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Docosahexaenoic Acid and Butyrate Synergistically

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Docosahexaenoic Acid and Butyrate Synergistically DOCOSAHEXAENOIC ACID AND BUTYRATE SYNERGISTICALLY MODULATE INTRACELLULAR CALCIUM COMPARTMENTALIZATION TO INDUCE COLONOCYTE APOPTOSIS A Dissertation by SATYA SREE N. KOLAR Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY August 2007 Major Subject: Nutrition DOCOSAHEXAENOIC ACID AND BUTYRATE SYNERGISTICALLY MODULATE INTRACELLULAR CALCIUM COMPARTMENTALIZATION TO INDUCE COLONOCYTE APOPTOSIS A Dissertation by SATYA SREE N. KOLAR Submitted to the Office of Graduate Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Approved by: Chair of Committee, Robert S. Chapkin Committee Members, Joanne R. Lupton Robert C. Burghardt Mark J. Zoran Chair of Nutrition Faculty, Nancy D. Turner August 2007 Major Subject: Nutrition iii ABSTRACT Docosahexaenoic Acid and Butyrate Synergistically Modulate Intracellular Calcium Compartmentalization to Induce Colonocyte Apoptosis. (August 2007) Satya Sree N. Kolar, B.M.S., Bangalore University, India; M.S., University of Kentucky Chair of Advisory Committee: Dr. Robert S. Chapkin Docosahexaenoic acid (DHA, 22:6n-3) from fish oil, and butyrate, a short-chain fatty acid fiber-fermentation product, protect against colon tumorigenesis in part by coordinately inducing apoptosis. We have demonstrated that the combination of these two bioactive compounds demonstrates an enhanced ability to induce colonocyte apoptosis by potentiating mitochondrial lipid oxidation. In order to explore the potential involvement of intracellular Ca2+ in the pro-apoptotic effect of DHA and butyrate, young adult mouse colonocytes (YAMC) and human colonocytes (HCT-116: p53+/+ and p53- /-) were treated with DHA or linoleic acid (LA) for 72 h ± butyrate for the final 6, 12 or 24 h. Cytosolic and mitochondrial Ca2+ levels were measured using Fluo-4 and Rhod-2. In addition, IP3 pool, store-operated channel (SOC)-mediated changes and apoptosis were measured. DHA did not alter basal Ca2+ or apoptosis following 6 h butyrate co- treatment. In contrast, at 12 and 24 h, DHA and butyrate treated cultures exhibited a decrease in cytosolic Ca2+ and enhanced apoptosis compared to LA and butyrate. DHA and butyrate also increased the mitochondrial-to-cytosolic Ca2+ ratio at 6, 12 and 24 h. iv The accumulation of mitochondrial Ca2+ preceded the onset of apoptosis which increased only following 12 h of butyrate co-treatment. RU-360, a mitochondrial uniporter inhibitor, abrogated mitochondrial Ca2+ accumulation and also partially blocked apoptosis in DHA and butyrate co-treated cells. p53+/+ and p53-/- cells demonstrated similar data with respect to all parameters. Additionally, mitochondrial Ca2+ measurements were also made in rat primary- colonocyte-culture. Rats were fed semipurified diets containing either fish oil (a source of DHA) or corn oil (a source of LA), and colonic crypts were incubated in butyrate ex- vivo and mitochondrial Ca2+ was quantified. Crypts from rats fed fish oil incubated in butyrate exhibited an increase in the mitochondrial-to-cytosolic Ca2+ ratio compared to fish oil only. In summary, our results indicate for the first time that the combination of DHA and butyrate, compared to butyrate alone, further enhances apoptosis by additionally recruiting a p53-independent Ca2+-mediated intrinsic mitochondrial pathway. These data explain in part why fermentable fiber when combined with fish oil exhibits an enhanced ability to induce apoptosis and protect against colon tumorigenesis. v DEDICATION I would like to dedicate this dissertation to my parents, Late Narasimha Murthy, and Mrs. Leela N. Murthy, my sister-in-law Late Naila Manzoor, brother Sathish Cayenne, sister Satyamba K, husband Ashish Sharma and my wonderful daughter Neha Narayan. It is their unconditional love, incessant encouragement and formidable support that has insipired me to stand strong and pursue my goals. vi ACKNOWLEDGEMENTS I extend my sincere gratitude to Dr. Robert Chapkin for his invaluable encouragement, support and outstanding guidance throughout my training. I’m especially indebted to him for believing in my strengths and standing by me at every moment. He has been a most admirable teacher, outstanding scientist, and exceptional mentor. As my mentor, he has taught me more than I can give him credit for by writing these few lines. He has shown me by his example, what a good scientist should be. The foundation he has given me will influence my future in both the scientific and personal world. I will forever be appreciative of his fervent support towards achieving my goals. It has been a great pleasure knowing and working with him. I also extend my sincere appreciation to my committee