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ROLE of TYPE IV SECRETION SYSTEMSIN TRAFFICKING of VIRULENCE DETERMINANTS of Burkholderia Cenocepacia

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ROLE of TYPE IV SECRETION SYSTEMSIN TRAFFICKING of VIRULENCE DETERMINANTS of Burkholderia Cenocepacia ROLE OF TYPE IV SECRETION SYSTEMS IN TRAFFICKING OF VIRULENCE DETERMINANTS OF Burkholderia cenocepacia A Dissertation by AMANDA SUZANNE ENGLEDOW Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY August 2006 Major Subject: Plant Pathology ROLE OF TYPE IV SECRETION SYSTEMS IN TRAFFICKING OF VIRULENCE DETERMINANTS OF Burkholderia cenocepacia A Dissertation by AMANDA SUZANNE ENGLEDOW Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Approved by: Chair of Committee, Carlos F. Gonzalez Committee Members, Dennis C. Gross Daniel J. Ebbole James E. Samuel Head of Department, Dennis C. Gross August 2006 Major Subject: Plant Pathology iii ABSTRACT Role of Type IV Secretion Systems in Trafficking of Virulence Determinants of Burkholderia cenocepacia. (August 2006) Amanda Suzanne Engledow, B.S., Texas A&M University Chair of Advisory Committee: Dr. Carlos F. Gonzalez Type IV secretion systems have been identified in several human pathogens including Bordetella pertussis, Helicobacter pylori, and Legionella pneumophila. These systems are responsible for the translocation of virulence proteins and/or DNA, thereby playing an important role in the pathogenesis of infection and plasticity of genomes. Burkholderia cenocepacia is an important opportunistic human pathogen, particularly in persons with cystic fibrosis (CF). Respiratory tract infection by B. cenocepacia in CF patients is often associated with a decline in respiratory function, and can result in acute systemic infection. Burkholderia cenocepacia strain K56-2 is part of the epidemic and clinically problematic ET12 lineage. Two type IV secretion systems have been identified in this strain; one system is plasmid encoded (designated the Ptw type IV secretion system) whereas the other is chromosomally encoded (designated the VirB/D type IV secretion system) and shows homology to the Agrobacterium tumefaciens VirB/D4 type IV secretion system. It was determined that the plasmid encoded Ptw system is a chimeric type IV secretion system composed of VirB/D4-like elements and F-specific subunits. More recently, it was found that this system translocates a protein effector (PtwE1) that is cytotoxic to plant cells. It was also determined that the positively iv charged C-terminal region of PtwE1 is important for translocation via the Ptw type IV secretion system. Strains of the epidemic B. cenocepacia PHDC lineage contain only a chromosomal VirB/D4-like type IV secretion system (designated BcVirB/D); and a putative effector protein associated with this system has been identified that has C- terminal transport signal and sequences different from the effectors of the Ptw type IV secretion system. It has also been shown that a competing plasmid substrate and a plasmid fertility inhibition factor act to render B. cenocepacia of the PHDC lineage incapable of expressing a plant phenotype. Thus, three type IV secretion systems have been identified in epidemic B. cenocepacia lineages. From two of these, an effector has been identified that has cytotoxic effects on eukaryotic cells, and at least one of these type IV secretion systems is able to translocate DNA substrates. v DEDICATION To my husband Jason, and my daughter Jayna, for the endless joy they bring to my life. vi ACKNOWLEDGEMENTS I would especially like to thank my committee chair, Dr. Carlos F. Gonzalez for the infinite guidance, wisdom, and support which he has kindly given me over the past five years. I thank him for always making time for me and providing an intellectually stimulating and friendly environment for research. In every sense, none of this work would have been possible without him. My thanks also goes to my committee members, Dr. Dennis C. Gross, Dr. Daniel J. Ebbole, and Dr. James E. Samuel, for their time, support, and insightful comments which they generously provided throughout the course of this research. I also extend my gratitude to Dr. John J. LiPuma’s Laboratory for performing the studies on human bronchial epithelial cell lines. I would also like to thank my friends and colleagues and the department faculty and staff for making my time at Texas A&M University a great experience. I would especially like to thank Bianca Batista, Fransisco Vielma, Michael Willett, Kathryn Cochrane, and Jacquelyn Vasquez for their excellent technical support. I want to extend my gratitude to the Cystic Fibrosis Foundation of America for providing funding for my research. Finally, I would like to thank my mother Nancy Dykes and father James Dykes for their encouragement and love, I would not be the woman I am today without them. I would also like to thank my good friend Sharon for her friendship and guidance over the past 14 years. I also give thanks to my husband’s mother Ann and her husband Thad for vii lending a hand and helping me when I needed it most, without ever asking for anything but love in return. My deepest thanks goes to my wonderful husband Jason Engledow whose understanding, patience, encouragement, and love have comforted me in hard times and made the good times infinitely more pleasurable. For all this, he is my everlasting love. And finally, I would like to thank my daughter Jayna for bringing me joy each and every day, for she is my greatest accomplishment. viii TABLE OF CONTENTS Page ABSTRACT.................................................................................................................... iii DEDICATION ................................................................................................................ v ACKNOWLEDGEMENTS ............................................................................................ vi TABLE OF CONTENTS................................................................................................ viii LIST OF FIGURES......................................................................................................... x LIST OF TABLES .......................................................................................................... xii CHAPTER I GENERAL INTRODUCTION........................................................................... 1 II INVOLVEMENT OF A PLASMID ENCODED TYPE IV SECRETION SYSTEM IN THE PLANT TISSUE WATERSOAKING PHENOTYPE OF Burkholderia cenocepacia AND THE STIMULATION OF IL-8 RELEASE FROM BRONCHIAL EPITHELIAL CELLS.................................. 6 Introduction ............................................................................................. 6 Experimental Procedures......................................................................... 10 Results ..................................................................................................... 26 Discussion ............................................................................................... 44 III IDENTIFICATION OF AN EFFECTOR TRANSLOCATED BY THE Burkholderia cenocepacia PTW TYPE IV SECRETION SYSTEM ................. 53 Introduction ............................................................................................. 53 Experimental Procedures......................................................................... 55 Results ..................................................................................................... 73 Discussion ............................................................................................... 84 ix CHAPTER Page IV IDENTIFICATION AND CHARACTERIZATION OF A GROUP IVA TYPE IV SECRETION SYSTEM AND EFFECTOR IN Burkholderia cenocepacia OF THE PHDC LINEAGE ............................................................ 88 Introduction ............................................................................................. 87 Experimental Procedures......................................................................... 90 Results ..................................................................................................... 105 Discussion ............................................................................................... 122 V CONCLUSION ................................................................................................... 129 REFERENCES................................................................................................................ 132 APPENDIX A ................................................................................................................. 159 APPENDIX B ................................................................................................................. 162 APPENDIX C ................................................................................................................. 165 APPENDIX D ................................................................................................................. 168 APPENDIX E.................................................................................................................. 173 APPENDIX F.................................................................................................................. 175 APPENDIX G ................................................................................................................. 177 APPENDIX H ................................................................................................................. 179 APPENDIX I..................................................................................................................
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