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Annonacin in Asimina Triloba Fruit : Implications for Neurotoxicity

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Annonacin in Asimina Triloba Fruit : Implications for Neurotoxicity University of Louisville ThinkIR: The University of Louisville's Institutional Repository Electronic Theses and Dissertations 12-2011 Annonacin in Asimina triloba fruit : implications for neurotoxicity. Lisa Fryman Potts University of Louisville Follow this and additional works at: https://ir.library.louisville.edu/etd Recommended Citation Potts, Lisa Fryman, "Annonacin in Asimina triloba fruit : implications for neurotoxicity." (2011). Electronic Theses and Dissertations. Paper 1145. https://doi.org/10.18297/etd/1145 This Doctoral Dissertation is brought to you for free and open access by ThinkIR: The University of Louisville's Institutional Repository. It has been accepted for inclusion in Electronic Theses and Dissertations by an authorized administrator of ThinkIR: The University of Louisville's Institutional Repository. This title appears here courtesy of the author, who has retained all other copyrights. For more information, please contact [email protected]. ANNONACIN IN ASIMINA TRILOBA FRUIT: IMPLICATIONS FOR NEUROTOXICITY 8y Lisa Fryman Potts 8.S. Centre College, 2005 M.S. University of Louisville, 2010 A Dissertation Submitted to the Faculty of the School of Medicine at the University of Louisville in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Department of Anatomical Sciences and Neurobiology University of Louisville School of Medicine Louisville, Kentucky December 2011 Copyright 2011 by lisa Fryman Potts All rights reserved ANNONACIN IN ASIMINA TRILOBA FRUIT: IMPLICATIONS FOR NEUROTOXICITY By Lisa Fryman Potts B.S. Centre College, 2005 M.S. University of Louisville, 2010 A Dissertation Approved on July 21, 2011 by the following Dissertation Committee: Irene Litvan, M.D. Dissertation Director Frederick Luzzio, Ph.D. Michal Hetman, M.D., Ph.D. David Hein, Ph.d. Theo Hagg, Ph.D. Martha Bickford, Ph.D. ii DEDICATION This dissertation is dedicated to my parents Mr. Harry Fryman and Mrs. Linda Fryman and my husband Mr. Joseph Potts who have supported me throughout my academic career and life iii ACKNOWLEDGEMENTS I would like to thank my mentor, Dr. Irene Litvan for her guidance and support. I would also like to thank Dr. Frederick Luzzio and Dr. Michal Hetman for their support and mentorship on specific aspects of this research. I also thank my other committee members, Dr. David Hein, Dr. Theo Hagg and Dr. Martha Bickford for their support and guidance during my graduate career at the University of Louisville. I would also like to thank Dr. Pierre Champy for sample donation and consultation, Ms. Juan Chen and Dr. Bogdan Bogdanov for their technical assistance, as well as Mr. Scott Smith for his technical assistance and moral support. I would also like to express my appreciation to Dr. Samuel Weakly and Ms. Lydia B. Miller for their generosity in donating research funds that supported this project. iv ABSTRACT ANNONACIN IN ASIMINA TRILOBA FRUIT: IMPLICATIONS FOR NEUROTOXICITY Lisa F. Potts November 28, 2011 The acetogenin annonacin, from the tropical annonaceous plant Annona muricata, is a lipophilic, mitochondrial complex I inhibitor reported to be more toxic than rotenone to mesencephalic neurons. The temperate annonaceous plant Asimina tri/oba (pawpaw) is native to the Eastern United States and its products are available online. This study determined whether annonacin is in the pawpaw fruit pulp and whether it or the crude ethyl acetate (EtOAc) extract is toxic to cortical neurons and induces pathological changes in the microtubule associated protein tau. Pawpaw extract was prepared by pulp extraction with methanol and liquid- liquid partitioning with EtOAc. Annonacin was isolated from the crude EtOAc extract via column chromatography using a gradient solvent system of increasing polarity. Mass spectroscopy, nuclear magnetic resonance and infrared v spectroscopy were used to compare isolated material with synthetic annonacin and a natural annonacin sample. Toxicity of isolated annonacin and the total EtOAc extract were determined in primary rat cortical neurons using the MIT (3- (4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay. The effects of annonacin on tau phosphorylation were determined by immunocytochemistry and western blot analysis. The average concentration of annonacin in the fruit pulp was 0.07 ± 0.03 mg/g. Purified annonacin (30.07 !-Ig/ml) and crude EtOAc extract (47.96 !