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© 2019 Edek Alex Joel Williams ALL RIGHTS RESERVED © 2019 Edek Alex Joel Williams ALL RIGHTS RESERVED FRUCTOSE AFFECTS THE GROWTH OF LONG BONES IN MICE INDEPENDENT OF KETOHEXOKINASE By EDEK ALEX JOEL WILLLIAMS A dissertation submitted to the School of Graduate Studies Rutgers, The State University of New Jersey In partial fulfillment of the requirements For the degree of Doctor of Philosophy Graduate Program in Biomedical Engineering Written under the direction of J. Christopher Fritton And approved by ___________________________________ ___________________________________ ___________________________________ ___________________________________ ___________________________________ New Brunswick, New Jersey May 2019 ABSTRACT OF THE DISSERTATION Fructose Affects the Growth of Long Bones in Mice Independent of Ketohexokinase By EDEK ALEX JOEL WILLIAMS Dissertation Director: J. Christopher Fritton Current trends in the Western-pattern diet are replacing bone-fortifying, calcium-rich beverages and foods with sweetened artificial alternatives. High-fructose corn syrup has only been used as a popular sweetener since 1970. Diet may impact growth by limiting the bioavailability of nutrients required for bone to reach its full genetic potential. The effects of reduced calcium, in animal models and man, have been studied extensively and in the work to be presented I uncovered that low calcium diet results in lower bone cellularity, i.e., fewer incorporating osteocytes per bone tissue volume. However, the current understanding of fructose and its effects on bone growth are varied, due to the absence of a standardized model and standard fructose administration regimen. Fructose is metabolized in the cytoplasm by the enzyme ketohexokinase (KHK), and excessive consumption may affect bone health. Specifically, previous work in calcium-restricted, growing mice demonstrated that fructose disrupted intestinal calcium transport. I hypothesized that the observed effects on bone were KHK-dependent and examined the effects of fructose on the long bones of growing mice in a series of studies. Congenic mice with intact KHK (wild-type, WT) or global knockout of both isoforms of KHK A/C (KHK- KO), were fed control diets or administered fructose either through diet or implanted osmotic pumps for 8 weeks. I found that dietary fructose increased by 40-fold plasma ii fructose in KHK-KO compared to controls (p < 0.05). Plasma fructose was less effected due to pump administration. Obesity (no differences in epidydimal fat or body weight) or altered insulin, was not observed due to the fructose levels introduced. Longitudinal growth of the femur long-bone was inhibited in the KHK-KO mice fed 20% fructose. Unexpectedly, fructose feeding resulted in greater bone mineral density, percent volume and number of trabeculae in the distal femur of KHK-KO. Moreover, higher plasma fructose concentrations correlated with greater trabecular bone volume, greater work-to- fracture in three-point bending of the femur mid-shaft, and greater plasma sclerostin. Since the metabolism of fructose is severely inhibited in the KHK-KO condition, the new results combined with additional data generated during the completion of this dissertation suggests that fructose reaching the lower intestine may affect bone growth through an interaction with the microbiota. Future pursuit of this line of research is important as the effects of increased fructose consumption on bone during growth may influence the future risk for osteoporotic fracture. iii DEDICATION Dedicated to my mother and father and the Boys and Girls of: Jamaica New York and New Jersey iv Acknowledgements This document is an acknowledgment that no man is an island and that an individual’s work is buoyed by the support of a great community. This work would not have been completed without the patience and guidance of my thesis advisor, Dr. J. Chris Fritton and collaborators Dr. Ronaldo Ferraris and Dr. Veronique Douard. I would like to thank the members of my committee: Dr. Patricia Buckendahl, Dr. Noshir Langrana Dr. Adrian Mann and Dr. Maribel Vazquez. I would like to thank my collaborators, Dr. Keiichiro Ishimoto, Dr. Kunihiro Kishada, Dr. Yves Sabbagh and Dr. Chirag Patel. I would like the acknowledge fellow lab members, past and present: Dr. Joseph Geissler, Dr. George Pellegrino, Dr. Devendra Bajaj and Brian Canter. Your support and objectivity have made the daily challenges of this thesis work less daunting. I would like to thank Dr. Phillip Payton, Dr. Mitchell Schaffler and Dr. Courtney St. Prix for creating the programs that introduced me to Biomedical Engineering at an early age. I would like to thank the undergraduate labs that were opened to me and for the valuable experiences in bone biomechanics and imaging. I would like to thank Dr. Ian Xu, Dr. Paolo Palachio and Dr. Ericka Calton for their mentorship. I would like to thank my graduate school classmates for levity during trying times. Namely, Dr. Emmanuel Ekeueme, Dr. Renea Faulknor, Dr. Antoinette Nelson, Dr. Joseph Kim, Dr. Brittany Taylor, Dr. Mathew Long, and Dr. Saurav De. I would like to thank the faculty and staff of Rutgers, Dr. David Schreiber, Dr. Joseph Freeman, Dr. Edouard Azzam, Linda, Stratos, Mayra Barreto, Beatrice Suffrant, Luke Fritzky, Ms. Diane, Ms. Annie, Ms. Gierve and security and animal facility personnel. Lastly, I would like to acknowledge the support of my family, my mother, my sister, niece, aunts and uncles and cousins. All I do has been for you. v Table of Contents ABSTRACT OF THE DISSERTATION ........................................................................... ii DEDICATION ................................................................................................................... iv Acknowledgements ............................................................................................................. v Table of Contents ............................................................................................................... vi List of Tables ................................................................................................................... viii List of Illustrations ........................................................................................................... xiv Chapter 1 : Introduction ...................................................................................................... 1 Fructose ....................................................................................................................... 2 Bone .......................................................................................................................... 12 Growth ...................................................................................................................... 21 Bone and the Regulation of Mineral Balance ........................................................... 25 Bone and the Regulation of Energy Balance ............................................................ 35 Chapter 2 : Bone Quality Assessment in Fructose Feeding Experiments ........................ 47 Introduction ............................................................................................................... 47 Materials and Methods .............................................................................................. 48 Results ....................................................................................................................... 51 Discussion ................................................................................................................. 67 Chapter 3 : Bone Growth is Influenced by Fructose in Adolescent Male Mice Lacking Ketohexokinase (KHK) .................................................................................................... 71 vi Abstract ..................................................................................................................... 71 Introduction ............................................................................................................... 72 Materials and methods .............................................................................................. 74 Results ....................................................................................................................... 80 Discussion ............................................................................................................... 103 Acknowledgments................................................................................................... 108 Chapter 4 : Elevation of Serum Fructose in both ketohexokinase sufficient and deficient mice with the use of osmotic pumps ............................................................................... 110 Abstract ................................................................................................................... 110 Introduction ............................................................................................................. 111 Materials and Methods ............................................................................................ 113 Results ..................................................................................................................... 119 Discussion ............................................................................................................... 139 Acknowledgments................................................................................................... 142 Chapter 5 : Conclusion...................................................................................................
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