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Investigation of Ammonia Transport Pathways in the Anal Papillae of Larval Aedes Aegypti Mosquito

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Investigation of Ammonia Transport Pathways in the Anal Papillae of Larval Aedes Aegypti Mosquito INVESTIGATION OF AMMONIA TRANSPORT PATHWAYS IN THE ANAL PAPILLAE OF LARVAL AEDES AEGYPTI MOSQUITO Razvan Adrian Ionescu A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE GRADUATE PROGRAM IN BIOLOGY YORK UNIVERSITY TORONTO, ONTARIO October, 2014 © Razvan Adrian Ionescu, 2014 ABSTRACT The elimination of nitrogenous waste products is a ubiquitous problem for animals. The anal papillae of Aedes aegypti larvae, are important sites of ammonia/ammonium excretion. They + express three putative ammonia (NH3/NH4 ) transporters, Rhesus protein 50-1 and -2 (AeRh-1, - 2) and AeAmt. Here, we pharmacologically characterize ammonia transport mechanisms in the anal papillae of larval A. aegypti and investigate the regulation of putative ammonia transporters in response to high environmental ammonia (HEA) treatment. Ammonium concentration gradients were measured adjacent to the anal papillae using scanning ion-selective electrode technique (SIET) and used to calculate ammonia fluxes by the anal papillae. Results suggest that the ionomotive pumps V-type H+ ATPase (VA) and Na+/K+ ATPase (NKA) as well as cation / H+ exchanger, isoform 3 (NHE3) participate in ammonia excretion at the anal papillae. VA is involved in ammonia trapping at the exterior unstirred layer of the anal papillae, while basal NKA + and apical NHE3 facilitate the transport of NH4 . Quantitative RT-PCR analysis revealed lower abundance of AeRh-2 in the anal papillae relative to the expression of AeRh-1; however Amt expression was approximately 12 fold higher than AeRh-1 (Note*: expression refers to relative mRNA abundance). In addition, the expression of AeRh-1/2 were lower but Amt expression was significantly higher in the presence of HEA, compared to controls. It is probable that ammonia transport by the anal papillae of A. aegypti larvae is achieved by multiple mechanisms, involving the cooperative efforts of various facilitative and active transporters. In addition carbonic anhydrase participates in ammonia excretion, via its normal role in acid/base balance, by supplying protons to the VA, which can be pumped out and used in ammonia trapping. ii AKNOWLEDGEMENTS First and foremost I would like to thank my supervisor and friend Dr. Andrew Donini. Thank you for giving me my first exposure to the world of insect studies and my first opportunity to do research in your friendly and welcoming lab. You have provided me with every opportunity to help me grow as a student, a scientist and a person. I could not have asked for a better mentor. Thank you for always having your door open to me, regardless of the situation, and always being supportive, straight forward, genuinely kind and patient. For your guidance, professionally and personally, I thank you. To the past and present Donini lab members, I would like to thank you for making my time here as a graduate student and for that matter an undergraduate student an interesting and fun ride. I would especially like to thank Sima Jonusaite for your help and encouragement, insightful conversations, and things we have in common, like the love of the sun, travel and a good argument; Phuong Bui for your relentless drive, work ethic, mentoring and great taste in music; Hina Akhter for your positive attitude, friendly smile and endless supply of headache meds; Jesmila Marusalin for your inspiration, late night conversations and for always keeping the lab warm and toasty; Melika Zadeh-Tahmasebi for your sense of humour, brilliant smile and great friendship. Thank you all, L’Aedes. I would like to extend a special thank you to fellow graduate students, post-docs and faculty members who have generously offered their time, advice, expertise and equipment, including Dr. Scott Kelly, Dennis Kolosov, Sean McKee and Chun Chin Chen. To Dr. Helen Chasiotis and Dr. Lisa Robertson, your kind words, willingness to teach and genuine care will be engrained in my mind forever. I consider you esteemed colleagues and lifelong friends. Finally, I would like to thank the most important people in my life, my family. To my wife, Sari and kids, Daniel, Bianca, Julian and Alexis, without your constant support, encouragement, patience and love, it would have been a virtual impossibility to complete this work. Your sacrifices, have not been un-noticed and will never be forgotten. Thank you! iii TABLE OF CONTENTS Abstract ........................................................................................................................................... ii Aknowledgements.......................................................................................................................... iii Table of contents ............................................................................................................................ iv List of tables ................................................................................................................................... vi List of Figures ............................................................................................................................... vii Abbreviations ............................................................................................................................... viii 1. Introduction ................................................................................................................................. 1 1.1 Effects of Ammonia Toxicity ............................................................................................... 1 1.2 Putative Ammonia Transporters ........................................................................................... 3 1.2.1 Methylammonium/ammonium permeases (MEPs) ....................................................... 3 1.2.2 Ammonium Transporters (Amts) ................................................................................... 5 1.2.2.1 AmtB Structure of E. coli ........................................................................................... 6 1.2.3 Mammalian Rhesus Proteins and Rhesus glycoproteins ............................................... 8 1.3 Formation of Ammonia in Insects ...................................................................................... 15 1.4 Nitrogenous Waste Processing Symbiosis in Insects.......................................................... 17 1.5 Ammonia Excretion in Insects ............................................................................................ 19 1.5.1 Nitrogenous Waste Excretion Strategies and Putative Ammonia Transporters in Insects .......................................................................................................................... 21 1.6 Rh-glycoproteins and Ammonia Excretion in Aquatic Animals ........................................ 30 1.7 The Model Organism: Aedes aegypti .................................................................................. 33 1.8 Aedes aegypti Larvae .......................................................................................................... 34 1.9 Objectives ........................................................................................................................... 36 2. Materials and Methods .............................................................................................................. 37 2.1 Insects ................................................................................................................................. 37 2.2 RNA Extraction and cDNA Synthesis ................................................................................ 37 2.2.1 PCR Primer Design ...................................................................................................... 38 2.2.2 Quantitative Real-time PCR Analysis ......................................................................... 39 2.3 Construction of Ion-selective Microelectrodes ................................................................... 40 2.3.1 Scanning Ion-selective Electrode Technique (SIET) ................................................... 41 2.3.2 Measurements of Voltage Gradients ............................................................................ 41 2.3.3 Calculation of Ion Fluxes ............................................................................................. 43 2.4 Characterization of Ammonium Transport Mechanisms across Anal Papillae Epithelium 44 iv 2.5 Statistical Analysis .............................................................................................................. 44 3. Results ....................................................................................................................................... 45 3.1 Expression of Rh-glycoproteins and Amt in gastrointestinal system of A. aegypti larvae . 45 + 3.2 Effect of Pharmacological Inhibitors on NH4 flux Adjacent the Anal Papillae ................ 45 3.2.1 Effect of BaCl2 on Anal Papillae Ion Transport .......................................................... 46 + + 3.2.2 Effects of pH-dependence on K and NH4 Fluxes ..................................................... 47 + + 3.2.3 Effects of Methazolamide and K Load on NH4 Excretion ....................................... 47 4. Discussion ................................................................................................................................. 54 4.1 Working Model of Ammonia Transport Mechanisms in Larval A. aegypti Papillae ......... 59 4.2 Final Remarks and Future Direction
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