-I9/ml) reduced relative viability of cortical neurons by 50% 48 hours post treatment. Annonacin toxicity was enhanced in the presence of crude extract. Annonacin treatment resulted in a decrease in the neuronal specific marker microtubule associated protein 2 (MAP2) and tau immunoreactivity, and tau expression was decreased on western blot. In conclusion, Asimina triloba fruit contains a high concentration of annonacin, which is toxic to cortical neurons. Based on these results, annonacin acts to reduce overall levels of tau, though it remains elusive whether or not this is a direct or indirect effect of annonacin action. Crude fruit extract also induced neurotoxicity, highlighting the need for additional studies to determine the bioavailability after consumption and potential risks of neurodegeneration associated with chronic exposure to pawpaw products. vi TABLE OF CONTENTS PAGE ACKNOWLEDGMENTS ...................................................................... iv ABSTRACT ........................................................................................v LIST OF TABLES ...............................................................................ix LIST OF FIGURES ..............................................................................x INTRODUCTION ................................................................................. 1 MATERIALS AND METHODS ................................................................ .23 Extraction and Isolation ............................ , ....................................23 In vitro neurotoxicity .....................................................................27 RESULTS ..........................................................................................32 Extraction and Isolation ................................................................32 In vitro cortical neurotoxicity .......................................................... 55 Annonacin effect on tau ................................................................66 DiSCUSSiON ......................................................................................71 STRENGTHS AND LIMITATIONS ..........................................................81 vii CONCLUSIONS AND FUTURE CONSIDERATIONS ................................. 84 REFERENCES ................................................................................... 88 APPENDICES ... .................................................................................1 04 CURRICULUM ViTAE ......................................................................... 11 0 viii LIST OF TABLES TABLE PAGE 1. Bioactive annonaceous acetogenins ..............................................7 2. Neurotoxicity of relevant compounds ............................................. 19 3. Chemical structures and 1Hand 13C NMR data for Annonacin and Annonacin T etraacetate ............................................................ .45 4. Annonacin content of Asimina triloba vs. Annona muricata ................ 54 ix LIST OF FIGURES FIGURE PAGE 1. Asimina triloba (pawpaw) tree ......................................................... 2 2. Distribution of As. triloba in North America ........................................ .4 3. Annona muricata (soursop) tree ...................................................... 5 4. Soursop fruit. ...............................................................................9 5. Pawpaw fruit. ...............................................................................9 6. Structure of Annonacin .................................................................1 0 7. Relevant Complex-1 Inhibitors ....................................................... 15 8. Annonacin TLC ...........................................................................35 9. FTMS of annonacin ......................................................................36 10. 1H NMR of annonacin .................................................................43 11. Conversion of annonacin to annonacin tetra acetate derivative ........... .47 12. Annonacin and tetraacetate TLC .................................................. .48 x 13. FTMS of annonacin and annonacin-tetraacetate .............................. 50 14. 1H NMR of annonacin and annonacin-tetraacetate ........................... 51 15. FTIR of annonacin and annonacin-tetraacetate ................................53 16. Cortical neurons 48 hrs after AN treatment.. ...................................56 17. Time-response of MAP2 immunoreactivity in cortical neurons after annonacin treatment ....................................................................57 18. Tau immunoreactivity in cortical neurons after annonacin treatment. .... 59 19. Solvent tolerance of cortical neurons after 48 hrs .............................62 20. Cortical neurons 48 hrs after pawpaw extract treatments ...................64 21. Dose-responses of cortical neurons 48 hrs after pawpaw extract treatments .................................................................................65 22. Tau expression 4 hrs. after annonacin treatment. ............................. 67 23.
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