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Innate Immune Response to Coxiella Burnetii University of Pennsylvania ScholarlyCommons Publicly Accessible Penn Dissertations 2015 Innate Immune Response to Coxiella Burnetii William Paul Bradley University of Pennsylvania, [email protected] Follow this and additional works at: https://repository.upenn.edu/edissertations Part of the Allergy and Immunology Commons, Immunology and Infectious Disease Commons, Medical Immunology Commons, and the Microbiology Commons Recommended Citation Bradley, William Paul, "Innate Immune Response to Coxiella Burnetii" (2015). Publicly Accessible Penn Dissertations. 1620. https://repository.upenn.edu/edissertations/1620 This paper is posted at ScholarlyCommons. https://repository.upenn.edu/edissertations/1620 For more information, please contact [email protected]. Innate Immune Response to Coxiella Burnetii Abstract Intracellular bacteria pose a unique set of challenges for the immune system. Many have evolved highly specialized virulence factors to evade intracellular detection and created a replicative niche. Coxiella burnetii is a zoonotic intracellular pathogen capable of causing severe acute and chronic Q fever in humans. C. burnetii grows in the lysosome and persists in cells for more than 10 days. Since C. burnetii can replicate inside cells for a prolonged period, we hypothesized that C. burnetii evolved multiple mechanisms to subvert innate immune detection. To test this hypothesis, we tested the ability of the C. burnetii Nine Mile Phase II clone 4/RSA439 strain to activate innate immune responses in restrictive C57BL/6 bone marrow-derived macrophages, specifically: detection by surface and cytosolic immune sensors; activation of the inflammasome; and production of Type I interferon. We found C. burnetii does not robustly stimulate cytosolic sensors, activate the inflammasome, nor induce obustr levels of Type I interferon. These pathways do not play a significant oler in mediating cell-intrinsic control of bacterial replication. We found TLR detection, specifically TLR2 and TLR4, primarily mediates innate immune detection and restriction of C. burnetii in C57BL/6 macrophages. We further implicated both TLR adaptors MYD88 and TRIF in this response. Building upon these findings, we demonstrated soluble TNF induced by TLR signaling plays a major role in the cell-intrinsic restriction of C. burnetii. We further examined TNF-dependent mechanisms of restriction: cell death, reactive nitrogen (RNS) and reactive oxygen (ROS) species, and guanylate binding proteins (GBPs). We found cell death is not induced in macrophages. Although expression of GBPs are induced upon C. burnetii infection, we ruled out five GBPs as mediators of bacterial restriction. Finally, we found RNS is induced by C. burnetii in a TNF-dependent manner, and ROS is also induced and plays a role in the cell-intrinsic control of C. burnetii replication. Together, these studies demonstrate that the C. burnetii Nine Mile phase II strain is able to evade many arms of the innate immune system in C57BL/6 macrophages and implicated a specific molecule, TNF, in mediating the cell-intrinsic control of this poorly understood bacterium. Degree Type Dissertation Degree Name Doctor of Philosophy (PhD) Graduate Group Cell & Molecular Biology First Advisor Sunn Shin Second Advisor Christopher A. Hunter Keywords Coxiella burnetii, Innate Immunity, TLRs, TNF Subject Categories Allergy and Immunology | Immunology and Infectious Disease | Medical Immunology | Microbiology This dissertation is available at ScholarlyCommons: https://repository.upenn.edu/edissertations/1620 INNATE IMMUNE RESPONSE TO COXIELLA BURNETII William P. Bradley A DISSERTATION in Cell and Molecular Biology Presented to the Faculties of the University of Pennsylvania in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy 2015 Supervisor of Dissertation _____________________ Sunny Shin Assistant Professor of Microbiology Graduate Group Chairperson ______________________ Daniel Kessler Professor of Pathology and Laboratory Medicine Dissertation Committee: Christopher Hunter, Ph.D., Professor of Pathobiology, Chair Sara Cherry, Ph.D., Associate Professor of Microbiology Rahul M. Kohli, M.D., Ph.D., Assistant Professor of Medicine Igor E. Brodsky, Ph.D., Assistant Professor of Pathobiology INNATE IMMUNE RESPONSE TO COXIELLA BURNETII COPYRIGHT 2015 William P. Bradley ABSTRACT THE INNATE IMMUNE RESPONSE TO COXIELLA BURNETII William P. Bradley Sunny Shin Intracellular bacteria pose a unique set of challenges for the immune system. Many have evolved highly specialized virulence factors to evade intracellular detection and created a replicative niche. Coxiella burnetii is a zoonotic intracellular pathogen capable of causing severe acute and chronic Q fever in