina Hytrosavirus Control Strategies in Tsetse Fly Factories: Application of Infectomics in Virus Management

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Glossina Hytrosavirus Control Strategies in Tsetse Fly Factories: Application of Infectomics in Virus Management Propositions 1. Hytrosaviruses cannot be used as bio-control agents for tsetse flies. (this thesis) 2. As an insect host metamorphoses to adulthood, vertical transmission of an insect virus becomes epizootically more important than horizontal transmission. (this thesis) 3. Microbial symbiosis is a remarkable source of evolutionary innovation. 4. The contents of a proteome, the repertoire of domains in the protein sequences, can be used to trace the evolutionary history of an organism. 5. The presence of protein-coding regions or open reading frames in a genome does not necessarily imply the presence of functional proteins. 6. The impression that hard work is degrading to fashionable life does not appeal to reason. 7. The maxim that ‘a slave’ first loses his name and then adopts the lingo is true in all facets of life. (Inference from ‘Mũrogi wa kagogo’, a satire by Ngũgĩ wa Thiong'o, 2006) Proposition belonging to the PhD thesis Glossina hytrosavirus control strategies in tsetse fly factories: Application of infectomics in virus management Henry Muriuki KARIITHI Wageningen, 20 November 2013 Glossina hytrosavirus control strategies in tsetse fly factories: Application of infectomics in virus management Henry Muriuki Kariithi Thesis committee Promotors Prof. Dr J.M. Vlak Personal Chair at the Laboratory of Virology Wageningen University Prof. Dr M.M. van Oers Professor of Virology Wageningen University Co-promotors Dr A.M.M. Abd-Alla Associate professor, Insect Pest Control Laboratories Joint FAO/IAEA Programme, Vienna, Austria Dr G.A. Murilla Centre Director, Trypanosomiasis Research Institute Kenya Agricultural Research Institute, Kikuyu, Kenya Other members Prof. Dr W. Takken, Wageningen University Prof. Dr D.G. Boucias, University of Florida, Gainesville, USA Prof. Dr J. van den Abbeele, Institute of Tropical Medicine, Antwerp, Belgium Prof. Dr S.C. de Vries, Wageningen University This research was conducted under the auspices of the Graduate School of Production Ecology and Resource Conservation. Glossina hytrosavirus control strategies in tsetse fly factories: Application of infectomics in virus management Henry Muriuki Kariithi Thesis submitted in partial fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. Dr M.J. Kropff, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Wednesday 20 November 2013 at 4.00 p.m. in the Aula. H.M. Kariithi Glossina hytrosavirus control strategies in tsetse fly factories: Application of infectomics in virus management, 207 pages. PhD thesis, Wageningen University, Wageningen, NL (2013) With references, with summaries in English, Dutch and Swahili ISBN 978-94-6173-753-3 To Graham, Jochebed and Leona Abstract African trypanosomosis is a fatal zoonotic disease transmitted by tsetse flies (Diptera; Glossinidae); blood-sucking insects found only in sub-Saharan Africa. Two forms of trypanosomoses occur: the animal African trypanosomosis (AAT; nagana), and the human African trypanosomosis (HAT; sleeping sickness). Since there are no effective vaccines against trypanosomosis, tsetse fly eradication is the most effective disease control method. Tsetse flies can be effectively eradicated by the sterile insect technique (SIT), which is applied in an area-wide integrated pest management approach. SIT is an environmentally benign method with a long and solid record of accomplishments. SIT requires large-scale production of sexually sterilized male flies (by exposure to a precise and specific dose of ionizing radiation, usually from a 60Co or 137Ce source), which are sequentially released into a target wild insect population to out-compete wild type males in inseminating wild virgin females. Once inseminated by sterile males, the virgin females do not produce viable progeny flies. Importantly, these females do not typically re-mate. Ultimately, the target wild insect population can decrease to extinction. However, tsetse SIT programs are faced with a unique problem: laboratory colonies of many tsetse species are infected by the Glossina pallidipes salivary gland hypertrophy virus (GpSGHV; family Hytrosaviridae). GpSGHV-infected flies have male aspermia or oligospermia, underdeveloped female ovarioles, sterility, salivary gland hypertrophy syndrome (SGH), distorted sex ratios, and reduced insemination rates. Without proper management, symptomatic GpSGHV infections (characterized by SGH symptoms) can cause collapse of Glossina colonies. To ensure colony productivity and survival, GpSGHV management strategies are required. This will ensure a sustained supply of sterile males for SIT programs. The aim of this PhD research