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Receptors for the Detection of L-Amino Acids and IMP by Mouse Taste Sensory Cells Shreoshi Pal Choudhuri University of Vermont

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Receptors for the Detection of L-Amino Acids and IMP by Mouse Taste Sensory Cells Shreoshi Pal Choudhuri University of Vermont University of Vermont ScholarWorks @ UVM Graduate College Dissertations and Theses Dissertations and Theses 2016 Receptors for the detection of L-amino acids and IMP by mouse taste sensory cells Shreoshi Pal Choudhuri University of Vermont Follow this and additional works at: https://scholarworks.uvm.edu/graddis Part of the Biology Commons, and the Neuroscience and Neurobiology Commons Recommended Citation Pal Choudhuri, Shreoshi, "Receptors for the detection of L-amino acids and IMP by mouse taste sensory cells" (2016). Graduate College Dissertations and Theses. 473. https://scholarworks.uvm.edu/graddis/473 This Dissertation is brought to you for free and open access by the Dissertations and Theses at ScholarWorks @ UVM. It has been accepted for inclusion in Graduate College Dissertations and Theses by an authorized administrator of ScholarWorks @ UVM. For more information, please contact [email protected]. RECEPTORS FOR THE DETECTION OF L-AMINO ACIDS AND IMP BY MOUSE TASTE SENSORY CELLS A Dissertation Presented by Shreoshi Pal Choudhuri to The Faculty of the Graduate College of The University of Vermont In Partial Fulfillment of the Requirements For the Degree of Doctorate of Philosophy Specializing in Biology January, 2016 Defense Date: November 2, 2015 Dissertation Examination Committee: Eugene R. Delay, Ph.D., Advisor Gary M. Mawe, Ph.D., Chairperson Rona J. Delay, Ph.D. George C. Wellman, PhD. Cynthia J. Forehand, Ph.D., Dean of the Graduate College ABSTRACT The sense of taste is one of the most important factors in regulating ingestive decisions. This is central to a number of disease conditions including but not limited to obesity, diabetes, anorexia, hypertension, coronary artery diseases and malnutrition. The detection of the molecules eliciting taste qualities in food is mediated by the coordinated actions of distinct types of taste sensory cells (TSCs) housed in taste buds within specialized papillae throughout the oral cavity. Taste receptors in the taste sensory cells that detect food molecules are the key players in selecting dietary nutrients. One such example is L-amino acids, a critical part of one’s diet. L-glutamate is the prototypical umami compound and is known to increase palatability of food. A unique characteristic of umami taste is the response potentiation of glutamate by 5’ ribonucleotide monophosphates, such as inosine 5’ monophosphate (IMP), which is also capable of eliciting an umami taste. Candidate receptors for umami taste include a heterodimer T1r1+T1r3, brain variants of mGluR1 and mGluR4, and the truncated variants of mGluR1 and mGluR4. Studies using heterogeneous expression of T1r1+T1r3 suggest it is an umami and a broadly tuned L-amino acid receptor. While much attention is devoted to understanding glutamate transduction, the detection mechanisms for other L-amino acids by TSCs are less well understood. Here calcium imaging of isolated TSCs and taste cell clusters from the circumvallate and foliate papillae of C57BL/6J and T1r3 knockout mice was performed to determine if other receptors are involved in the detection of L-amino acids and IMP. Ratiometric imaging with Fura-2 was used to study calcium responses to IMP and four L-amino acids (monopotassium L- glutamate, L-serine, L-arginine, and L-glutamine) with and without IMP. The results of these experiments showed that the response patterns elicited by L-amino acids varied significantly across TSCs. Only a small subset of cells responded to all stimuli. Interestingly, L-amino acids other than glutamate elicited synergistic responses in a subset of TSCs. Additionally IMP alone elicited a response in a large number of TSCs. Our data indicate that synergistic and non- synergistic responses to L-amino acids and IMP are mediated by multiple receptors or possibly a receptor complex. Next the roles of mGluR1 and mGluR4 in the detection of the IMP and L-amino acids were investigated. Selective agonists for mGluR1, (RS)-3, 5-dihydroxyphenylglycine (DHPG; a group I mGluR agonist), and mGluR4, L-(+)-2-amino-4-phosphonobutyric acid (L-AP4; a group III mGluR4 agonist) elicited responses in TSCs. In addition, TSCs responsive to these agonists were also responsive to L-amino acids and IMP. More importantly, selective antagonists against different mGluRs such as (RS)-1-aminoindan-1,5-dicarboxylic acid (AIDA; a group I mGluR antagonist), and (RS)-α-methylserine-O-phosphate (MSOP; a group III mGluR antagonist) significantly suppressed L-amino acid- and IMP-mediated responses in TSCs of T1r3 knockout mice. Collectively, these data provide evidence for the involvement of taste and the brain variants