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University of Florida Thesis Or Dissertation Formatting MOSQUITOCIDAL ACTIVITY AND MODE OF ACTION OF THE ISOXAZOLINE FLURALANER By SHIYAO JIANG A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2016 © 2016 Shiyao Jiang To my Mom ACKNOWLEDGMENTS I would first like to thank my family for their understanding and encouragement during my first two years of life in UF. To my advisor Dr. Jeffery Bloomquist and lab manager Dr. Judy Mollet, thank you for the support toward my research and efforts to run this wonderful lab. I would also like to thank my committee members, Dr. Phillip Kaufman and Dr. Ulrich Bernier, for your kind guidance throughout this early stage of my career. To former and present Bloomquist’s lab members (Aaron Gross, Fan Tong, Baonan Sun, Jennina Taylor-Wells, Rafique Islam, Sheena Francis, Maia Tsikolia, Nurhayat Tabanca, Yuxin Li, Minyuan Tie, and Natasha Agramonte), thanks for your help and precious friendship. Special thanks to Maia, for your efforts in preparing chemicals including fluralaner; and to Aaron, for all your kind assistance using the Socratic Method to build up my critical thinking skills. This research was funded by Deployed War Fighter Research Program under USDA Specific Cooperative Agreements 58-0208-0-068 and 58-0208-5-001. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 7 LIST OF FIGURES .......................................................................................................... 8 LIST OF OBJECTS ......................................................................................................... 9 ABSTRACT ................................................................................................................... 10 CHAPTER 1 LITERATURE REVIEW .......................................................................................... 12 1.1 Mosquitoes as Vectors and Their Control ......................................................... 12 1.2 Mosquitocide Resistance .................................................................................. 13 1.3 GABA Receptors in Mammals and Insects ....................................................... 15 1.4 Insecticides Targeting GABA Receptors ........................................................... 18 1.5 Second Generation Non-competitive GABA Antagonists .................................. 20 1.6 Overall Objective............................................................................................... 22 2 TOXICITY AND GABA RECEPTOR-DIRECTED ACTIONS OF FLURALANER .... 25 2.1 Introduction ....................................................................................................... 25 2.2 Materials and Methods ...................................................................................... 26 2.2.1 Chemicals ................................................................................................ 26 2.2.2 Insects ..................................................................................................... 26 2.2.3 Larval Mosquito Bioassays ...................................................................... 27 2.2.4 Adult Mosquito Bioassays ....................................................................... 28 2.2.5 Adult D. melanogaster Bioassays ............................................................ 32 2.2.6 Electrophysiological Recording on D. melanogaster Larval CNS ............ 32 2.2.7 Test of GABAergic Compounds on Mammalian GABAA Receptors ........ 34 2.2.8 Statistical Analysis ................................................................................... 36 2.3 Results .............................................................................................................. 36 2.3.1 Larval Mosquito Bioassays ...................................................................... 36 2.3.2 Adult Mosquito Bioassays ....................................................................... 37 2.3.3 Adult D. melanogaster Bioassays ............................................................ 42 2.3.4 CNS Recordings on D. melanogaster...................................................... 43 2.3.5 Test on Mammalian GABA Receptors ..................................................... 50 2.4 Discussion ........................................................................................................ 50 3 CONCLUSION AND FUTURE PERSPECTIVES ................................................... 58 3.1 Conclusion ........................................................................................................ 58 5 3.2 Future Perspectives .......................................................................................... 59 REFERENCES .............................................................................................................. 61 BIOGRAPHICAL SKETCH ............................................................................................ 69 6 LIST OF TABLES Table page 2-1 Larval bioassays of fluralaner on fourth-instar Ae. aegypti and An. gambiae larvae. ................................................................................................................. 37 2-2 Topical bioassays of fluralaner on Ae. aegypti and An. gambiae adult females. .............................................................................................................. 39 2-3 Injection, glass contact, and feeding bioassays of fluralaner and fipronil on Ae. aegypti adult females. .................................................................................. 40 2-4 Comparison of fluralaner toxicity on Ae. aegypti adult females with paper or glass as contact exposure routes. ...................................................................... 41 2-5 Comparison of the effect of PBO, DEF, and DEM in feeding assays of fluralaner against Ae. aegypti adult females. ...................................................... 41 2-6 Comparison of the effect of PBO, DEF, and DEM in topical assays of fluralaner against Ae. aegypti adult females. ...................................................... 42 2-7 Glass contact and feeding bioassays of fluralaner against susceptible and resistant adult D. melanogaster strains. ............................................................. 43 7 LIST OF FIGURES Figure page 1-1 Diagrammatic representation of the structure of a GABAA receptor ................... 18 1-2 Chemical structures of chloride channel agonists and antagonists referred to in the text ............................................................................................................ 23 1-3 Chemical structures of isoxazolines and meta-diamides referred to in the text .. 24 2-1 WHO paper assay tubes .................................................................................... 31 2-2 D. melanogaster larval CNS photos taken from a dissecting scope ................... 32 2-3 D. melanogaster larval CNS recordings demonstrating statistical analysis ........ 34 2-4 Mortality data for adult topical assay showing the increase of toxicity over time ..................................................................................................................... 38 2-5 DMSO effects on D. melanogaster larval CNS ................................................... 44 2-6 Electrophysiological recordings on intact or severed CS-OR D. melanogaster larval CNS .......................................................................................................... 45 2-7 Electrophysiological recordings on CS-OR or rdl-1675 D. melanogaster intact larval CNS .......................................................................................................... 47 2-8 Time to 50% blocking of baseline firing rate after treatment in D. melanogaster larval CNS recording .................................................................... 47 2-9 Effects of GABA on Drosophila larval CNS preparations ................................... 48 2-10 Electrophysiological recordings on severed D. melanogaster larval CNS, with GABA inhibition .................................................................................................. 49 2-11 Concentration response curve of fluralaner on resistant and susceptible strains of D. melanogaster, in larval CNS recordings ......................................... 50 8 LIST OF OBJECTS Object page 2-1 Intoxication symptoms of fluralaner on fourth-instar Ae. aegypti larvae .............. 57 2-2 Fourth-instar Ae. aegypti larvae treated with 0.5% ethanol ................................ 57 2-3 Intoxication symptoms of fluralaner on Ae. aegypti adults in topical assay ........ 57 2-4 Ae. aegypti adults treated with ethanol in topical assay ..................................... 57 9 Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science MOSQUITOCIDAL ACTIVITY AND MODE OF ACTION OF THE ISOXAZOLINE FLURALANER By Shiyao Jiang August 2016 Chair: Jeffrey R. Bloomquist Major: Entomology and Nematology Mosquitoes, such as Aedes aegypti and Anopheles gambiae, are important vectors of human diseases. Fluralaner, a recently introduced parasiticide, was evaluated as a mosquitocide in this study. On Ae. aegypti and An. gambiae fourth- instar
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