was to investigate the functional and structural genomics and proteomics (infectomics) of GpSGHV as a prerequisite to development of rationally designed viral control strategies. A series of experiments were designed to: (i) investigate epidemiology and diversity of GpSGHV; (ii) identify GpSGHV proteome and how viral and host proteins contribute to the pathobiology of the virus; and (iii) investigate the interplay between GpSGHV, the microbiome and the host, and how these interactions influence the outcomes of viral infections. By relating GpSGHV and host infectomics data, cost-effective viral management strategies were developed. This resulted in significant reduction of GpSGHV loads and elimination of SGH from laboratory colonies of G. pallidipes. Table of Contents Abstract Chapter 1 General Introduction 11 Chapter 2 Dynamics of GpSGHV transmission in G. pallidipes colonies 25 Chapter 3 Prevalence and diversity of GpSGHV in wild G. pallidipes populations 45 Chapter 4 Proteome and virion components of GpSGHV 59 Chapter 5 Salivary secretome of GpSGHV-infected G. pallidipes 85 Chapter 6 Role of microbiome in GpSGHV transmission 103 Chapter 7 Management of GpSGHV infections in G. pallidipes colonies 125 Chapter 8 General Discussion 137 Appendix I 153 References 155 Abbreviations and definition of terms 185 Summary 189 Samenvatting 191 Muhtasari 195 Acknowledgements 199 List of publications 203 PE&RC education certificate 205 Affiliations, credits and grants obtained 207 Chapter 1 General introduction Introduction This PhD dissertation covers various aspects of the pathobiology, epidemiology, morphology and morphogenesis of the Glossina pallidipes salivary gland hypertrophy virus (GpSGHV), a double-stranded DNA (dsDNA) virus classified in the Hytrosaviridae family of insect viruses (ICTV; Abd-Alla et al., 2009b). GpSGHV is a major pathogen of laboratory colonies of Glossina spp. (Diptera; Glossinidae). Typically, a small proportion of laboratory G. pallidipes flies infected by GpSGHV develop hypertrophied salivary glands and midgut epithelial cells, and show gonadal/ovarian anomalies, distorted sex ratios, reduced insemination rates, fecundity and lifespan. These symptoms are rarely observed in wild tsetse fly populations. In East Africa, G. pallidipes is one of the most important vectors of the debilitating zoonotic disease, African trypanosomosis. A large arsenal of tsetse and trypanosomosis management tactics is available. The sterile insect technique (SIT) is a robust and effective method to eradicate tsetse fly populations when integrated with other control tactics in an area-wide integrated approach. SIT requires production of sterile male flies in large-scale tsetse production facilities. To supply sufficient numbers of sterile males for the SIT component against G. pallidipes, strategies must be developed to manage GpSGHV infections in the fly colonies. This chapter provides a historic account of tsetse fly and trypanosomoses control, and a chronology of the emergence and biogeography of hytrosaviruses. The thesis rationale is also described. African trypanosomoses – the "neglected tropical diseases" Tsetse flies are important vectors of two debilitating diseases; human African trypanosomosis (HAT or sleeping sickness), and animal African trypanosomosis (AAT or Nagana) (Mattioli et al., 2004). Tsetse flies and trypanosomosis render vast areas of agricultural land un-exploitable, especially during the rainy seasons (Mamoudou et al., 2008). Although there are over 30 species and sub-species of tsetse, most of which can transmit trypanosomosis, only 8-10 of these species are of medical and agricultural importance. The most important tsetse vectors are the riverine species (G. palpalis, G. fuscipes, and G. tachinoides) in Western and Central Africa and the savannah species 11 Chapter 1 (G. morsitans, G. austeni and G. pallidipes) in Eastern and Southern Africa (Smith et al., 1998). Although tsetse fly fossils have been found in 26-million-year-old shales of Florissant, Colorado, USA (Cockerell, 1907), to date, tsetse flies are confined to Africa except from an isolated population on the Arabian Peninsula (Elsen et al., 1990). HAT is one of the most serious of the so-called 'neglected tropical diseases' (NTDs) (Hotez and Kamath, 2009). NTDs are a group of chronic diseases endemic in low- income populations in Africa, Asia and the Americas (Hotez et al., 2007). Trypanosomosis is restricted to 37 sub-Saharan African countries and its distribution extends to more than 10 million square kilometres of the African continent (Cecchi et al., 2008) (Figure 1). Figure 1: Representation of the distribution of different tsetse fly species in sub-Saharan African countries. The different colours in the figure legend represent the different tsetse fly species in the map (Map
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