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Determining the Role of the Peritrophic Matrix in Trypanosoma Brucei Migration Through the Midgut of Glossina Morsitans Morsitans

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Determining the Role of the Peritrophic Matrix in Trypanosoma Brucei Migration Through the Midgut of Glossina Morsitans Morsitans Unzipping the barriers: Determining the role of the peritrophic matrix in Trypanosoma brucei migration through the midgut of Glossina morsitans morsitans Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy by: Clair Rose April 2016 © Clair Rose 2016 i ABSTRACT Unzipping the barriers: Determining the role of the peritrophic matrix in Trypanosoma brucei migration through the midgut of Glossina morsitans morsitans By Clair Rose Tsetse flies serve as biological vectors for several species of African trypanosomes. These parasites undergo a life-cycle stage in both mammals and in the insect. Within the fly, it is proposed that for successful survival, proliferation and establishment of a midgut infection, trypanosomes must cross the tsetse fly peritrophic matrix (PM). Although having been well documented, the mechanism(s) of how trypanosomes are able to cross the PM is not well understood and the crossing event has never been visualised. The peritrophic matrix is an acellular secretion that lines the guts of most insects and is mainly composed of chitin and glycoproteins. The functions of the PM involve facilitating digestion, and epithelial cell protection against ingested pathogens, toxins and against mechanical damage. In order to better understand the nature of the tsetse PM, dissected PMs from lab-reared Glossina morsitans morsitans were solubilised under stringent conditions and their protein composition determined using a mass spectrometry-based proteomics approach. It was found that the tsetse PM is comprised of just short of 300 proteins, including several proteins from the tsetse endosymbiont, Sodalis glossinidius. Tsetse PM proteins were classified into functional groups as peritrophins, enzymes, immune related proteins and other proteins. This study also includes the first report of three tsetse PM peritrophins (GMOY002708, GMOY007191 and GMOY011810), increasing the known repertoire of peritrophins from two to five. Peritrophins were then further classified into four main groups comprising simple, binary, complex and repetitive based on their structural organisation. Comparisons of these peritrophins in Glossina morsitans morsitans were carried out against orthologous proteins of several major Glossina vectors and two comparative non blood-feeders, Musca domestica and Drosophila melanogaster. The vast number of peritrophins in M. domestica and D. melanogaster compared to those in Glossina, and given the feeding habits of these flies, suggested that the PM peritrophins have a role in the protection of the midgut against ingested pathogens. Additionally, peritrophin silencing by RNAi provided information regarding the expression and regulation of peritrophins. Multiple microscopy techniques showed the presence of trypanosomes within the layers of the PM which has previously been shown before. However, there was no evidence of ii trypanosomes crossing the mature PM in the anterior midgut as judged by tissue tomography analysis and 3D reconstruction. Subsequent analysis of the tsetse proventriculus (PV; site of PM secretion) revealed that trypanosomes could be seen in this tissue both between and either side of the PM from as soon as 5 days after receiving a trypanosome-infected bloodmeal. This suggests that the immature PM within the PV provides a probable point of entry for parasites after differentiation into the procyclic life stage. Moreover, the opportunity for breaching of the PM must occur quite quickly after bloodmeal ingestion as refractory flies had already cleared the infection by 5 days post infection. Overall, the results from this thesis suggest that the tsetse PM: a) is structurally composed of a family of peritrophins that differ in complexity and confer resistance to degradation by trypanosomes in the midgut b) functions as a way to clear parasite infections by engulfing them before elimination in the hindgut; and c) the lifecycle of T. brucei may occur entirely (or in parallel with a developmental cycle in the ectoperitrophic space) within the PV of the fly where they are proposed to complete maturation before migration to the salivary glands. iii DECLARATION I hereby certify that this dissertation constitutes my own product, that where the language of others is set forth, quotation marks so indicate, and that appropriate credit is given where I have used the language, ideas, expressions or writings of another. I declare that the dissertation describes original work that has not previously been presented for the award of any other degree of any institution. Signed, …………………………………………………………………. iv Dedications This thesis is dedicated to my two best mates To my mum, Carol 1948-2013 R.I.P my guardian angel Hope I have made you proud and continue to do so To my Ellie You make me proud every day “The minute you think of giving up, think of the reason you held on for so long” - Author unknown v Acknowledgements To my supervisor Alvaro Acosta-Serrano, you had me at ‘sexy flies’! Thank you for taking a chance on me all those years ago when neither of us could understand each other. Now that my Scouse has been honed and I can understand your Spanglish, I wanted to say how grateful I am to you for everything you have done throughout my Ph.D., both professionally and personally. To Mike Lehane, for your invaluable T.E.M insights and pearls of wisdom. You showed me we don’t all have to be born with silver spoons in our mouths to succeed. To Lee and Dee, the terrible two! For the great discussions and advice but most of all for the great laughs. If the Ph.D. falls through at least I know I will have a secondary career to fall back on, even if it’s only you two in the audience laughing at the tales of woe that is my life. To the greatest lab group there ever was past and present, for the good times, the laughs, the late nights and the lunches. For keeping me sane and grounded through some of the toughest times of my life and for making my time so enjoyable. To the people who helped make completion of this project possible, Naomi, Ben, Carla, Dan, Ali and Marco. To the LSTM for funding my studentship And to Ellie. For being you. vi Table of contents List of abbreviations ............................................................................................................ xiii List of tables ....................................................................................................................... xvi List of figures ...................................................................................................................... xvi Chapter 1 ........................................................................................................................ 1 1.1 General Introduction ....................................................................................................... 2 1.2 Importance of trypanosomiasis ....................................................................................... 2 1.3 Tsetse fly biology ............................................................................................................ 5 1.4 Trypanosome biology ...................................................................................................... 5 1.5 Development of T. brucei in the tsetse vector ................................................................. 5 1.6 Insect gut ........................................................................................................................ 7 1.7 Insect Peritrophic Matrix ............................................................................................... 10 1.7.1 Tsetse Peritrophic Matrix ........................................................................................... 10 1.7.1.1 Production and Structure ........................................................................................ 10 1.7.1.2 Chitin ...................................................................................................................... 10 1.7.1.3 Peritrophins ............................................................................................................. 11 1.7.1.4 Insect Intestinal Mucins ........................................................................................... 11 1.7.1.5 Function .................................................................................................................. 12 1.7.1.6 Permeability ............................................................................................................ 12 1.8 Recent findings on the functions of peritrophic matrices and implications for novel vector control strategies and transmission blocking vaccines ........................................................ 13 1.9 Aims and objectives of this study .................................................................................. 14 Chapter 2 ...................................................................................................................... 15 2.1 Introduction ................................................................................................................. 16 2.2 Materials and Methods ............................................................................................... 19 2.2.1 Tsetse fly maintenance and dissection of peritrophic matrices ................................... 19 2.2.2 Mild acid hydrolysis of G. m. morsitans PM proteins .................................................. 19 2.2.3 Chemical de-glycosylation of G. m. morsitans
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