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Differential Activity and Content of High-Affinity Glutamate Transporters

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Differential Activity and Content of High-Affinity Glutamate Transporters University of Kentucky UKnowledge Theses and Dissertations--Animal and Food Sciences Animal and Food Sciences 2017 DIFFERENTIAL ACTIVITY AND CONTENT OF HIGH-AFFINITY GLUTAMATE TRANSPORTERS, CONTENT OF THEIR REGULATORY PROTEINS, AND CAPACITY FOR GLUTAMINE AND GLUTATHIONE SYNTHESIS IN TISSUES OF FINISHED VERSUS GROWING STEERS Jing Huang University of Kentucky, [email protected] Author ORCID Identifier: https://orcid.org/0000-0003-2923-2158 Digital Object Identifier: https://doi.org/10.13023/ETD.2017.492 Right click to open a feedback form in a new tab to let us know how this document benefits ou.y Recommended Citation Huang, Jing, "DIFFERENTIAL ACTIVITY AND CONTENT OF HIGH-AFFINITY GLUTAMATE TRANSPORTERS, CONTENT OF THEIR REGULATORY PROTEINS, AND CAPACITY FOR GLUTAMINE AND GLUTATHIONE SYNTHESIS IN TISSUES OF FINISHED VERSUS GROWING STEERS" (2017). Theses and Dissertations-- Animal and Food Sciences. 81. https://uknowledge.uky.edu/animalsci_etds/81 This Doctoral Dissertation is brought to you for free and open access by the Animal and Food Sciences at UKnowledge. It has been accepted for inclusion in Theses and Dissertations--Animal and Food Sciences by an authorized administrator of UKnowledge. For more information, please contact [email protected]. STUDENT AGREEMENT: I represent that my thesis or dissertation and abstract are my original work. Proper attribution has been given to all outside sources. I understand that I am solely responsible for obtaining any needed copyright permissions. I have obtained needed written permission statement(s) from the owner(s) of each third-party copyrighted matter to be included in my work, allowing electronic distribution (if such use is not permitted by the fair use doctrine) which will be submitted to UKnowledge as Additional File. I hereby grant to The University of Kentucky and its agents the irrevocable, non-exclusive, and royalty-free license to archive and make accessible my work in whole or in part in all forms of media, now or hereafter known. I agree that the document mentioned above may be made available immediately for worldwide access unless an embargo applies. I retain all other ownership rights to the copyright of my work. I also retain the right to use in future works (such as articles or books) all or part of my work. I understand that I am free to register the copyright to my work. REVIEW, APPROVAL AND ACCEPTANCE The document mentioned above has been reviewed and accepted by the student’s advisor, on behalf of the advisory committee, and by the Director of Graduate Studies (DGS), on behalf of the program; we verify that this is the final, approved version of the student’s thesis including all changes required by the advisory committee. The undersigned agree to abide by the statements above. Jing Huang, Student Dr. James C. Matthews, Major Professor Dr. David Harmon, Director of Graduate Studies DIFFERENTIAL ACTIVITY AND CONTENT OF HIGH-AFFINITY GLUTAMATE TRANSPORTERS, CONTENT OF THEIR REGULATORY PROTEINS, AND CAPACITY FOR GLUTAMINE AND GLUTATHIONE SYNTHESIS IN TISSUES OF FINISHED VERSUS GROWING STEERS DISSERTATION A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the College of Agriculture, Food and Environment at the University of Kentucky By Jing Huang Lexington, Kentucky Director: Dr. Matthews, Professor of Animal Science Lexington, Kentucky 2017 Copyright © Jing Huang 2017 ABSTRACT OF DISSERTATION DIFFERENTIAL ACTIVITY AND CONTENT OF HIGH-AFFINITY GLUTAMATE TRANSPORTERS, CONTENT OF THEIR REGULATORY PROTEINS, AND CAPACITY FOR GLUTAMINE AND GLUTATHIONE SYNTHESIS IN TISSUES OF FINISHED VERSUS GROWING STEERS Improvement of feeding regimens for production animals has been hindered by a lack of fundamental knowledge about how the capacity to regulate nutrient absorption across cell membranes affects the function of nutrient metabolizing enzymes. The objective is to determine if the activities and protein content of system - X AG glutamate transporter, its regulatory protein (GTRAP3-18 and ARL6IP1), glutamine synthetase (GS) and glutathione (GSH) content, changes in liver (Experiment 1), longissimus dorsi (LM) and subcutaneous adipose tissue (SF) (Experiment 2) as beef steers transitioned from predominantly-lean (growing) to - - lipid (finished) tissue accretion phases. In liver (Experiment 1), system X AG activity in canalicular membranes was abolished as steers developed from growing to finished stages but did not change in basolateral membranes. EAAC1 protein content in liver homogenates decreased in finished vs. growing steers, whereas GTRAP3-18 and ARL6IP1 content increased and GLT-1 content did not change. Concomitantly, hepatic