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Citrus Bioactive Compounds: Isolation, Characterization

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Citrus Bioactive Compounds: Isolation, Characterization CITRUS BIOACTIVE COMPOUNDS: ISOLATION, CHARACTERIZATION AND MODULATION OF BACTERIAL INTERCELLULAR COMMUNICATION AND VIRULENCE A Dissertation by AMIT VIKRAM 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 May 2011 Major Subject: Horticulture Citrus Bioactive Compounds: Isolation, Characterization and Modulation of Bacterial Intercellular Communication and Virulence Copyright 2011 Amit Vikram CITRUS BIOACTIVE COMPOUNDS: ISOLATION, CHARACTERIZATION AND MODULATION OF BACTERIAL INTERCELLULAR COMMUNICATION AND VIRULENCE A Dissertation by AMIT VIKRAM 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, Bhimanagouda S. Patil Committee Members, Suresh D. Pillai Arul Jayaraman Leonardo L. Lombardini Kil Sun Yoo G. K. Jayaprakasha Head of Department, Tim Davis May 2011 Major Subject: Horticulture iii ABSTRACT Citrus Bioactive Compounds: Isolation, Characterization and Modulation of Bacterial Intercellular Communication and Virulence. (May 2011) Amit Vikram, B.Sc.; M.Sc., G. B. Pant University of Agriculture and Technology, Pantnagar, India Chair of Advisory Committee: Dr. Bhimanagouda S. Patil The secondary metabolites of citrus such as limonoids and flavonoids constitute an important part of human diet. The present work was undertaken to elucidate the effect of citrus limonoids and flavonoids on the bacterial cell-cell signaling in Vibrio harveyi, Escherichia coli O157:H7 and Salmonella Typhimurium LT2. The first experiment was focused on purification of limonoids from grapefruit and sour orange seeds. The limonoids were extracted using organic solvents and purified by chromatographic techniques. A total of ten limonoids (7 aglycones and 3 glucosides) were purified. Currently, simultaneous measurement of aglycones and glucosides of limonoids is not available. To address this limitation, an analytical method using high performance liquid chromatography was developed with the capability of measuring both aglycones and glucosides in a single run. Furthermore, its applicability in the fruit and juice samples was demonstrated. The third study investigated the V. harveyi cell-cell signaling inhibitory potential of purified limonoids. Isolimonic acid, ichangin, obacunone and nomilin showed potent iv inhibitory activity. Furthermore, isolimonic acid and ichangin inhibit the signal transduction pathway by up-regulating the response regulator luxO. Isolimonic acid was also found to be a potent inhibitor of Escherichia coli O157:H7 cell-cell signaling in the fourth study. The results demonstrated that isolimonic acid inhibits the autoinducer/epinephrine mediated cell-cell signaling, biofilm and virulence in QseBC and QseA dependent fashion. Further investigations using limonin analogues, in the fifth study, demonstrated that the analogue limonin-7-methoxime inhibited the E. coli biofilm in type 1 pili and antigen 43 dependent-fashion, by preventing the binding of the adhesins to plastic surfaces. Another limonoid, obacunone was demonstrated to attenuate the Salmonella virulence by repressing Salmonella Pathogenicity Island 1 (SPI-1) in EnvZ/OmpR dependent mecahnism. The seventh study showed that naringenin, among the flavonoids, was the most potent inhibitor of V. harveyi and E. coli O157:H7 cell-cell signaling. Furthermore, naringenin was found to repress the (SPI-1) in PstS-HilD dependent fashion in the eighth study. The results of the study suggest that several limonoids and flavonoids possess the ability to interfere with cell-cell signaling and virulence in three bacterial species. v DEDICATION This dissertation is dedicated to the spirit, who visited us on this planet earth. vi ACKNOWLEDGEMENTS This work would not have seen the daylight without the support and guidance of many people, who shared their experiences, knowledge and passion for science. The foremost among them is my mentor, Dr. Bhimanagouda S. Patil, whose thoughtful guidance and measured ‗challenges‘ allowed me to grow as a scientist. I would like to thank him for his keen support and assistance through the completion of my doctoral degree program. I would also like to thank members of my graduate committee, Dr. Pillai, Dr. Lombardini, Dr. Jayaraman, Dr. Yoo and Dr. Jayaprakasha, for their productive criticism and support through the thick and thin of my graduate life, especially for letting me test my crazy ideas and using the lab facilities without hindrance. I also would like to thank Dr. Jayaprakasha and Dr. Jesudhasan for teaching me the techniques I have used in my research. Additionally, I would like to recognize my collegues and fellow labmates, Ram, Priyanka, Jinhee, HaeJeen, Murthy and Kranthi, for