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REGULATION of the HELICOBACTER PYLORI Rpon REGULON by the FLAGELLAR

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REGULATION of the HELICOBACTER PYLORI Rpon REGULON by the FLAGELLAR REGULATION OF THE HELICOBACTER PYLORI RpoN REGULON BY THE FLAGELLAR PROTEIN EXPORT APPARATUS by TODD GARETH SMITH (Under the Direction of Timothy R. Hoover) ABSTRACT Helicobacter pylori is a significant human pathogen that infects a large percentage of the worldwide population with infections potentially resulting in acute gastritis, peptic ulcers, gastric carcinoma and non-Hodgkin lymphoma. Many essential H. pylori colonization factors have been identified including flagellar motility. Flagellar biosynthesis requires over 40 proteins and all three sigma factors (RpoD, RpoN and FliA) in the cell. Transcription of the H. pylori RpoN regulon is controlled by the FlgS/FlgR two-component regulatory system which responds to undefined cellular cues. Previous studies showed that expression of the RpoN- and FliA- dependent flagellar genes is linked to a functional flagellar protein export apparatus. FlhB, a membrane-bound component of the export apparatus, has a large cytoplasmic domain (FlhBC) which is processed by a site-specific autocleavage. FlhBC processing accompanies a switch in substrate specificity of the export apparatus. To determine if processing of FlhB influenced flagellar gene expression, two mutations at the cleavage site in FlhB were constructed. Both substitutions inhibited autocleavage of FlhB as well as motility. The mutants were able to export rod-/hook-type substrates but not filament-type substrates. The FlhB variant strains expressed RpoN- and FliA-dependent reporter genes at wild-type levels. Disruption of the hook length control protein FliK in the FlhB variant strains had different consequences for expression of the reporter genes suggesting that FliK has different effects on the export apparatus depending on the conformation of FlhB. Disruption of fliK in a ΔflhB mutant did not restore expression of RpoN- dependent reporter genes indicating that failure to export FliK does not account for inhibition of the RpoN regulon in export apparatus mutants. FlhA, another membrane-bound component of the export apparatus, also has a large cytoplasmic domain. Specific flhA insertion mutations stimulated expression of RpoN-dependent reporter genes. These flhA mutants were deficient in motility and export of both rod-/hook-type and filament-type substrates confirming that the export apparatus is not required for export of an inhibitor of the RpoN regulon. Taken together, these results support a model in which FlgS directly or indirectly senses the conformation of the export apparatus. INDEX WORDS: Helicobacter pylori, flagella, regulation, flagellar export apparatus, FlhB, FliK, FlhA, RpoN REGULATION OF THE HELICOBACTER PYLORI RpoN REGULON BY THE FLAGELLAR PROTEIN EXPORT APPARATUS by TODD GARETH SMITH B. S., The Ohio State University, 2004 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2009 © 2009 Todd Gareth Smith All Rights Reserved REGULATION OF THE HELICOBACTER PYLORI RpoN REGULON BY THE FLAGELLAR PROTEIN EXPORT APPARATUS by TODD GARETH SMITH Major Professor: Timothy R. Hoover Committee: Robert J. Maier Duncan C. Krause John J. Maurer Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia August 2009 DEDICATION This work is dedicated to all the teachers in my life from my first and greatest teachers Mom and Dad, to my elementary school teacher Betty Spradlin who let me “experiment” by making paper airplanes, to Scott Kegley who first opened my eyes to the microbial world, to my high school science teachers Rick Alwood and Randy McClay who taught me more than just basic chemistry and biology, to Rick Clark my high school soccer coach, to my pastors Dr. Harley Roston and Rev. Troy Diersing, to my undergraduate mentors Dr. Neil Baker, Dr. Stephanie Scott and Dr. Bob Tabita who gave me my first opportunities to “do” science, through my graduate advisor Dr. Tim Hoover who has led by example and shown abundant patience in teaching me how to think about science and life. Last but not least, this work is dedicated to my loving and supportive wife Sarah. iv ACKNOWLEDGEMENTS First and foremost I thank God for blessing me with the opportunities, means and perseverance to fulfill this work. I would like to thank all the people that are listed on the previous page and all the others that I can‟t list that have shaped my life and career. I thank my advisory committee Dr. Rob Maier, Dr. Duncan Krause and Dr. John Maurer as well as Dr. Anna Karls for their support and guidance. For financial support I acknowledge the American Society for Microbiology, the Department of Microbiology, the Graduate School, the Atlanta Chapter of the ARCS Foundation and finally the National Institutes of Health. I thank Dr. Wendy Dustman for her support through the first years of teaching. I would like to thank all the members of the Maier lab past and present that have tolerated my constant presence. I especially would like to thank Dr. Stephane Benoit for his help in troubleshooting problems and Dr. Praveen Alamuri for teaching me how to do my first XylE assay. I thank all of my classmates and friends from Athens for their understanding and support over the years. Finally, I acknowledge our colleague Dr. Bijal Patel who enjoyed every day but did not get to enjoy this day. v TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .............................................................................................................v CHAPTER 1 Introduction and Literature Review ..........................................................................1 Background and Significance ....................................................................................1 Colonization and Virulence Factors ..........................................................................3 Flagellar Gene Regulation and Flagellum Assembly in H. pylori ............................7 Research Summary ..................................................................................................12 References ...............................................................................................................16 2 Deciphering Bacterial Flagellar Gene Regulatory Networks in the Genomic Era ...........................................................................................................................27 Abstract ...................................................................................................................28 Introduction .............................................................................................................29 Master Regulators ....................................................................................................31 RpoN (54) Regulators ............................................................................................47 FliA (28) and FlgM ................................................................................................53 Conclusions .............................................................................................................58 Acknowledgements .................................................................................................58 References ...............................................................................................................59 vi 3 Helicobacter pylori FlhB Processing-deficient Variants Affect Flagellar Assembly but not Flagellar Gene Expression .......................................................................83 Summary .................................................................................................................84 Introduction .............................................................................................................85 Methods ...................................................................................................................89 Results .....................................................................................................................93 Discussion ...............................................................................................................99 Acknowledgements ...............................................................................................104 References .............................................................................................................105 4 Flagellar Protein Export Apparatus Function is not Required for Expression of 54-dependent Flagellar Genes in Helicobacter pylori ......................................117 Abstract .................................................................................................................117 Introduction ...........................................................................................................118 Results ...................................................................................................................121 Discussion .............................................................................................................127 Materials and Methods ..........................................................................................133 Acknowledgements ...............................................................................................136 References .............................................................................................................138 5 Direct Analysis of the Extracellular Proteome from Two Strains of Helicobacter pylori
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