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Characterization of the Immunoregulatory Roles of IFN-Β in T Cells and Dendritic Cells

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Characterization of the Immunoregulatory Roles of IFN-Β in T Cells and Dendritic Cells Characterization of the immunoregulatory roles of IFN-β in T cells and dendritic cells by Leesa Pennell A thesis submitted in conformity with the requirements for the degree Doctor of Philosophy Graduate Department of Immunology University of Toronto © Copyright by Leesa Pennell 2017 Characterization of the immunoregulatory roles of IFN-β in T cells and dendritic cells Leesa Pennell Doctor of Philosophy Department of Immunology University of Toronto 2017 Abstract Multiple sclerosis (MS) is an autoimmune disease that targets the central nervous system (CNS). Interferon (IFN)-β was the first approved therapy for relapsing-remitting MS more than 20 years ago, however, its mechanism of action remains ill-defined. Using a myelin oligodendrocyte glycoprotein (MOG)-induced murine experimental autoimmune encephalomyelitis (EAE) model for MS, our earlier studies identified that IFN-β-/- mice exhibit an earlier onset and a more rapid progression of disease compared to IFN-β+/+ mice. CD4+ T cells, specifically of the Th17 lineage, are posited to be pathogenic in MS and in EAE, and CD11c+ dendritic cells (DCs) are critical antigen-presenting cells that have the potential to regulate pathogenic T cells in MS and EAE. Accordingly, we investigated the immunoregulatory effects of IFN-β on CD4+ T cells and DCs. Our studies revealed that CD4+ T cells isolated from IFN-β-/- mice are primed to polarize to the Th17 lineage, associated with expression of Th17-associated cytokine receptors. Stimulation with a cocktail of Th17-inducing cytokines led to increased expression of Th17- associated genes in IFN-β-/- Th17 cells compared to IFN-β+/+ Th17 cells, suggestive of a regulatory role for IFN-β in determining the Th17 cell transcriptome. Consistent with these findings, we observed a greater proportion of Th17 cells in the LNs of IFN-β-/- mice compared with IFN-β+/+ mice during EAE, with increased numbers of CD4+ T cells in the CNS of IFN-β-/- mice, regardless of stage of disease. We identified that IFN-β exerts immunoregulatory effects on DCs, associated with determining cytokine production and expression of co-stimulatory activation markers. IFN-β-/- DCs drive increased proliferation of MOG-transgenic CD4+ T cells, ii and produce more IL-6 and IL-23, critical for induction of Th17 cells. Finally, we provide evidence that IFN-β regulates the migration of DCs into the CNS during EAE, by modulating STAT1-dependent CCR7 expression. Taken together, our data indicate immunoregulatory roles for IFN-β in suppression of Th17 cells and in limiting the activation and trafficking of DCs during EAE. iii Acknowledgements First and foremost, I would like to thank my supervisor, Dr. Eleanor Fish, for taking me under your wing when I first came to Toronto and giving me the opportunity to work in your lab. I have learned so much from you, Eleanor. You have taught me how to design thoughtful experiments, how to communicate my work with others, and how to be a successful female scientist. You have been a source of inspiration and a role model that I will always look up to. Thank you so, so much. To my committee members, Dr. Michele Anderson and Dr. Shannon Dunn. Thank you for all of the support and guidance you have given me throughout my PhD. Whether our discussions happened during my committee meetings or at departmental seminars or events, I valued each and every one and came away with new ideas that helped to shape my work. To the members of the Fish Lab, past and present (Beata, Carole, Daniel, Erin, Olivia, Ben and Darrin). Thank you for putting up with my slightly OCD tendencies when it came to my lab markers and labelling of everything I possibly could. Our lunchtime discussions and coffee breaks saved my sanity during long days of experiments. Beata, you make the lab run. Thank you for all your help and support in the lab and otherwise. Carole, thank you for starting up the project that I took over. Our scientific discussions and your valuable input over the years were so important to me. Thank you, also, for teaching me not to be afraid of multi-colour flow cytometry. To my parents and my family. Thank you for your understanding and support when I said I would ‘still be in school a bit longer’ for so many years. I know it wasn’t easy to understand but I appreciate your love and patience throughout this process. To my husband, Tomas. You are a source of inspiration every day. You have encouraged me, supported me, and urged me to follow my dreams. I can’t wait for the rest of our future together and only hope I can be just as supportive for you as you have been for me. To all of the members of the Department of Immunology and friends I’ve made over the years. Your support and friendship helped motivate me through the tough times and you were always there to celebrate success. All of the scientific and non-scientific discussions we had certainly made for an unforgettable journey. I will always rememeber the IGSA events and meetings, pub nights, intramural activites, and all the times we spent together. My time here would not have been the same without these experiences and for that, I am so grateful. iv List of Publications Pennell LM, Fish EN. 2017. Interferon-β regulates dendritic cell activation and migration in experimental autoimmune encephalomyelitis. (Manuscript under review). Pennell LM, Fish EN. 2014. Immunoregulatory effects of interferon-β in suppression of Th17 cells. J Interferon Cytokine Res. 34(5):330–41 Pennell, LM., Galligan, CL. and Fish, EN. 2012. Sex Affects Immunity. J Autoimmun. 38(2-3): J282-91 Galligan CL, Pennell LM, Murooka TT, Baig E, Majchrzak-Kita B, et al. 2010. Interferon-beta is a key regulator of proinflammatory events in experimental autoimmune encephalomyelitis. Mult Scler. 16(12):1458–73 v Table of Contents Abstract ............................................................................................................................... ii-iii Acknowledgements ........................................................................................................................ iv List of Publications .......................................................................................................................... v Table of Contents ..................................................................................................................... vi-vii List of Tables ................................................................................................................................ viii List of Figures ................................................................................................................................ ix List of Abbreviations ................................................................................................................. x-xii Chapter 1: Introduction ........................................................................................................... 1-47 1.1 Interferons ......................................................................................................................... 2 1.1.1 Classification of IFNs ............................................................................................................... 2 1.1.1.1 Type I IFNs ........................................................................................................................ 3 1.1.1.2 Type II and III IFNs ........................................................................................................... 4 1.1.2 Type I IFN induction and signaling .......................................................................................... 4 1.1.3 Regulation of type I IFN responses .......................................................................................... 7 1.2 CD4+ T helper cells ........................................................................................................... 7 1.2.1 CD4+ T helper subsets .............................................................................................................. 8 1.2.1.1 Th1 cells ........................................................................................................................... 10 1.2.1.2 Th2 cells ........................................................................................................................... 10 1.2.1.3 Th17 cells ......................................................................................................................... 11 1.2.1.4 Regulatory T cells ............................................................................................................ 12 1.2.2 Activation of T cells, TCR signaling & T cell migration ....................................................... 13 1.2.2.1 Activation of T cells and TCR signaling .......................................................................... 14 1.2.2.2 Migration of T cells .......................................................................................................... 16 1.2.3 IFN effects on T cells ............................................................................................................. 20 1.3 Dendritic cells .................................................................................................................. 21 1.3.1 Types of DCs .......................................................................................................................... 22 1.3.1.1 cDCs ................................................................................................................................
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