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Dynamic Host-Pathogen Interactions Result in Fungal Epitope Unmasking Alex Hopke University of Maine, Alex [email protected]

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Dynamic Host-Pathogen Interactions Result in Fungal Epitope Unmasking Alex Hopke University of Maine, Alex Hopke@Umit.Maine.Edu The University of Maine DigitalCommons@UMaine Electronic Theses and Dissertations Fogler Library Summer 8-19-2016 Dynamic Host-Pathogen Interactions Result in Fungal Epitope Unmasking Alex Hopke University of Maine, [email protected] Follow this and additional works at: http://digitalcommons.library.umaine.edu/etd Part of the Bacterial Infections and Mycoses Commons, Fungi Commons, Immunity Commons, Immunology of Infectious Disease Commons, Infectious Disease Commons, Medical Microbiology Commons, Molecular Biology Commons, Other Immunology and Infectious Disease Commons, and the Pathogenic Microbiology Commons Recommended Citation Hopke, Alex, "Dynamic Host-Pathogen Interactions Result in Fungal Epitope Unmasking" (2016). Electronic Theses and Dissertations. 2478. http://digitalcommons.library.umaine.edu/etd/2478 This Open-Access Dissertation is brought to you for free and open access by DigitalCommons@UMaine. It has been accepted for inclusion in Electronic Theses and Dissertations by an authorized administrator of DigitalCommons@UMaine. DYNAMIC HOST-PATHOGEN INTERACTIONS RESULT IN FUNGAL EPITOPE UNMASKING By Alex Hopke B.S. University of Maine, 2010 A DISSERTATION Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy (in Microbiology) The Graduate School The University of Maine August 2016 Advisory Committee: Robert Wheeler, Associate Professor of Microbiology, Advisor Julie Gosse, Associate Professor of Biochemistry Carol Kim, Professor of Microbiology, Vice President of Research, Dean of Graduate School John Singer, Professor of Microbiology Derry Roopenian, Professor, The Jackson Laboratory Dissertation Acceptance Statement On behalf of the Graduate Committee for Alex Hopke I affirm that this manuscript is the final and accepted dissertation. Signatures of all committee members are on file with the Graduate School at the University of Maine, 42 Stodder Hall, Orono, Maine. ______________________________________________________________________________ Dr. Robert Wheeler, Associate Professor of Microbiology 12/15/2015 ii LIBRARY RIGHTS STATEMENT In presenting this dissertation in partial fulfillment of the requirements for an advanced degree at The University of Maine, I agree that the Library shall make it freely available for inspection. I further agree that permission for “fair use” copying of this dissertation for scholarly purposes may be granted by the Librarian. It is understood that any copying or publication of this dissertation for financial gain shall not be allowed without my written permission. Signature: Date: DYNAMIC HOST-PATHOGEN INTERACTIONS RESULT IN FUNGAL EPITOPE UNMASKING By Alex Hopke Dissertation Advisor: Dr. Robert Wheeler An Abstract of the Dissertation Presented in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy (in Microbiology) August 2016 Molecular camouflage is used by a diverse set of pathogens to disguise their identity and avoid recognition by protective host receptors. The opportunistic fungal pathogen Candida albicans is a good example, as it masks the inflammatory component β-glucan in its cell wall to evade detection by the immune receptor Dectin-1. Interestingly, it has been seen that β-glucan becomes unmasked during infection in vivo, though the underlying mechanisms remained unclear. Exposure levels of this epitope may be important, as Dectin-1 mediates protection from some strains of C. albicans and alterations in the organization and composition of the Candida cell wall can influence host responses. This research sought to understand C. albicans cell wall dynamics, particularly within the context of host-pathogen interactions. Special attention was paid to elucidating mechanisms of β-glucan unmasking and we have revealed a novel and dynamic interaction in which neutrophils damage the fungal cell wall via a mechanism involving neutrophil extracellular traps. This damage provoked the disruption of fungal cell wall architecture including increased chitin deposition and β-glucan unmasking at sites of immune attack. Surprisingly, these cell wall changes were also dependent on an active fungal response, which required cell wall integrity signaling and involved relocalization of cell wall remodeling components. Importantly, neutrophil mediated β-glucan unmasking could result in enhanced immune responses to fungi from macrophages, suggesting that this epitope unmasking could have functional consequences during infection. Work we participated in helped elucidate mechanisms involved in baseline fungal epitope masking in the form of Cho1 and phosphatidylserine biosynthesis and also demonstrated that