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Prevotella Melaninogenica, an Oral Anaerobic Bacterium, Prevalent in Cystic Fibrosis Chronic Lung Infection

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Prevotella Melaninogenica, an Oral Anaerobic Bacterium, Prevalent in Cystic Fibrosis Chronic Lung Infection PREVOTELLA MELANINOGENICA, AN ORAL ANAEROBIC BACTERIUM, PREVALENT IN CYSTIC FIBROSIS CHRONIC LUNG INFECTION Sarah Elizabeth Council A dissertation submitted to the faculty of the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Curriculum in Oral Biology Chapel Hill 2013 Approved By: Matthew Wolfgang, Ph.D. Roland Arnold, Ph.D. Richard Boucher, M.D. Marcia Hobbs, Ph.D. Thomas H. Kawula, Ph.D. Anthony Richardson, Ph.D. ABSTRACT SARAH ELIZABETH COUNCIL: Prevotella melaninogenica, an oral anaerobic bacterium, prevalent in cystic fibrosis chronic lung infection. (Under the direction of Dr. Matthew Wolfgang) Prevotella melaninogenica, an anaerobic Gram-negative bacterium, is a member of the normal oral flora and is one of the most abundant anaerobic species found in respiratory specimens from individuals with cystic fibrosis (CF). Because of P. melaninogenica’s designation as a commensal, its role in CF disease pathogenesis and host immune response has been largely ignored. In our study of 61 CF patients at UNC hospitals, P. melaninogenica was cultured from 61% of adults and 57% of pediatric CF patients, and represented the most abundant strict anaerobe in both groups. Lung function did not correlate with the presence or abundance of P. melaninogenica but there was an increased antibody response against P. melaninogenica in both adult and pediatric CF patients compared to non-diseased controls. To explore innate host response, we characterized the structure and inflammatory effect of P. melaninogenica LPS. P. melaninogenica lipid A structure is heterogeneous, with the most prominent form being diphosphorylated and penta-acylated. In THP-1 cells, P. melaninogenica LPS induced significantly less IL-8 and IL-1β cytokine production than Pseudomonas aeruginosa LPS. We also showed that P. melaninogenica LPS could signal through a TLR4 independent pathway. These results show the presence of P. melaninogenica in CF patients and its recognition by the human host. ii From the tongue to the lung, P. melaninogenica must acquire nutrients to sustain life. The lung environment within chronically infected CF patients contains high levels of host iron proteins and pockets of anaerobic space. In vitro growth experiments demonstrated that heme or hemoglobin were sufficient iron sources for P. melaninogenica growth. To identify the first step of acquisition, we sequenced the P. melaninogenica genome and searched for homologues of known hemoglobin receptors. We identified a comprehensive list of putative P. melaninogenica hemoglobin receptors. Together these studies characterize the prevalence of P. melaninogenica in CF infection, evaluate P. melaninogenica’s impact on the host and determine nutritional requirements, which will lead to a better understanding about the role of P. melaninogenica in CF. Continued research into anaerobic pathogens, in particular P. melaninogenica, will lead to improvement in treatment interventions to reduce the severity of CF lung disease. iii ACKNOWLEDGEMENTS I first must thank my Mom and Dad who have always been behind me, pushing me towards my full potential. Thank you for letting me grow my own sugar crystals in the foyer, allowing me to tumble rocks in the basement and helping me with my science projects involving egg shells, coke and toothpaste. My family has been such an integral part of my journey. This includes many encouraging talks with Grandma and hanging out with my cousins Carrie and Kristan, who have become my sisters. For Grandpa and Mama, who passed away during this time, I will remember and cherish the time I spent with you. The daily grind of graduate school would have been too much without my roommates, Brittany and Jen, whose constant support and smiles after a bad day in lab were indispensable. I am blessed to have had so many supportive friends through the years from high school, college, NIH, church, and in my home away from home, lab. Ami, Gulshan, Marya and Emily have always had my back since high school. The same is true for Beth, Jon, Jes, Jared, Bhavna, Julie, Stephanie, Virginia, Chris, Brian, Amy, Emily, Josh, Marylois, John, Ted, Barbara and Hank in more recent years. I have to thank my lab mates Nan, Kim, Erin, Erich, Joe, Jeremiah and Cindy. Along with those whose lab I was only unofficially a part of even though I was a regular presence -- Phil, Donnie, Susan, Isabelle, Bill, Neelima, Debbie, Pete, Sharon, Jason and Cheryl. A special thank you to Dr. Flood, Cindy and students of the Oral Biology program who lovingly let me take part in the dynamic research community of the Dental school. I’d like to thank my committee Tom, Tony, Ric, Marcia and Dr. Arnold for their encouragement in the midst of a ‘broad characterization’ project. I especially would like iv to thank Marcia, who was and is supportive and always pushing me to do better. I have truly benefitted from her guidance and mentorship. And thank you to Matt for giving me a cool project, allowing me to combine my love of everything related to oral ecology and systemic disease. Finally, I’d like to recognize Joy, who gave my project life, literally!!! She has been an inspiration to me as I’ve watched her overcome the rigors of living with cystic fibrosis. She is someone who I can always turn to for a sarcastic joke. Now to him who is able to do far more abundantly than all that we ask or imagine, according to the power at work within us, to him be glory in the church and in Christ Jesus throughout all generations, forever and ever. Amen. Ephesians 3:20- 21. v Table of Contents List of Tables ................................................................................................................. viii List of Figures ..................................................................................................................ix List of Abbreviations ........................................................................................................xi Chapter 1 : Introduction ................................................................................................... 1 P. melaninogenica Classification and Epidemiology .................................................... 1 Host Immune Response .............................................................................................. 4 Nutritional Requirements of P. melaninogenica ......................................................... 11 CF Lung Infection ....................................................................................................... 16 References ................................................................................................................. 24 Chapter 2: Prevotella melaninogenica, an oral anaerobe, in chronic cystic fibrosis lung disease .......................................................... 40 Abstract ...................................................................................................................... 40 Introduction ................................................................................................................ 41 Material and Methods: ............................................................................................... 43 Results: ...................................................................................................................... 48 Discussion.................................................................................................................. 53 Figures ....................................................................................................................... 55 References ................................................................................................................. 68 Chapter 3: Structure and innate immune response to lipopolysaccharide lipid A of Prevotella melaninogenica ............................. 72 Abstract: ..................................................................................................................... 72 Introduction: ............................................................................................................... 73 Materials and Methods: .............................................................................................. 76 Results: ...................................................................................................................... 80 Discussion.................................................................................................................. 83 Figures: ...................................................................................................................... 87 References ................................................................................................................. 92 vi Chapter 4: Prevotella melaninogenica iron requirements and hemoglobin receptor characterization. ........................................................ 99 Abstract ...................................................................................................................... 99 Introduction: ............................................................................................................. 100 Materials and Methods: ............................................................................................ 103 Results: .................................................................................................................... 106 Discussion...............................................................................................................
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