of mGluR1 and mGluR4 in L-amino acid and IMP taste responses in mice, and support the hypothesis that multiple receptors contribute to the IMP and L-amino acid tastes. CITATIONS Material from this dissertation has been published in the following form: Pal Choudhuri, S., Delay, R. J., & Delay, E. R.. (2015). L-Amino Acids Elicit Diverse Response Patterns in Taste Sensory Cells: A Role for Multiple Receptors. PLoS One, 10(6), e0130088. doi: 10.1371/journal.pone.0130088 Material from this dissertation has been accepted for publication in Neuroscience on 12/4/2015 in the following form: Pal Choudhuri, S., Delay, R. J., & Delay, E. R.. (2015). Metabotropic Glutamate Receptors Are Involved In The Detection Of IMP And L-Amino Acids By Mouse Taste Sensory Cells. Neuroscience. ii DEDICATION This is dedicated to my mother Ushasi Pal Choudhuri and my father Subrata Pal Choudhuri iii ACKNOWLEDGEMENTS I would like to thank all the people who made possible to develop this project. First of all, I am very grateful to my advisor, Dr. Eugene R. Delay (more popularly known as Dr. D), who had been indispensable during my development as a scientist. I would like to thank Dr. D and my co-advisor Dr. Rona J. Delay for their patience, assistance, supervision, guidance, and encouragement to develop and finish this project. They taught me that patience, persistence and diligence is the key. I am thankful to my committee members, Dr. Gary M. Mawe and Dr. George C. Wellman, who have patiently guided me through a challenging project over the past several years. I also want to thank all the professors in the Biology, especially Dr. Judith Van Houten and Dr. Bryan Ballif who were always available to help with their advice whenever I needed. I also want to thank our lab technician Diane Morgan for her help with lab work and for the fun times we spent together. I have a number of friends and colleagues I have made that supported me and made this journey enjoyable. Thank you Dr. Nabanita Mukherjee, Dr. Jonathan Vick, Dr. Suraj Cherian, and Dave Harris for we are, or have been, fortunate to have one another as friends and learning partners. I also want to thank Nora Awadallah, Brenden Chandler, and Kyle Joseph, for their friendship and support and for all the fun chats that we had. I am also very thankful to my mother, Ushasi Pal Choudhuri, for always being the most supportive person, for always giving me encouragement to follow the dreams, and for teaching me to never give up. And thanks Dad (Subrata Pal Choudhuri) for always being there to support, and for the courage you infused in me. I also want to thank iv my sweet brother Sayanta Pal Chowdhury for believing in me and always supporting me (No questions asked). I also want to thank my husband Paresh Panchal for giving me the push when I needed them most. Thank you for listening to my endless complaints about experimental failures and giving me the strength to keep going. Last but not the least, I want to thank my extended Vermont family, all my friends, for giving me the family away from home. v TABLE OF CONTENTS CITATIONS ....................................................................................................................... ii DEDICATION ................................................................................................................... iii ACKNOWLEDGEMENTS ............................................................................................... iv LIST OF TABLES ............................................................................................................. ix LIST OF FIGURES ............................................................................................................ x Chapter 1 : TASTE TRANSDUCTION – A COMPREHENSIVE LITERATURE REVIEW ............................................................................................................................. 1 1.1 Taste ....................................................................................................................................... 1 1.1.1 Sense of Taste: ................................................................................................................ 1 1.1.2 Taste and Physiological Functions: ................................................................................. 5 1.1.3 Taste Confusion: ............................................................................................................. 5 1.2 Taste System .......................................................................................................................... 7 1.2.1 The Structure of the Primary Sensory Organ, Tongue: ................................................... 7 1.2.2. Taste Bud Cells: ............................................................................................................ 10 1.3 Transduction Mechanisms of Taste Molecules by the TSCs ...............................................
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