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The Role of the Intestinal Microbiota in the Modulation of Food Intake and Body Weight

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The Role of the Intestinal Microbiota in the Modulation of Food Intake and Body Weight THE ROLE OF THE INTESTINAL MICROBIOTA IN THE MODULATION OF FOOD INTAKE AND BODY WEIGHT Matthew John Dalby BSc (Hons) Medical Microbiology, University of Edinburgh MSc (Distinction) Molecular Nutrition, University of Aberdeen A thesis presented for the degree of Doctor of Philosophy at the University of Aberdeen 2016 DECLARATION I declare that this thesis has been composed by myself and not been presented or accepted in any previous application for degree. The work recorded herein was carried out by myself unless otherwise stated. All sources of information have been acknowledged by means of reference. Matthew John Dalby Page | II ACKNOWLEDGEMENTS I would like to express my gratitude to my supervisors, Peter Morgan and Sandy Ross, for their continuous support and guidance during my project, for being so understanding when my health has made work difficult, and for generally being the best supervisors I could have wished for. I am indebted to Lynn Thomson for her invaluable help, advice in the lab, and for always knowing where everything is; and, to Karen Garden for enabling the completion of work I would not have been able to finish. I also wish to thank Lynda Williams for her advice over the years. I am grateful to everyone associated with the Lawson Lab for being so kind, friendly, and helpful throughout my time there. I am also indebted to Alan Walker for his teaching and time in grasping the complexities Next Generation sequencing. I am grateful to Donna Wallace and all of the staff at the MRF for all of the help and work in setting up and running the mouse studies, and to Christine Grant for her aid with sample collection. I wish to thank Gill Campbell and Pauline Young at the Genomic department for all their help with sequencing and arrays, and to Claus-Dieter Mayer for help with microarray analysis. Thanks are also due to everyone at the Rowett over the past four years. I would like to thank the BBSRC and EASTBIO for funding my project and enabling me to gain so much experience. Last but not the least, I would like to thank my family for their support and belief in me, despite my being so far away for so long. Finally, to Tiffany, for making the final two years of this PhD immeasurably better. Page | III SUMMARY The continued rise in prevalence of overweight and obesity over recent decades has focused attention on environmental factors that may be impacting on body weight. This increase has driven research into understanding mechanisms underlying energy homeostasis and the pathophysiology of obesity. Over the past decade, evidence has accumulated that suggests the intestinal microbiota, complex communities of microorganisms inhabiting the gut, have a functional role in influencing the body weight of their host. Differences in the composition of the intestinal microbiota have been observed between lean and obese mice, as well as human subjects. Transfer of microbiota from lean or obese mice into germ-free mice has been reported to transfer the obese phenotype, implicating a causal role for the microbiota. While a number of different mechanisms have been proposed to mediate these effects, the role of the gut microbiota in energy homeostasis still remains unclear. Chronic low-grade inflammation resulting from circulating gut-derived lipopolysaccharide (LPS), which activates toll-like receptor 4 (TLR4), has been proposed as one mechanism contributing to obesity. Linked to this, inflammation in the hypothalamus, a centre of neuroregulation of energy homeostasis, has also been implicated in the development of obesity. Additionally, bacterial products from the fermentation of dietary polysaccharides in the lower intestine provides another mechanism through which the microbiota can influence bodyweight, both through the harvest of undigested energy and also the stimulation of anorectic peptide hormone released by the gut. The aim of this thesis was to investigate some of the roles of the intestinal microbiota in shaping host food intake and body weight. This included investigation of potential immunomodulation by gut derived lipopolysaccharide (LPS) through TLR4 signalling, changes in gut microbiota composition in response to the diet, and, in particular, the role of dietary fibre in stimulating release of intestinal peptide hormones. High-fat diet feeding in mice, in addition to causing obesity, has been reported to increase circulating LPS and infusion of low-dose LPS into mice reportedly increased body fat, while CD14 null mice were protected from both High-Fat diet and LPS-induced Page | IV obesity. On the basis of these findings, TLR4 signalling has been implicated in the development of obesity. To investigate this, TLR4-/- or CD14-/- mice and C57BL/6J controls were fed a High-Fat or Low-Fat diet. Against prediction, neither TLR4-/- nor CD14-/- were protected against High-Fat diet-induced obesity. Body weight, body composition, and food intake remained indistinguishable between TLR4-/- or CD14-/- mice and C57BL/6J controls over 8 weeks of High-Fat diet feeding. High-Fat diet increased hypothalamic expression of SerpinA3N and SOCS3 regardless of genotype, indicating diet-induced changes in the hypothalamus. However, inflammatory gene expression was not increased. Analysis of the microbiota revealed relatively small differences between the composition of the caecal microbiota in C57BL/6J fed Low or High-Fat diets, despite large increases in body weight in High-Fat fed mice. It was hypothesised that this lack of change in the microbiota composition in the above study was due to the composition of the diets used in the experiments, namely refined High-Fat and Low-Fat diets. Previous studies reported in the literature indicate baseline control diets have typically been reported as an undefined Chow diet; this may be an important factor in microbial composition of the gut as these diets are high in fermentable dietary fibre. To investigate the relationship between diet, microbiota changes, and obesity, C57BL/6J mice were fed a Chow diet or a refined diet that was either High-Fat or Low-Fat. Relative to Chow, both High- and Low-Fat refined diets had major, yet similar, effects on the microbial composition of the gut, including changes in microbial diversity, at the phylum level with increases in the Firmicutes:Bacteroidetes ratio, and at the species level. By contrast, only High-Fat diet feeding increased obesity and glucose intolerance. This indicates that it is loss of fibre that is the main driver of shifts in microbial composition seen in mouse studies of High-Fat diet-induced obesity and that High-Fat, rather than microbial composition, drives obesity. The addition of fermentable fibre to the diet of mice fed High-Fat diets reduced food intake and body fat. The role of colonic GLP-1 and PYY secreted by enteroendocrine L- cells in mediating this effect was investigated using GLP-1R-/- and PYY-/- mice a fed a High-Fat diet supplemented with inulin or cellulose. Inulin supplementation reduced body fat and food intake in High-Fat diet fed C57BL/6J control mice compared to those supplemented with cellulose. In contrast, both the GLP-1R-/- and PYY-/- mice showed attenuated responses to the body fat and food intake-reducing effects of dietary inulin. Page | V In summary, this research questions the role of TLR4 and LPS, and also hypothalamic inflammation, in the development of diet-induced obesity in mice. These results demonstrate that the use of a well-defined control diet in studies of obesity in mice is essential and, importantly, suggests that many of the obesity-associated changes in the gut microbiota are due to the use of undefined Chow diets as an inappropriate control for the effects of refined High-Fat diets. These results also provide evidence for an essential role for both GLP-1 and PYY in mediating the food intake and bodyweight- reducing effects of fermentable fibre. Page | VI TABLE OF CONTENTS DECLARATION .............................................................................................................................. II ACKNOWLEDGEMENTS ............................................................................................................... III SUMMARY ................................................................................................................................. IV TABLE OF CONTENTS .................................................................................................................VII LIST OF FIGURES ...................................................................................................................... XVI LIST OF TABLES ....................................................................................................................... XVIII LIST OF ABBREVIATIONS............................................................................................................ XIX CHAPTER 1. .................................................................................................................................. 2 INTRODUCTION............................................................................................................................ 2 1 Introduction ............................................................................................................................................ 3 1.1 Recent key findings .................................................................................................................................... 4 1.2 The human gut microbiota .......................................................................................................................
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