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Wolbachia Endosymbiont of Onchocerca Volvulus: Driver of Immunopathology and Target for Therapy

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Wolbachia Endosymbiont of Onchocerca Volvulus: Driver of Immunopathology and Target for Therapy Wolbachia endosymbiont of Onchocerca volvulus: driver of immunopathology and target for therapy Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy by Francesca Tamarozzi October 2012 I TABLE OF CONTENTS LIST OF FIGURES……………………………………………………………………………VI LIST OF TABLES……………………………………………………………………………VIII ABBREVIATIONS…………………………………………………………………………….IX ABSTRACT……………………………………………………………………………………XII Chapter 1. INTRODUCTION TO ONCHOCERCIASIS…………………………......1 1.1 Parasitological and epidemiological features ....................................... 1 1.2 Wolbachia endosymbionts of filarial nematodes .................................. 3 1.3 Onchocercal disease in humans ......................................................... 5 1.4 Therapy and control of onchocerciasis .............................................. 14 1.5 Aim of the work ................................................................................ 18 Chapter 2. EVALUATION TRIAL: LONG TERM IMPACT OF COMMUNITY- DIRECTED DELIVERY OF DOXYCYCLINE FOR THE TREATMENT OF ONCHOCERCIASIS ....................................................................................... 23 ABSTRACT…………………………………………………………………………………….23 2.1 INTRODUCTION ............................................................................... 24 2.1.1 Rationale ................................................................................... 24 2.1.2 Study design .............................................................................. 25 2.2 METHODS ....................................................................................... 28 2.2.1 Data collection ........................................................................... 28 2.2.2 Evaluation of microfilaridermia and onchocercomas .................. 28 2.2.3 Ultrasonography of onchocercomas ............................................ 29 2.2.4 Statistical analysis ..................................................................... 29 2.3 RESULTS ......................................................................................... 29 2.3.1 Study population ....................................................................... 29 2.3.2 Microfilaridermia prevalence and load ........................................ 31 2.3.3 Palpable nodule prevalence and load .......................................... 33 2.3.4 Results of ultrasonography of palpable nodules ......................... 34 2.4 DISCUSSION .................................................................................... 36 Chapter 3. CYTOKINE RESPONSES IN GHANAIAN MICROFILARIDERMIC ONCHOCERCIASIS PATIENTS AND CONTROLS .......................................... 39 ABSTRACT…………………………………………………………………………………….39 3.1 INTRODUCTION ............................................................................... 40 3.1.1 Cytokine profile in onchocerciasis .............................................. 40 II 3.1.2 Scope of the experimental study ................................................ 47 3.2 METHODS ....................................................................................... 48 3.2.1 Study populations ..................................................................... 48 3.2.2 Stimuli for cell culture ............................................................... 48 3.2.3 Isolation and culture of PBMC ................................................... 49 3.2.4 Assessment of cytokines in PBMC culture supernatants by ELISA …………………………………………………………………………………………… 49 3.2.5 Assessment of microfilaridermia ................................................ 50 3.2.6 Statistical analysis ..................................................................... 50 3.3 RESULTS ......................................................................................... 51 3.3.1 Study population ....................................................................... 51 3.3.2 Type-1 (IFNγ) immune response ................................................. 52 3.3.3 Type-2 (IL-5 and IL-13) immune responses ................................ 54 3.3.4 Type-17 (IL-17A) immune response ............................................ 58 3.3.5 Innate pro-inflammatory (IL-6 and TNFα) immune responses ..... 60 3.3.6 Anti-inflammatory (IL-10) immune response .............................. 65 3.3.7 Synopsis of results……………………………………………………67 3.4 DISCUSSION .................................................................................... 67 Chapter 4. THE INTERACTION BETWEEN NEUTROPHILS AND WOLBACHIA ................................................................................................. 