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Disease Models and Infectious Phenotypes of Mycobacterium Avium Subspecies Paratuberculosis

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Disease Models and Infectious Phenotypes of Mycobacterium Avium Subspecies Paratuberculosis AN ABSTRACT OF THE DISSERTATION OF Jamie L. Everman for the degree of Doctor of Philosophy in Microbiology presented on December 9, 2014. Title: Disease Models and Infectious Phenotypes of Mycobacterium avium subspecies paratuberculosis Abstract approved: ___________________________________________________ Luiz E. Bermudez Mycobacterium avium subspecies paratuberculosis (MAP) is the causative agent of Johne’s disease, a chronic inflammatory bowel disease that affects ruminant populations worldwide. The characteristic stages of the disease make diagnosis difficult, resulting in silent transmission among animals in a herd for years before proper detection of the infection. The extensive prevalence of Johne’s disease has driven a continuous effort to more readily understand the pathogenesis of the bacterium and to develop more effective preventative measures to curb the spread of the disease within herds. In this dissertation, we aim to create a more effective model for studying MAP infection within the intestinal mucosa, to utilize the milk-induced virulence phenotype to study how opsonization affects cell infection, and to study the metabolic interaction between MAP and the host phagocyte during infection. We describe a novel in vitro cell culture passage model which indicates that MAP changes during passage between bovine epithelial cells and macrophages, developing a more pro-inflammatory phenotype. We show that the inflammatory MAP phenotype not only increases gene expression of lipid metabolism- and modification-related genes, but that it is also composed of a set of lipids that are unique to the phenotype. Ultimately, we were able to identify these inflammatory- related transcripts in naturally MAP-infected bovine tissues, thus validating our model and indicating that the changing MAP phenotype may be a contributing factor in driving the development of inflammation within MAP infected animals. By using a different infectious phenotype that develops after MAP exposure to milk, a reservoir and transmission source of the bacterium, we demonstrate that opsonization of MAP results in more efficient translocation across an epithelial monolayer. Upon infection, we determine that macrophages more readily kill opsonized MAP in a rapid and specific manner. Furthermore, we begin to characterize one of the highest upregulated genes in this milk-induced phenotype, MAP1203, and its interaction with the intestinal epithelium. We establish that the putative cell wall associated protein is involved in both binding to and invasion of bovine MDBK epithelial cells when over-expressed in MAP during infection. Together, these data indicate the importance of the infectious phenotype developed after milk exposure and its role in the pathogenesis and transmission of Johne’s disease. Finally, we utilize Acanthamoeba castellanii (amoeba) as a phagocytic host and describe the influence that MAP infection has on the metabolic activity of the cell. We detail how MAP stimulates the metabolism of the amoeba and how that stimulation directly mirrors the pattern of survival and the intracellular burden of MAP over the course of infection. We identify bacterial mutants that result in excessive or deficient stimulation of the metabolic activity within host cell and by utilizing phenotype arrays, we illustrate that amoeba change the use of specific carbon sources based on the MAP strain used for infection. These data aid in beginning to understand the bacterial mechanisms that drive the metabolic interactions between MAP and the phagocytic host. Our results describe novel model systems for studying Johne’s disease and further our understanding about the host-pathogen interactions that occur within the intestinal mucosa of infected cattle. We show that the shifting phenotypes of MAP may be important contributing factors for detection, diagnosis, and in driving the progression of Johne’s disease. These findings offer new methods and the identification of new bacterial phenotype targets that could be used as the basis of developing more efficacious strategies in detecting and preventing Johne’s disease. ©Copyright by Jamie L. Everman December 9, 2014 All Rights Reserved Disease Models and Infectious Phenotypes of Mycobacterium avium subspecies paratuberculosis by Jamie L. Everman A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented December 9, 2014 Commencement June 2015 Doctor of Philosophy dissertation of Jamie L. Everman presented on December 9, 2014 APPROVED: Major Professor, representing Microbiology Chair of the Department