members Dr. Joanne R. Lupton, Dr. Robert C. Burghardt and Dr. Mark J. Zoran who have given me extensive professional guidance, encouragement and their invaluable time. They have been ever willing to answer my questions and have helped me make the right decisions. I consider myself to be very lucky to have had such an excellent advisory committee, who have been so supportive of me through my graduate work. I’d also like to thank Dr. Nancy D. Turner for her advice and support throughout my training. I would like to offer my exceptional thanks to Dr. Rola Barhoumi, for her incredible assistance with all my experiments. Her expertise coupled with her helpful guidance and tremendous moral support has helped me cruise through the difficult times and enjoy the good moments of reseach. She has been a very supportive member of the vii team without whom this work would not be possible. Her endless patience, effort, hours of work on the microscope, unconditional support and confidence in my skills has gotten me to where I am. I am very appreciative of the thoughtful advice and moral support extended to me by Dr. Laurie Davidson throughout my tenure not just in the Chapkin lab, but also during my stay at College Station. I’d also like to thank Evelyn Callaway for her willingness to help, technical expertise and timely encouragement to make this project successful. I would like to thank Dr. Yang Yi Fan for her patient instruction at every step of growth of this project. My thanks go out to Wooki Kim who has provided the technical assistance, a sweet smile and kind word when I needed it. It has been a great pleasure and wonderful experience to work with such a nice team. This lab team has not just helped with my work but has helped me understand things better and grow as a person. This section would be incomplete without a mention of the role of my family in the pursuit of this project. I’d like to thank my parents, brother and sister whose love and guidance is with me in whatever I pursue. My parents have been my ultimate role models. More importantly, I wish to thank my loving husband whose patience, advice and encouragement has taken me a long way through my work. He has provided me with unending inspiration, persistent motivation and has been my forte. Last but never the least, I want to thank my daughter Neha whose level of tolerance has taught me a lot. She has accompanied me to the lab and has stayed awake with me through the wee hours of the morning, during my odd-hour experiments. She has been my greatest supporter viii and has been the reason for me to rise every morning and pursue my dream. She has never failed to tell me that I will be “a winner” in whatever I did. She has provided me with the vigor and power to succeed. I thank all of my friends whose names are not mentioned here due to space constraints. I strongly believe that each of you have made a great impact in my life. I love and thank you all and owe all of you the best part of me and my work. ix TABLE OF CONTENTS Page ABSTRACT.................................................................................................................... iii DEDICATION ..................................................................................................................v ACKNOWLEDGEMENTS .............................................................................................vi TABLE OF CONTENTS.................................................................................................ix LIST OF FIGURES..........................................................................................................xi LIST OF TABLES ........................................................................................................ xiii LIST OF ABBREVIATIONS ........................................................................................xiv CHAPTER I INTRODUCTION AND LITERATURE REVIEW..........................................1 Intestinal physiology and pathogenesis of colon cancer ........................1 Diet and colon cancer.............................................................................8 Ion transport across biological membranes..........................................13 Intracellular Ca2+ homeostasis..............................................................19 Tumor suppressor gene-p53.................................................................25 Summary and purpose..........................................................................27 Hypotheses...........................................................................................29 Specific aims ........................................................................................29 II DOCOSAHEXAENOIC ACID AND BUTYRATE SYNERGISTICALLY INDUCE COLONOCYTE
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