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University of Florida Thesis Or Dissertation Formatting CELLULAR FUNCTIONS OF DNA GYRASE AND CONDITIONAL GENE REGULATION IN THE MALARIA PARASITE Plasmodium falciparum By TONYA DAVIDIAN BONILLA A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2008 1 © 2008 Tonya Davidian Bonilla 2 ACKNOWLEDGMENTS I sincerely thank my major advisor Dr. John Dame for providing me with the opportunity, resources, and support in which to conduct this work. I thank Dr. Dame for providing mentorship, thoughtful scientific discussions, and for his enthusiasm and dedication to malaria research. I also thank Dr. Dame for encouraging me to find independence as a researcher. I extend the deepest gratitude to my husband Dr. Fred Bonilla for his mentorship in the laboratory, and for working with me on numerous technical procedures. I thank Fred for his excellent insight, thoughtful scientific discussions, and moral support throughout the years. I gratefully thank my supervisory committee (Dr. David Allred, Dr. Anthony Barbet, Dr. Ken Cline, and Dr. Tom Rowe) for contributing their time and expertise in guiding my research, and for encouraging my growth as a scientist. I also thank Mr. Charles Yowell for providing technical assistance and laboratory support. 3 TABLE OF CONTENTS page ACKNOWLEDGMENTS ...............................................................................................................3 LIST OF TABLES...........................................................................................................................9 LIST OF FIGURES .......................................................................................................................10 ABSTRACT...................................................................................................................................13 CHAPTER 1 INTRODUCTION ..................................................................................................................15 Malaria Overview ...................................................................................................................15 Plasmodium Lifecycle ............................................................................................................16 The Apicoplast........................................................................................................................18 Origin of the Apicoplast ..................................................................................................18 The Apicoplast Genome ..................................................................................................19 Replication of the Apicoplast Genome............................................................................21 Protein Targeting to the Apicoplast.................................................................................21 Apicoplast Division.........................................................................................................22 Functions of the Apicoplast.............................................................................................25 Apicoplast as a Drug Target............................................................................................26 DNA Gyrase ...........................................................................................................................29 Functions of the Bacterial Type II Topoiomserase .........................................................29 The type II Topoisomerase Reaction...............................................................................30 Inhibitors of Type II Topoisomerase...............................................................................31 Characterization of the Plasmodium DNA Gyrase .........................................................33 Conditional Gene Regulation .................................................................................................34 Study Rational and Specific Objectives .................................................................................36 Hypothesis ..............................................................................................................................37 Specific Aims..........................................................................................................................37 2 MATERIALS AND METHODS ...........................................................................................39 Parasite Culture.......................................................................................................................39 Synchronization of Asexual Parasite Stages...........................................................................39 Sorbitol Method...............................................................................................................39 Percoll / Sorbitol Density Gradient Centrifugation.........................................................39 Magnetic Isolation...........................................................................................................40 Parasite Transfection ..............................................................................................................41 Direct Electroporation Method........................................................................................41 RBC-loading Method ......................................................................................................41 Drug Assays............................................................................................................................42 Parasitemia Counts ..........................................................................................................42 4 Parasite Growth Inhibition Measured by [3H]-hypoxanthine Incorporation...................43 Parasite Proliferation Rate by Flow Cytometry...............................................................43 Derivation of Plasmid Constructs...........................................................................................44 Southern Blot Analysis...........................................................................................................45 Northern Blot Analysis...........................................................................................................46 Western Blot Analysis ............................................................................................................46 Quantitative PCR and Quantitative Reverse-Transcriptase PCR ...........................................47 Fluorescent In Situ Hybridization (FISH) ..............................................................................48 Combined FISH / IFA ............................................................................................................49 FISH Probe Synthesis.............................................................................................................51 Production of DNA Gyrase Antibody ....................................................................................51 Immunoprecipitation of DNA.................................................................................................52 3 RESULTS ...............................................................................................................................61 Drug Studies ...........................................................................................................................61 Effect of DNA Gyrase Inhibitors on Parasite Proliferation.............................................61 Effects of Ciprofloxacin on Parasite Proliferation, Growth, and Viability .....................61 Organelle Genome Copy Number and DNA Loss with Drug Treatment ..............................62 Apicoplast and Mitochondrial Genome Copy Number...................................................62 Effects of Ciprofloxacin Treatment on Organellar DNA Replication.............................63 Effects of Ciprofloxacin on Organellar DNA Transcription...........................................64 Drug-induced Cleavage ..........................................................................................................65 Immunoprecipitation of DNA.................................................................................................66 Organellar DNA Segregation .................................................................................................67 Visualization of Apicoplast and Mitochondrial DNAs during Asexual Parasite Development................................................................................................................67 Effects of Ciprofloxacin Treatment on Organellar DNA Division .................................67 Visualization of the Apicoplast and Apicoplast DNA during Asexual Parasite Development................................................................................................................68 Effects of Ciprofloxacin on the Apicoplast and Apicoplast DNA ..................................69 Conditional Gene Regulation .................................................................................................69 Analysis of Parasites Transformed with pTGPI-GFP .....................................................69 Targeted Genomic Insertion of the Tet-Operator / Min Cam Promoter..........................71 Creation and Characterization of the TA Parasite Lines.................................................71 Creation and Characterization of the C3-TA Parasite
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