changes to cell wall composition and architecture influence the importance of β-glucan exposure to host responses to C. albicans. Overall, this work helps elucidate the importance of host-pathogen interactions in influencing fungal cell wall dynamics during disseminated candidiasis. Given the importance of the cell wall as a drug target, understanding how this fungus maintains integrity and epitope masking during attack may identify therapeutic targets to aid the treatment of candidiasis. This work also highlights an important concept, which is that microbial cell walls can change dynamically during infection with important consequences for host recognition and immunity. ACKNOWLEGDEMENTS The amount of people I owe thanks to are numerous. First and foremost, I owe a great debt to my family who have supported my interest in the sciences from a young age and whose continued support has been instrumental in allowing me to pursue this degree. Thank you! Secondly, I want to thank my advisor Dr. Robert Wheeler. His mentorship has helped me grow immeasurably as both a scientist and a person during my time as a graduate student. I would like to thank Nadine Nicke, whose assistance made complicated experiments easier to handle and whose friendship continues to brighten my days. I would also like to thank Allison Scherer, who helped remind me to live a little outside of the lab and has made the ending years of my degree some of the most enjoyable I’ve ever had. I would like to thank Judith Berman, Megan Lenardon, James B. Konopka and Janet Quinn for strains, Gordon Brown for the sDectin-1-Fc construct, Christine Pham for the DPPI KO mice and Erica Hidu and Rebekah Stetson for their contributions to this project. I gratefully acknowledge the expert pathology assistance of James E. Wheeler, MD. I would also like to thank Brenda Kennedy-Wade for general mouse care and Dawna Beane for her assistance with processing organs for histological analysis. iii TABLE OF CONTENTS ACKNOWLEDGEMENTS...................................................................................................................iii LIST OF TABLES..............................................................................................................................viii LIST OF FIGURES..............................................................................................................................ix Chapter 1. REVIEW OF THE LITERATURE 1.1 Host-Pathogen Interactions: Shaping the Outcome of Infection...........................1 1.2 Host Recognition of Infection................................................................................2 1.3 Fungal Infections....................................................................................................3 1.4 Candida albicans....................................................................................................5 1.5 Host Recognition of C. albicans Infection..............................................................7 1.5.1 Toll-like Receptors....................................................................................8 1.5.2 C-Type Lectin Receptors...........................................................................8 1.5.2.1 Dectin-1..............................................................................................9 1.5.2.2 Dectin-2 and Dectin-3.......................................................................10 1.5.2.3 Mincle and Mannose Receptor........................................................10 1.5.2.4 DC-SIGN ...........................................................................................11 1.5.3 NOD-like Receptors ................................................................................11 1.5.4 RIG-I like Receptors ................................................................................12 iv 1.6 Host Defense against C. albicans Infection..........................................................12 1.6.1 Neutrophils.............................................................................................13 1.6.1.1 Neutrophil Antimicrobial Mechanisms.............................................13 1.6.2 Mononuclear Phagocytes.......................................................................14 1.6.3 The Inflammasome.................................................................................16 1.6.4 Natural Killer Cells...................................................................................16 1.6.5 Adaptive Immunity.................................................................................17 1.7 Pathogen Epitope Masking..................................................................................18 1.7.1 Parasite Epitope Masking........................................................................18 1.7.2 Bacterial Epitope Masking......................................................................20
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