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Investigating the Stimulatory Mechanisms of Phlorizin, Phloretin and Chlorogenic Acid Polyphenols on Akkermansia Muciniphila in Vitro

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Investigating the Stimulatory Mechanisms of Phlorizin, Phloretin and Chlorogenic Acid Polyphenols on Akkermansia Muciniphila in Vitro Investigating the stimulatory mechanisms of phlorizin, phloretin and chlorogenic acid polyphenols on Akkermansia muciniphila in vitro by Ayano Hojo A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Master of Science in Food Science Guelph, Ontario, Canada © Ayano Hojo, December, 2019 ABSTRACT INVESTIGATING THE STIMULATORY MECHANISMS OF PHLORIZIN, PHLORETIN AND CHLOROGENIC ACID POLYPHENOLS ON AKKERMANSIA MUCINIPHILA IN VITRO Ayano Hojo Advisor: University of Guelph, 2019 Dr. Gisèle LaPointe Plant polyphenol extracts are shown to have prebiotic-like, stimulatory effect on Akkermansia muciniphila. A. muciniphila is a potentially health beneficial commensal gut microbe that utilizes mucin for energy. However, the exact mechanism of the stimulation is unknown. In this study, mechanisms that may lead to competitive advantages for A. muciniphila were tested using pure forms of phlorizin, phloretin, and chlorogenic acid in vitro. The polyphenols had no significant effect on the production of mucin by the host cells. No significant inhibition of the bacterial growth by phlorizin or chlorogenic acid were observed up to 1000 μM. However, phloretin significantly inhibited the growth of mucus-associated competitors of A. muciniphila except for Escherichia coli at 250 μM. The polyphenols tested may not directly affect mucin production by the host or function as prebiotics. Rather, the stimulation of A. muciniphila may be due to its higher tolerance for polyphenols relative to competitors. iii ACKNOWLEDGEMENTS I am very grateful for my advisor, Dr. Gisèle LaPointe, for her mentorship and support thorough out this journey. I admire her teaching approach that encouraged me to think critically and be independent. Her doors were always open for questions and discussions. The meetings I had with Gisèle were challenging at times but always guided me to the next steps. I truly respect her interdisciplinary expertise and passion in research. Working together, I gained so much experience both technically and personally as an academic researcher. I would like to thank my advisory committee members, Dr. Massimo Marcone and Dr. Sampathkumar Balamurugan, for their valuable inputs. I would also like to thank Dr. Michelle Edwards for all the statistical advice and directions. As well, I was fortunate to have our lab research associate Dr. Ajila Matheyambath for her expertise in HPLC. Without her I would have had difficult times with the HPLC experiments. Many thanks to my friends and everyone from Dr. LaPointe’s lab and CRIFS for being by my side. I was very comfortable to talk about my problems and frustrations at stressful times. We all shared ups and downs, and I felt that I was a part of a community. I also enjoyed all the foods that brightened up my days. Special thanks go to our CRIFS building manager Nafiseh Jam, who often brought delicious sweets and ice creams. Being at CRIFS, I was able to meet and bond with people with whom I wish I can keep in touch in the future. Finally, I need to thank my family for their continuing support for my education. Whenever I was bad-tempered from being busy or things not going well, they were very understanding. I always had a good night’s sleep and being at home for sure kept me healthy! Thank you so much for everyone who made this opportunity possible. iv DECLARATION I, Ayano Hojo, was the principal author of this thesis. All experimental designs, experimental procedures and analysis of results were constructed and performed by me under the supervision of Dr. Gisèle LaPointe. v TABLE OF CONTENTS ABSTRACT ................................................................................................................................... ii ACKNOWLEDGEMENTS ........................................................................................................ iii DECLARATION.......................................................................................................................... iv TABLE OF CONTENTS ............................................................................................................. v LIST OF TABLES ....................................................................................................................... ix LIST OF FIGURES .................................................................................................................... xii LIST OF ABBREVIATIONS ................................................................................................... xiii LIST OF APPENDICES ............................................................................................................ xv Chapter 1. Literature Review ...................................................................................................... 1 1.1 Introduction ...................................................................................................................... 1 1.2 Apple polyphenols............................................................................................................ 2 1.2.1 Apple polyphenol consumption and health benefits ................................................. 2 1.2.2 Chemical structure and composition of apple polyphenols ...................................... 5 1.2.3 Bioavailability of apple polyphenols ...................................................................... 12 1.3 A. muciniphila and mucus-associated gut microbiota .................................................... 16 1.3.1 A. muciniphila as a beneficial commensal gut microbe .......................................... 16 1.3.2 Mucin-degrading and mucus-residing gut microbes ............................................... 19 1.4 Polyphenol and gut microbiota interactions ................................................................... 24 1.4.1 Polyphenols as prebiotics and antibacterial compounds ......................................... 24 vi 1.4.2 Proposed prebiotic or stimulatory mechanisms of polyphenols on A. muciniphila 29 Chapter 2. Hypothesis and Objectives ...................................................................................... 39 2.1 Hypothesis ...................................................................................................................... 39 2.2 Objectives ....................................................................................................................... 39 Chapter 3. Materials and Methods ............................................................................................ 40 3.1 Polyphenols used in the study ........................................................................................ 40 3.2 Mucin gene expression and production by HT29-MTX cells in presence of polyphenols ........................................................................................................................................ 40 3.2.1 Cell culture conditions ............................................................................................ 40 3.2.2 Sulforhodamine B (SRB) assay .............................................................................. 41 3.2.3 Polyphenol exposure to HT29-MTX cells .............................................................. 42 3.2.4 RNA and protein extraction .................................................................................... 42 3.2.5 RT-qPCR for evaluation of the expression of selected mucin genes ...................... 43 3.2.6 ELLA for quantification of total mucin-like glycoprotein ..................................... 48 3.3 Inhibitory effect of phlorizin, phloretin and chlorogenic acid on select bacteria .......... 50 3.3.1 Bacteria viable counts and optical density .............................................................. 50 3.3.2 Broth minimal inhibitory concentration (MIC) ...................................................... 51 3.4 In vitro growth of bacteria in mixed culture with the presence of polyphenols............. 51 3.4.1 In vitro mixed culture.............................................................................................. 51 3.4.2 PMA-qPCR for enumeration of bacteria ................................................................ 52 vii 3.4.3 HPLC for polyphenol degradation analysis ............................................................ 57 3.5 Statistical analysis .......................................................................................................... 58 Chapter 4. Results ....................................................................................................................... 59 4.1 The effect of polyphenols on the expression of mucin genes and mucin production by HT29-MTX cells ....................................................................................................................... 59 4.2 The MIC of phlorizin, phloretin, and chlorogenic acid for the selected mucus-associated gut bacteria ................................................................................................................................ 63 4.3 The effect of polyphenols on the abundance of mucus-associated gut bacteria in in vitro mixed culture ............................................................................................................................ 65 Chapter 5. Discussion ................................................................................................................. 73 5.1 Effect of polyphenols on human epithelial cells ...........................................................
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