71 ABSTRACT…………………………………………………………………………………….72 4.1 INTRODUCTION ............................................................................... 73 4.1.1 Overview of neutrophils biology .................................................. 73 4.1.2 TLRs, lipoproteins and neutrophils: a literature review ............... 75 4.1.3 The role of neutrophils in helminth infections ............................ 81 4.1.4 Neutrophils-Wolbachia interaction and their role in onchocerciasis ………………………………………………………………………………….81 4.1.5 Scope of the experimental study ................................................ 87 4.2 METHODS ....................................................................................... 88 4.2.1 Stimuli for neutrophil functional assays..................................... 88 4.2.2 Evaluation of filarial extracts and WoLP reactivity ...................... 89 4.2.3 Isolation and culture of human neutrophils ............................... 89 4.2.4 Morphological assessment of neutrophil activation ..................... 90 4.2.5 Chemotaxis and chemokinesis assays ........................................ 90 III 4.2.6 Assessment of surface adhesion molecules and Fcγ Receptors expression .......................................................................................... 91 4.2.7 Assessment of neutrophil apoptosis ........................................... 92 4.2.8 Respiratory burst chemiluminescence assay .............................. 92 4.2.9 Measurement of cytokines by ELISA .......................................... 93 4.2.10 Statistical analysis ..................................................................... 93 4.3 RESULTS ......................................................................................... 93 4.3.1 Reactivity of filarial soluble extracts and WoLP ........................... 93 4.3.2 Neutrophil purity and viability after isolation ............................. 94 4.3.3 Neutrophils acquire activated cell morphology upon exposure to WoLP ………………………………………………………………………………….94 4.3.4 WoLP exerts a chemotactic effect on neutrophils ........................ 94 4.3.5 WoLP modulates the surface expression of the β2-integrin CD11b/CD18 and of L-Selectin in neutrophils .................................... 97 4.3.6 WoLP modulates surface expression of Fcγ Receptors in neutrophils ......................................................................................... 98 84.3.7 Apoptosis is delayed in neutrophils exposed to WoLP ................. 98 4.3.8 WoLP directly induces and primes for the production of reactive oxygen species .................................................................................. 101 4.3.9 Exposure to WoLP induces the production of IL-8 by neutrophils ………………………………………………………………………………...104 4.4 DISCUSSION .................................................................................. 105 Chapter 5. CELLULAR SOURCE OF WOLBACHIA-DEPENDENT IL-17A PRODUCTION: INVESTIGATION IN ONCHOCERCOMAS AND IN VITRO ... 111 ABSTRACT…………………………………………………………………………………..112 5.1 INTRODUCTION ............................................................................. 113 5.1.1 Type-17 immune response: an overview ................................... 113 5.1.2 Type-17 immune response and filariasis .................................. 125 5.1.3 Scope of the experimental study .............................................. 126 5.2 METHODS ..................................................................................... 127 5.2.1 Onchocercomas and cell pellets ............................................... 127 5.2.2 Neutrophils and PBMC isolation and cultures .......................... 127 5.2.3 HL60 and HEK cell cultures ..................................................... 128 5.2.4 Immunohistochemistry and cell imaging .................................. 128 5.2.5 Cell lysis .................................................................................. 132 IV 5.2.6 Protein precipitation ................................................................ 132 5.2.7 Analysis of IL-17A production by ELISA and Luminex assays ... 133 5.2.8 SDS-PAGE gel electrophoresis and Western Blot ...................... 133 5.2.9 RNA extraction and RT-PCR ..................................................... 135 5.2.10 Immunoprecipitation and mass spectrometry analysis ............. 137 5.2.11 Statistical analysis ................................................................... 139 5.3 RESULTS ....................................................................................... 140 5.3.1 Wolbachia is present in nodules from patients treated with placebo and absent in those from doxycycline ± IVM treated patients ............. 140 5.3.2 The inflammatory cellular infiltrate in onchocercomas depends upon the presence of Wolbachia ........................................................ 140 5.3.3 Wolbachia-dependent IL-17A+
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