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(Mdma) Mediated Hyperthermia in Rats

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(Mdma) Mediated Hyperthermia in Rats THE ROLE OF GUT MICROBIOME IN 3,4 METHYLENE DIOXYMETHAMPHETAMINE (MDMA) MEDIATED HYPERTHERMIA IN RATS Sayantan Roy Choudhury A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE August 2018 Committee: Vipaporn Phuntumart, Advisor Raymond Anthony Larsen, Co-Advisor Jon Eric Sprague © 2018 Sayantan Roy Choudhury All Rights Reserved iii ABSTRACT Vipaporn Phuntumart, Advisor The gut microbiome is known to be home to 105 to 106 micro-organisms which are known to be phylogenetically diverse. There is growing evidence that the composition of the gut microbiota plays a large role in the health and well-being of its host. Changes gut microbial populations are associated with the pathogenesis of variety of metabolic, malignant, and inflammatory diseases. Evidence suggests the existence of a ‘gut-brain axis’ as the involving interactions between gut microbiome and the central nervous system (CNS). Little is known about the involvement of this axis in modulating gut microbial populations in response to drugs of abuse. The present study investigates the effect of 3,4 methylene dioxymethamphetamine (MDMA) on the gut microbiome of male Sprague-Dawley rats. Treatment with MDMA resulted in a rapid compositional shift of the cultivatable bacterial population in the rat cecum. Specifically, the cecal contents of normal MDMA-treated rats yielded a large number of swarming bacteria when cultured on nutrient agar at dilutions suitable for colony counting, whereas organisms with a swarming phenotype were not present at levels detectible in similarly diluted cecal contents from animals that did not receive MDMA. When plated on media containing bile salts, swarming was inhibited, allowing recovery of pure isolates. These isolates were found to be gram-negative rods and non-lactose fermenting rods. Bioinformatic analysis using the 16S rRNA gene from these isolates confirmed then to be members of the genus Proteus. iv Dedicated to my parents, Mr. Sanjoy Roy Choudhury and Mrs. Binota Roy Choudhury and my beloved sister Ms. Sudreesa Roy Choudhury, and to all my teachers and mentors who continue to be the strongest pillars of support and the biggest inspirations in my academic and personal life. v ACKNOWLEDGMENTS Throughout my journey as a Master’s student I have enjoyed learning new things and rediscover a novel way of perceiving the world of Biology. This would not have been without the constant help and support from very valuable people with whom I got the opportunity to work with. Therefore, I want to express my sincere thanks to my advisor, Dr. Vipaporn Phuntumart for continuously encouraging and motivating me throughout this study. Her constant support has helped me learn the basic aspects of scientific research. I also owe my gratitude to my co-advisor, Dr. Raymond Anthony Larsen without whom executing this project would have been impossible. While working with him I had learnt novel ways of envisioning science and research. I also extend my gratitude to Dr. Jon Eric Sprague, Director, Center for the Future of Forensic Sciences for immensely supporting me throughout the study. I am also indebted to Dr. Carol Heckman and Dr. Michael Eric Geusz for their constant encouragement. I also convey my note of thanks to Dr. Jeffrey Gibson Miner and the Department of Biological Sciences, Bowling Green State University for giving me the opportunity to be a part of this journey. I would like to thank my wonderful lab members, Gayathri Beligala, Satyaki Ghosh, Sudhan Pachchain, Kevin Rowlands, Seth Bischoff, Renee Dollard and Joe Toguchi for being with me and helping me in the lab. I am also indebted to all the Forensic Lab Members, especially Emily Ann Ridge and Paul Lungu for helping me collect samples for the study. Since the day I landed into the United States I got the opportunity to be in touch with some very special friends. Therefore, I am grateful to all my friends especially Wanzhou Liu, Akshay Gupta, Greg Gustafson, Mike Balinski and Madhurima Bhattacharyya for their incredible moral support. I also extend my thanks to my friend, Pallav Routh for helping me with the statistical analysis. vi I always fall short of words to express my gratitude for my beloved parents and my family for their unconditional support and love. I would be immensely guilty if I do not recognize the sacrifices they go through for my goodwill. I feel blessed to have a family which always encourages me to live up to my dreams and achievements. Lastly, I thank my elder brother, Dr. Surajit Bose for helping me perceive the world of Biological Sciences in a different way. I am grateful to my childhood friend, Souradip Ghosh for being by my side. I also thank the United States India Educational Foundation (USIEF), Kolkata for making me believe that dreams do come true. vii TABLE OF CONTENTS Page CHAPTER 1. INTRODUCTION & BACKGROUND………………………………….. 