of Microbiology Dean of the Graduate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my dissertation to any reader upon request. Jamie L. Everman, Author ACKNOWLEDGEMENTS I would first and foremost like to thank Dr. Luiz Bermudez for allowing me to conduct my doctoral research in his lab, for continuous discussion and exchange of ideas, and for the constant support he has offered throughout my time in the lab. His lessons, mentoring, contributions, and guidance have been invaluable in shaping me into becoming the research scientist I am today. I would also like to thank my committee members Dr. Dan Rockey, Dr. Martin Schuster, Dr. Manoj Pastey, Dr. Lia Danelishvili and Dr. Ricardo Letelier for their support and input to my projects. I would like to extend my sincerest thanks to all of the Bermudez lab members past and present. To the graduate students, technicians, and research staff, Lia Danelishvili, Lmar Babrak, Sasha Rose, Brendan Jeffrey, Rashmi Gupta, Jessica Chinison, Michael McNamara, and Laura Hauck, your suggestions, brainstorming, help, and laughs made working in the lab a wonderful experience. To all of the undergraduates and professional veterinary students I have worked with, Erin Flannery, Navid Ziaie, Eugenio Mannucci, Sadie Rice, and Lucy Garcia Flores, your contributions to all our projects have been immense and are greatly appreciated. To all of the students, faculty, and administrative staff in Dryden hall, thanks you for being my sounding board and for all the friendship throughout the years. A big thanks to the Department of Microbiology, especially Mary Fulton, and the Department of Biomedical Sciences, specifically Beth Chamblin, Denny Weber, and Jayne Theurer, for providing assistance with all the paperwork, travel, and official business, and for listening to and helping me with all my questions and concerns. Many thanks go to the Department of Veterinary Medicine for technical advice and guidance on bovine sample preparation, blood collection, milk collection, and general veterinary techniques. The following personnel were wonderfully forgiving with all my questions and early morning interruptions, and offered a friendly face and suggestions during various stages of my projects: Robert Murray (LARC), Dr. Helen Diggs and Dr. Jennifer Grossman (Laboratory Research Veterinarians), Teresa Sawyer (TEM), Darlene Joyner (LARC), Hayden Bush and Jeff Behm (OSU Dairy Center), and the Histology laboratory. To all the members of every softball, soccer, dodgeball, ultimate frisbee team, and gym class I have been a part of while in Corvallis, for all the fun memories and for the maintenance of my sanity, I give my sincerest thanks. Last but certainly not least, I would like to extend my love and immense gratitude towards my family. Mom and Dad, thanks for lending words of confidence during the tough days and for pretending to understand all my research when I got excited talking about it when it worked. Finally, to my wonderful boyfriend Brian, thank you so much for standing by me for all these years all the way from Colorado, it has been a long road but your encouragement and support has been invaluable. CONTRIBUTION OF AUTHORS Chapter 2: Jamie L. Everman conducted the experiments, contributed to experimental design, preparation of the manuscript, and data analysis. Dr. Luiz E. Bermudez contributed to the experimental design, data analysis, manuscript preparation, and funding of the project. Chapter 3: Jamie L. Everman conducted the experiments, contributed to experimental design, preparation of the manuscript, and data analysis. Dr. Torsten M. Eckstein performed and analyzed lipidomics and HPLC-ES/MS data. Dr. John Bannantine designed and produced the MAP K10 microarray slides and contributed to array protocols and experimental design. Jonathan Roussey and Dr. Paul Coussens contributed bovine tissue samples from their ongoing study at Michigan State University. Dr. Luiz E. Bermudez was involved in the experimental design, data analysis, manuscript composition, and funding of the project. Chapter 4: Jamie L. Everman conducted the experiments, contributed to experimental design, preparation of the manuscript, and data analysis. Erin F. Flannery conducted the screening of the MAP libraries and optimization of metabolic activity assays. Eugenio U. Mannucci contributed to the experimental design and optimization of phenotype arrays with amoeba. Dr. Luiz E. Bermudez contributed to the experimental design, data analysis, manuscript preparation, and funding of the project. Chapter 5: Jamie L. Everman conducted the experiments, contributed to experimental design, preparation of the manuscript, and data analysis. Lucero Garcia Flores conducted induction and purification assays of MAP1203 protein. Dr. Luiz E. Bermudez contributed
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