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Acute Phase Response and the Possible Involvement of an Endotoxin-Like Molecule in the Pathogenesis of Murine African Trypanosom

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Acute Phase Response and the Possible Involvement of an Endotoxin-Like Molecule in the Pathogenesis of Murine African Trypanosom ACUTE PHASE RESPONSE AND THE POSSIBLE INVOLVEMENT OF AN ENDOTOXIN-LIKE MOLECULE IN THE PATHOGENESIS OF MURINE AFRICAN TRYPANOSOMIASIS Department of Veterinary Clinical Studies, University of Glasgow Veterinary School. BY RAPHAEL MUCHANGI NGURE BVM. (NAIROBI) A thesis submitted for the degree of Doctor of Philosophy Faculty of Veterinary Medicine University of Glasgow February 1996 © Raphael Muchangi Ngure ProQuest Number: 13832512 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a com plete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest ProQuest 13832512 Published by ProQuest LLC(2019). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States C ode Microform Edition © ProQuest LLC. ProQuest LLC. 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106- 1346 i ojn I ABSTRACT This thesis describes a series of studies in mice infected with either Trypanosoma brucei brucei and Trypanosoma congolense, with the primary aim of identifying the pathogenic mechanism responsible for the acute phase response which occurs during African trypanosomiasis. The acute phase response was monitored by measuring the acute phase proteins, serum amyloid P-component (SAP) and haptoglobin (Hp) during a tissue invasive and non­ tissue invasive infection. The possible involvement of trypanosome endotoxin in the pathogenesis of trypanosomiasis was also investigated, by measuring the endotoxin levels and acute phase proteins in plasma of infected animals during treatment with either a general, systemic antibiotic (norfloxacin) or one that is restricted to the intestinal tract and binds to and neutralises the pathogenic effects of endotoxin (polymyxin-B). In addition, the endotoxin-like molecule(s) in trypanosome lysates or enriched protein membranes were examined to determine the presence of lipopolysaccharide or the active moiety, lipid-A, using polyacrylamide gel electrophoresis and the silver stain, or Western blot utilising a lipid-A specific monoclonal antibody. Chapter I comprises an introduction and literature review on African trypanosomiasis with emphasis on endotoxin, cytokines and acute phase proteins. Chapter II describes the general materials and methods used in these studies. Chapter III describes the development of a direct antigen enzyme linked immunosorbent assay (ELISA) for the quantification of mouse serum amyloid P-component. Chapter IV describes the acute phase response during chronic murine trypanosome infection with tissue invasive and non-invasive trypanosomes, and II the effect of subcurative treatment with the trypanocidal drug, diminazine aceturate. It was found that the acute phase proteins SAP and haptoglobin increased significantly after infection. Following infection withT. b. brucei, SAP increased in both infections to peak 7-10 days after infection (DAI), after which it declined to levels just above control values where it remained for the rest of the infection period. In contrast, withT. congolense infection a second peak occurred around 34 DAI. The levels of SAP were not affected by the treatment with diminazine aceturate. Haptoglobin (Hp) increased to peak at 7-10 DAI, and remained elevated throughout the infection in both experiments, but decreased significantly following treatment with diminazine aceturate in theT. congolense but not in the T. brucei infection where it remained elevated. The diminazine aceturate treatment in T. brucei infected mice resulted in severe cellular infiltration of mononuclear cells in the brains of these animals. As acute phase response occurs with both species of trypanosomes, it was concluded that tissue invasiveness is not the main means by which trypanosomes initiate tissue damage in infected hosts but that tissue pathology in the brain can cause synthesis of acute phase protein in the liver. Chapter V describes the changes in plasma endotoxin-like activity, the concentration of the acute phase proteins, SAP and Hp, and tissue pathology during chronicT. b. brucei infections in mouse, the presence or absence of an antibiotic umbrella, with norfloxacin or polymyxin-B. The concentration of acute phase proteins and endotoxin-like activity increased significantly following infection. The animals also showed varying pathological changes during the different stages of infection. The spleen showed cellular activity, livers were markedly infiltrated with inflammatory cells with occasional necrosis, while the choroid plexus of the brains was infiltrated by