humans. C. burnetii grows in the lysosome and persists in cells for more than 10 days. Since C. burnetii can replicate inside cells for a prolonged period, we hypothesized that C. burnetii evolved multiple mechanisms to subvert innate immune detection. To test this hypothesis, we tested the ability of the C. burnetii Nine Mile Phase II clone 4/RSA439 strain to activate innate immune responses in restrictive C57BL/6 bone marrow-derived macrophages, specifically: detection by surface and cytosolic immune sensors; activation of the inflammasome; and production of Type I interferon. We found C. burnetii does not robustly stimulate cytosolic sensors, activate the inflammasome, nor induce robust levels of Type I interferon. These pathways do not play a significant role in mediating cell-intrinsic control of bacterial replication. We found TLR detection, specifically TLR2 and TLR4, primarily mediates innate immune detection and restriction of C. burnetii in C57BL/6 macrophages. We further implicated both TLR adaptors MYD88 and TRIF in this response. Building upon these findings, we demonstrated soluble TNF induced by TLR signaling plays a major role in the cell-intrinsic restriction of C. burnetii. We further examined TNF-dependent iii mechanisms of restriction: cell death, reactive nitrogen (RNS) and reactive oxygen (ROS) species, and guanylate binding proteins (GBPs). We found cell death is not induced in macrophages. Although expression of GBPs are induced upon C. burnetii infection, we ruled out five GBPs as mediators of bacterial restriction. Finally, we found RNS is induced by C. burnetii in a TNF-dependent manner, and ROS is also induced and plays a role in the cell-intrinsic control of C. burnetii replication. Together, these studies demonstrate that the C. burnetii Nine Mile phase II strain is able to evade many arms of the innate immune system in C57BL/6 macrophages and implicated a specific molecule, TNF, in mediating the cell-intrinsic control of this poorly understood bacterium. iv TABLE OF CONTENTS CONTENT PAGE Copyright Notice..……………………………….…………………………………………….....ii Abstract…………………………………………………………………………………………...iii Table of Contents………………………….……………………………………………………..v List of Figures……..………………………………………………………………….………….vi CHAPTER 1: INTRODUCTION….……………..…………………………………….………..1 CHAPTER 2: Innate immune recognition and restriction of C. burnetii in C57BL/6 bone marrow derived macrophages……………….………………………………………………..29 Abstract………………………………………………………………………………………….30 Introduction……………………………………………………………………………………...30 Methods.……………………………………….………………………………………………..35 Results………………………………………….………………………………...……………..42 Discussion…………………………………………………………….………………………...53 CHAPTER 3: TNF mediated restriction of Coxiella burnet………………….……………..73 Abstract………………………………………………………………………………………….74 Introduction……………………………………………………………………………………...75 Methods.……………………………………….………………………………………………..80 Results………………………………………….………………………………...……………..84 Discussion…………………………………………………………….………………………...89 CHAPTER 4: DISCUSSION……….…………………………………………….………..…102 BIBLIOGRAPHY………………………………………………………………………………120 v LIST OF FIGURES FIGURE 1.1. The intracellular lifestyle of C. burnetii……………………………………….28 FIGURE 2.1. TLR2 and TLR4 mediate immune responses to Coxiella burnetii in mouse macrophages …………….……………………………………………………………..………59 FIGURE 2.2. Myd88 and Trif are required for cytokine production and the restriction of intracellular growth …………………………………………………………………….………61 FIGURE 2.3. C. burnetii LPS does not induce TNF production ………………...………...63 FIGURE 2.4. C. burnetii’s T4SS is capable of injecting effectors into C57BL/6 BMDM..64 FIGURE 2.5. C. burnetii T4SS expression does not lead to enhanced cytokine production or early p38 MAPK phosphorylation ……………………………..……………..66 FIGURE 2.6. Coxiella burnetii infection does not induce detectable inflammasome activation……………………………………………………………………………...…………68 FIGURE 2.7. Coxiella burnetii infection does not induce robust type I interferon production and intracellular replication is not restricted by type I IFNs…………...………70 FIGURE 2.8. Levels of internalized WT Coxiella burnetii are similar for different genotypes of bone marrow-derived macrophages at 24 hours post-infection……...……72 FIGURE 3.1. Endogenous TNF restricts intracellular growth of C. burnetii.………………………………………………………………………………….……….95 FIGURE 3.2. C. burnetii does not induce apoptosis in B6 macrophages ……………………………………………………………………………………………………97 vi - FIGURE 3.3. C. burnetii infection does induce iNOS mRNA and NO2 in a TNF- dependent manner ………………………………………………………………...…………..98 FIGURE 3.4. C. burnetii infection does induce whole cell ROS and ROS plays a role in restricting intracellular growth in B6 BMDMs………….…………………………………….99 FIGURE 3.5. C. burnetii infection induces mGBP-1 and mGBP-2,
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