their support. I would also like to extend my special thanks to Ms. Connie Sebesta and her team for taking excellent care of all the administrative formalities and providing immense help in coping with the not-so-routine non-research stuff. I would like to thank the entire Vegetable and Fruit Improvement Center family where multidisciplinary researchers and students exchange ideas and conduct experiments, which provided me the foundation to face future challenges as a scientist. I appreciate the financial support from the project, ―Designing Foods for Health‖ through the Vegetable and Fruit Improvement Center. vii I am also grateful to my parents, Dr. R. S. L. Srivastava and Mrs. Asha Srivastava, for bringing me in to this world and their unequalled support and love. I would also like to recognize my brother, Avijit, sister, Neerajakshi, and their families for unconditional love. Finally, I am thankful to my wife, Meenu, and my daughter, Arushi, whose unwavering and cheerful support during the crazy times kept me going. viii TABLE OF CONTENTS Page ABSTRACT .............................................................................................................. iii DEDICATION .......................................................................................................... v ACKNOWLEDGEMENTS ...................................................................................... vi TABLE OF CONTENTS .......................................................................................... viii LIST OF FIGURES ................................................................................................... xi LIST OF TABLES .................................................................................................... xv CHAPTER I INTRODUCTION AND LITERATURE REVIEW ............................ 1 1.1 Background .............................................................................. 1 1.2 Citrus ........................................................................................ 1 1.3 Quorum Sensing ....................................................................... 10 1.4 The Under-utilized Potential of Plants ..................................... 19 1.5 Interference with Quorum Sensing .......................................... 20 1.6 Main Hypothesis and Aims of the Project ............................... 23 II ISOLATION AND PURIFICATION OF LIMONOIDS ..................... 25 2.1 Synopsis ................................................................................... 25 2.2 Introduction .............................................................................. 26 2.3 Materials and Methods ............................................................. 28 2.4 Results ...................................................................................... 32 2.5 Discussion ................................................................................ 39 III HIGH PERFORMANCE LIQUID CHROMATOGRAPHY METHOD FOR SIMULTANEOUS MEASUREMENT OF CITRUS LIMONOID AGLYCONES AND GLUCOSIDES .............. 42 3.1 Synopsis ................................................................................... 42 3.2 Introduction .............................................................................. 43 ix CHAPTER Page 3.3 Materials and Methods ............................................................. 48 3.4 Results and Discussion ............................................................. 51 IV INTERFERENCE OF VIBRIO HARVEYI CELL-CELL SIGNALING AND BIOFILM FORMATION BY LIMONOIDS ...... 62 4.1 Synopsis ................................................................................... 62 4.2 Introduction .............................................................................. 63 4.3 Materials and Methods ............................................................. 65 4.4 Results ...................................................................................... 72 4.5 Discussion ................................................................................ 82 V INHIBITION OF ESCHERICHIA COLI O157:H7 CELL-CELL COMMUNICATION AND VIRULENCE BY LIMONOIDS ............ 89 5.1 Synopsis ................................................................................... 89 5.2 Introduction .............................................................................. 90 5.3 Materials and Methods ............................................................. 92 5.4 Results ...................................................................................... 98 5.5 Discussion ................................................................................ 109 VI INHIBITION OF E. COLI BIOFILM BY LIMONIN ANALOGUES ....................................................................................
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