trypanosome. Treatment with the antibiotic polymyxin-B, had no significant effect on any of ill the parameters examined, whereas in the norfloxacin-treated animals there was a small but significant decrease in the haptoglobin levels in the terminal stages of infection after 21 DAI. The norfloxacin-treated animals also showed reduced liver pathology but only in the early stages of infection, i.e., before 21 DAI. Chapter VI describes the characterisation of trypanosome lysate and protein-enriched membrane proteins by the silver stain and by Western blot. The results showed that trypanosomes do not contain a gram negative bacteria­ like LPS molecule. On the other hand, the lipid-A monoclonal antibody (8A1) recognised epitopes on trypanosome lysate and protein-enriched membranes on Western blots; this were destroyed by pre-treatment of the samples with proteinase K, suggesting they are protein in nature or are associated with protein. The general discussion and conclusions drawn from the study are presented in chapter VII. African trypanosomiasis causes an acute phase response and tissue damage probably by the production of pro-inflammatory cytokines which are induced probably by molecule(s) from trypanosomes with endotoxin-like activity. The molecule(s) responsible for the increased endotoxin-like activity is of trypanosome origin. Although this molecule(s) has lipid-A like activity and epitopes recognised by lipid-A monoclonal antibody, this trypanosome molecule(s), is dissimilar to the gram negative bacteria LPS. IV DECLARATION The work presented in this thesis is original and has been carried out solely by the author, except where collaboration with others has been acknowledged. Raphael Muchangi Ngure v ACKNOWLEDGEMENTS The success and completion of the studies reported in this thesis is as a result of help, collaboration and input from several people. I would like to give special thanks to the members of the Department of Veterinary Clinical Studies and Veterinary Parasitology, University of Glasgow Veterinary School for the technical help and advice, especially Ms Jean Rodgers, Arlene Macrae, Mr Chris McComb, David Harvey, David Moffat, David French, Christine Marshall and Brian Wright. I am very thankful for the collaborative efforts of my supervisors Dr(s) P.D. Eckersall, Joanne M. Burke, F.W. Jennings and Prof. Max Murray for their constant encouragement and guidance in carrying out these studies and to their criticism during the writing of this thesis. Their continual collaborative assistance helped shape the nature of these studies and the interpretation of the results obtained. Special thanks go to Mr. Colin Chapman and Mrs. Barbara Bradley, of the Department of Veterinary Parasitology for performing the animal infections, maintaining the experimental animals and collecting samples; I am thankful to the members of staff in the Department of Veterinary Pathology for processing tissues for histology and to Mr Alan May for the help with the photographic materials. I am very grateful to the collaboration effort of Dr D. Heumann of the Division of Infectious Disease Lausanne, Switzerland for doing the cytokine assays. Special thanks go to Centorcor, Malvern, Pennsylvania, (USA) for kindly providing the anti lipid-A monoclonal antibody (8A1). The statistical analysis of the data would have been difficult without the kind help and guidance from Dr. M. J. Stear of the Department of Veterinary Clinical Studies. VI A special appreciation to all my colleagues in the Veterinary Clinical Studies, University of Glasgow, Veterinary School, especially Mr. Messa Dyiaye and Mrs. Susan Duthie for their support and company. I would like to thank the British Council for funding my studies and stay in Glasgow for the study period, and the Director, Kenya Trypanosomiasis Research Institute, for allowing me study leave. Finally, I would like to express my gratitude to my mum, family and friends for their continued support, prayers, moral support and encouragement during the last three years. VII DEDICATION To my mum, thank you for your encouragement, prayers and love. To my dad, I am sure you would have been happy and proud for all the effort you put into all this. To my God Jehovah, great is Thy faithfulness, great is Thy faithfulness o GOD my father, great is thy faithfulness, great is thy faithfulness, morning by morning new mercies I have seen; all I have needed Thy hand hath provided, great is Thy faithfulness, Lord, unto me. VIII TABLE OF CONTENTS Title i Abstract ii Declaration V Acknowledgements vi Dedication viii Table of Contents ix List of Tables xxi List of Figures xxii List of Appendices xxxii Abbreviations xxxiii CHAPTER 1 1 INTRODUCTION AND GENERAL 1 LITERATURE REVIEW 1.1 INTRODUCTION 2 1.2 CLASSIFICATION OF TRYPANOSOMES
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