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Identification of Protective Immune Responses and the Immunomodulatory Capacity of Litomosoides Sigmodontis

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Identification of Protective Immune Responses and the Immunomodulatory Capacity of Litomosoides Sigmodontis Identification of protective immune responses and the immunomodulatory capacity of Litomosoides sigmodontis Dissertation zur Erlangung des Doktorgrades (Dr. rer. nat.) der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn vorgelegt von JESUTHAS AJENDRA aus Dillingen/Saar Bonn 2016 i Angefertigt mit Genehmigung der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn 1. Gutachter: Prof. Dr. Achim Hörauf 2. Gutachter: Prof. Dr. Waldemar Kolanus Tag der Promotion: 25.08.2016 ii Erscheinungsjahr: 2016 Erklärung Die hier vorgelegte Dissertation habe ich eigenständig und ohne unerlaubte Hilfsmittel angefertigt. Die Dissertation wurde in der vorgelegten oder in ähnlicher Form noch bei keiner anderen Institution eingereicht. Es wurden keine vorherigen oder erfolglosen Promotionsversuche unternommen. Bonn, 23.03.2016 Teile dieser Arbeit wurden vorab veröffentlicht in folgenden Publikationen: “ST2 deficiency does not impair type 2 immune responses during chronic filarial infection but leads to an increased microfilaremia due to an impaired splenic microfilarial clearance.” Ajendra J, Specht S, Neumann AL, Gondorf F, Schmidt D, Gentil K, Hoffmann WH, Taylor MJ, Hoerauf A, Hübner MP. PLoS One. 2014 Mar 24;9(3):e93072. doi: 10.1371/journal.pone.0093072. eCollection 2014. “Development of patent Litomosoides sigmodontis infections in semi-susceptible C57BL/6 mice in the absence of adaptive immune responses.” Layland LE, Ajendra J, Ritter M, Wiszniewsky A, Hoerauf A, Hübner MP. Parasit Vectors. 2015 Jul 25;8:396. doi: 10.1186/s13071-015-1011-2. “Combination of worm antigen and proinsulin prevents type 1 diabetes in NOD mice after the onset of insulitis.” Ajendra J, Berbudi A, Hoerauf A, Hübner MP. Clin Immunol. 2016 Feb 16; 164:119- 122. doi: 10.1016/j.clim.2016.02.005 Des Weiteren wurden Auszüge auf verschiedenen Konferenzen als Vortrag oder Poster präsentiert. iii Table of Contents Summary ..................................................................................................................................... 1 Zusammenfassung ...................................................................................................................... 2 1. Introduction ............................................................................................................................ 4 1.1 Nematodes as parasites of humans ....................................................................................... 4 1.2 Filarial nematodes and filariasis - neglected diseases of the tropics .................................... 6 1.3 Litomosoides sigmodontis – a murine model for LF ............................................................ 9 1.4 Life cycle of Litomosoides sigmodontis ............................................................................. 10 1.5 Wolbachia – Endosymbiont and drug target ...................................................................... 12 1.6 Immune mechanisms against helminth infections .............................................................. 14 1.7 Nod-like-receptors .............................................................................................................. 20 1.8 The NOD2 receptor ............................................................................................................ 21 1.9 The NOD2 receptor in the context of parasite infections ................................................... 24 1.10 Immunmodulatory ability of helminths ............................................................................ 25 1.11 Type 1 Diabetes and helminth infections ......................................................................... 26 1.12 Objectives of this thesis .................................................................................................... 28 2. Materials & Methods ............................................................................................................ 30 2.1 Mice…… ............................................................................................................................ 30 2.2 Life cycle of L. sigmodontis ............................................................................................... 30 2.3. Infection with L. sigmodontis ............................................................................................ 31 2.4 Euthanasia of mice .............................................................................................................. 32 2.5. Determination of worm load .............................................................................................. 32 2.6. Determination of microfilarial load ................................................................................... 32 2.7 Plasma isolation .................................................................................................................. 33 2.8. Isolation of thoracic cavity cells ........................................................................................ 33 2.9. Isolation of lymphocytes from the pancreas ...................................................................... 33 2.10 Isolation of cells from pancreatic lymph nodes ................................................................ 34 2.11 Preparation of cells from the thoracic cavity .................................................................... 34 2.12 Spleen cell isolation .......................................................................................................... 34 2.13 Determination of cell number ........................................................................................... 35 2.14 Enzyme-linked immunosorbent assay (ELISA) ............................................................... 35 2.15 Fluorescence activated cell sorting (FACS) ..................................................................... 36 iv 2.16 Histology .......................................................................................................................... 37 2.17 Neutrophil depletion ......................................................................................................... 38 2.18 Macrophage depletion ...................................................................................................... 38 2.19 IL-5 depletion ................................................................................................................... 38 2.20 In vitro analyses of neutrophils ........................................................................................ 38 2.21 Gene expression analysis .................................................................................................. 39 2.22 Reporter assays ................................................................................................................. 39 2.23 Statistics ............................................................................................................................ 40 3. Results .................................................................................................................................. 41 3.1. Type 1 Diabetes ................................................................................................................. 41 3.1.1 Combination therapy prevents T1D in 10 week old NOD mice ..................................... 41 3.1.2 Combination therapy does not prevent T1D in 12-week old NOD mice ........................ 42 3.1.3 Less infiltration of autoreactive T cells in pancreata of 10-week old NOD mice after combination therapy ................................................................................................................. 43 3.1.4 Splenic T cell frequencies do not differ between CT-treated NOD mice and PBS controls ..................................................................................................................................... 44 3.1.5. Increased frequency of CD4+ T cells in pancreata of CT treated mice ......................... 46 3.1.6. Combination therapy leads to a significant increase in regulatory T cell frequencies in the pancreatic lymph nodes ...................................................................................................... 48 3.2. The role of the NOD2-receptor during L. sigmodontis infection ...................................... 52 3.2.1 NOD2 receptor is activated by Wolbachia-containing worm extract .............................. 52 3.2.2 NOD2-/- mice are more susceptible to L. sigmodontis infection than WT controls ......... 53 3.2.3 No differences in the composition of major cell types and cytokine concentrations in the pleural cavity of infected NOD2-/- compared to WT controls during early time points of infection .................................................................................................................................... 54 3.2.4 Macrophage depletion does not reverse the phenotype of infected NOD2-/- mice .......... 57 3.2.5. IL-5 depletion does not reverse the phenotype of NOD2-/- mice ................................... 58 3.2.6. No impaired production of IgM in NOD2-/- mice during early L. sigmodontis infection .................................................................................................................................................. 59 3.2.7 NOD2-/- do not have an increased worm burden after subcutaneous injection of L3 larvae .......................................................................................................................................
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