GS activity decreased in finished steers whereas GS protein content did not differ. Hepatic GSH content did not differ in finished vs. growing steers. These results demonstrate a negative functional relationship between GTRAP3-18 and - system X AG activity with glutamine synthesis capacity in livers of fattened cattle. In addition to liver, skeletal muscle and adipose tissues play important roles in maintaining whole-body glutamate and nitrogen homeostasis. In Experiment 2, Western blot analysis of LM homogenates showed decreased EAAC1 and GS content, whereas GTRAP3-18 and ARL6IP1 did not differ in finished vs. growing steers. GSH content in LM was increased in finished vs. growing steers in concomitance with increased mRNA expression of GSH-synthesizing enzymes. In SF, GTRAP3-18 and ARL6IP1 content was increased, whereas EAAC1 and GS content did not differ. Concomitantly, GSH content in SF was decreased in finished vs. growing steers in parallel with decreased mRNA expression of GSH- metabolizing enzymes. These results demonstrate that the negative regulatory relationship between GTRAP3-18 and ARL6IP1 with EAAC1 and GS expression, which exists in liver, does not exist in LM and SF of fattened cattle; and antioxidant capacity in LM and SF changes and differs as steer compositional gain shifts from lean to lipid phenotype. To further explore the upstream regulatory machinery of EAAC1, transcriptome analysis (Experiment 3) was conducted to gain a greater understanding of hepatic metabolic shifts associated with the change in whole-body compositional gain of growing vs. finished beef steers. The expression of upstream regulators of EAAC1 was decreased in a manner consistent with the decreased EAAC1 activity in Experiment 1. Bioinformatic analysis found that, for amino acid metabolism, finished steers had increased capacities for ammonia, arginine, and urea production, and shunting of amino acid carbons into pyruvate. For carbohydrate metabolism, capacity for glycolysis was inhibited, whereas glycogen synthesis was stimulated in finished steers. For lipid metabolism, finished steers showed decreased capacity for fatty acid activation and desaturation, but increased capacity for fatty acid β-oxidation and lipid storage. In addition, redox capacity and inflammatory responses were decreased in finished steers. Collectively, these data describe novel - regulatory relationships of system X AG in liver and peripheral tissues, and the metabolic mechanisms that control nutrient use efficiency, as beef steers develop from lean to lipid phenotypes. Keywords: Finishing steers, Peripheral tissues, Glutamate transport, Glutathione, Transcriptome Jing Huang Student’s Signature 9-24-17 Date DIFFERENTIAL ACTIVITY AND CONTENT OF HIGH-AFFINITY GLUTAMATE TRANSPORTERS, CONTENT OF THEIR REGULATORY PROTEINS, AND CAPACITY FOR GLUTAMINE AND GLUTATHIONE SYNTHESIS IN TISSUES OF FINISHED VERSUS GROWING STEERS By Jing Huang Dr. James C. Matthews Director of Dissertation Dr. David Harmon Director of Graduate Studies 9-24-17 (Date) ACKNOWLEDGEMENTS I would like to express my appreciation to my PhD advisor, Dr. James Matthews for giving me a good opportunity to learn about animal science. I am indebted to him for his knowledge and guidance throughout the course of my PhD study. I would also like to express my gratitude to my dissertation committee members, Dr. Robert Harmon, Dr. Merlin Lindemann, Dr. Phillip Bridges, Dr. Kuey Chen for their advice and support of this research, and to Dr. Zhengheng Guo, the outside examiner. I would especially like to acknowledge my parents for being supportive as I have made brave decisions and gone through difficult transitions during my PhD study. Thank you for instilling values in me: faith, love, hard work and perseverance that I can carry on throughout my life. I wouldn’t be here without you two. Finally, I wish to thank my friends here in Lexington. Thank you for being there for me when I need you the most. I am blessed to have such amazing people in my life! iii Table of Contents ACKNOWLEDGEMENTS .............................................................................................. III LIST OF TABLES ........................................................................................................... VII LIST OF FIGURES .......................................................................................................... IX CHAPTER 1. INTRODUCTION ....................................................................................... 1 CHAPTER 2. LITERATURE REVIEW ............................................................................ 4 MOLECULAR AND FUNCTIONAL CHARACTERIZATION OF PROTEINS CAPABLE OF GLU TRANSPORT ...................................................................................................................... 4 GLU TRANSPORT
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