1 1.1 The gut microbiota and its significance…………………………………… 1 1.2 Diversity of microbiomes in the gut microenvironment………………… . 2 1.3 The Gut Microbiome: A silent partner in disease manifestations…………… 5 1.4 Exploring the relationship of 3,4 methylene dioxy methamphetamine (MDMA) with hyperthermia……………………………………………….. 7 1.5 MDMA induced hyperthermia and gut microbiota: Is there an existing crosstalk?............................................................................................ 14 1.6 Establishing a link between MDMA and gut swarmers……………………… 17 CHAPTER 2. AIMS AND OBJECTIVES………………………………………………... 19 CHAPTER 3. MATERIALS AND METHODS…………………………………………... 20 3.1 Examination of the effects of MDMA on gut microbiome……………………. 20 3.1.1 Animals………………………………………………………………….. 20 3.1.2 Drugs and chemicals……………………………………………………. 20 3.1.3 Study design……………………………………………………………… 20 3.1.4 Isolation of antibiotic resistant bacteria from cecal contents…………….. 21 3.1.5 Isolation of non-antibiotic resistant bacteria associated with MDMA treatment…………………………………………………….. 21 3.1.6 Assay of swarmer bacteria……………………………………………….. 22 3.2 Identification of the swarming bacteria………………………………………… 22 3.2.1 Colony PCR………………………………………………………………. 22 3.2.2 DNA sequencing and analysis…………………………………………… 23 viii CHAPTER 4. RESULTS………………………………………………………………….. 24 4.1 Agar plate assay for assessing kanamycin resistant bacteria……………………. 24 4.2 Isolation of bacterial swarmer species………………………………………….. 26 4.2.1 Isolation of swarmer colonies from cecal contents……………………….. 26 4.2.2 Analysis of bacterial species in fecal and cecal contents of MDMA treated rats…………………………………………………..... 27 4.2.3 Swarmer assay of bacterial colonies………………………………………. 28 4.2.4 Gram staining of isolated swarmer species………………………………. 29 4.3 Biochemical identification of swarmer species………………………………….. 29 4.3.1 Isolation of swarmer colonies on MacConkey agar………………………. 29 4.3.2 Hektoen-Enteric agar assay………………………………………………. 30 4.4 Molecular Identification of swarmer species……………………………………… 32 CHAPTER 5. DISCUSSION…………………………………………………………….... 34 REFERENCES…………………………………………………………………………….. 38 ix LIST OF FIGURES Figure Page 1 The chemical structure of the drug 3,4-methylene-dioxymethamphetamine (MDMA)………………………………… 7 2 The mechanism of adrenergic-mediated hyperthermia……………………………... 10 3 The role of fatty acids in regulating UCP mediated thermogenesis………………… 13 4 An explanation of how gut microbial populations regulate the process of mitochondrial energy expenditure……………………………………………...... 15 5 An illustration of the binding site of the Eubacteria 16S rRNA primers……………. 23 6 A bar plot illustrating the percentage ratio of kanamycin resistant to kanamycin sensitive bacterial colonies…………………………………………… 25 7 Diluted cecal contents of MDMA+H2O treated animals displayed growth of swarmer colonies on LB agar media………………………………………………… 26 8 Analysis of fecal and cecal contents of MDMA treated rats……………………….... 27 9 Swarming assay of bacterial isolates………………………………………………… 28 10 Gram staining of swarmers…………………………………………………………... 29 11 Growth of swarmer colonies on MacConkey agar…………………………………... 30 12 Hektoen-Enteric (HE) agar assay of swarmer species……………………………….. 31 13 Agarose Gel Electrophoresis of 16S rRNA Amplicons……………………………… 32 14 Phylogenetic Analysis of between the 16S rRNA sequences of isolated swarmer species……………………………………………………………… 33 1 CHAPTER 1. INTRODUCTION & BACKGROUND 1.1 The gut microbiota and its significance The symbiotic relationship between microbes and their corresponding mammalian hosts are well documented. The microbial diversity does not only comprise of different kinds of bacteria, but also various viruses and eukaryotic microbes (Jandhalya et al., 2015; Shreiner et al., 2015). A vast majority of these organisms have been found to exist in the gastrointestinal tract (GIT) (Gill et al., 2006). The human enteric environment is estimated to be home to approximately 10-100 trillion microorganisms including various eubacteria, archaea, fungi and viruses which act as symbionts (Bäckhed et al., 2005). Over the last decade, researchers have studied the gut microbiome in detail. The development of the Human Microbiome Project by the National Institutes of Health (NIH) in 2007 has helped scientists enormously in unravelling the fundamentals of the gut microbiome (Turnbaugh et al., 2008). Additionally, the project had also aided microbiologists to study how microbes populate the gut environment. Moeller et al. (2016) examined the co-evolution of humans and gut commensals. They used primates as a model organism to demonstrate
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