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226141109.Pdf STUDIES ON TRITERPENE SAPONINS FROM Saponaria vaccaria SEED AND THEIR APOPTOSIS-INDUCING EFFECT ON HUMAN CANCER CELL LINES A Thesis Submitted to the College of Graduate Studies and Research in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Department of Pharmacology University of Saskatchewan Saskatoon By Irving Javier Ramirez-Erosa © Copyright Irving J. Ramirez-Erosa, March 2008. All rights reserved. The University of Saskatchewan claims copyright in conjunction with the author. Use shall not be made of the material contained herein without proper acknowledgement. PERMISSION TO USE In presenting this dissertation in partial fulfillment of the requirements for a Postgraduate degree from the University of Saskatchewan, I agree that the Libraries of this University may make it freely available for inspection. I further agree that permission for copying of this dissertation in any manner, in whole or in part, for scholarly purposes may be granted by the professor or professors who supervised my dissertation work or, in their absence, by the Head of the Department or the Dean of the College in which my thesis work was done. It is understood that any copying or publication or use of this dissertation or parts thereof for financial gain shall not be allowed without my written permission. It is also understood that due recognition shall be given to me and to the University of Saskatchewan in any scholarly use which may be made of any material in my dissertation. DISCLAIMER Reference in this dissertation to any specific commercial products, process, or service by trade name, trademark, manufacturer, or otherwise, does not constitute or imply its endorsement, recommendation, or favoring by the University of Saskatchewan. The views and opinions of the author expressed herein do not state or reflect those of the University of Saskatchewan, and shall not be used for advertising or product endorsement purposes. Requests for permission to copy or to make other uses of materials in this dissertation in whole or part should be addressed to: Head of the Department of Pharmacology University of Saskatchewan A120 Health Sciences Building 107 Wiggins Road Saskatoon, Saskatchewan S7N 5E5 Canada OR Dean College of Graduate Studies and Research University of Saskatchewan 107 Administration Place Saskatoon, Saskatchewan S7N 5A2 Canada i TO GOD He chose to bring me and my wife to this university in the middle of the Canadian prairies. He has used our lives and the lives of others around us to teach us to grow, to be open, and to learn to walk the line between cultures, deeply enjoying both sides. All glory and honor to Him. TO MY DEAR AND EVERLOVING WIFE, CLAUDIA, AND CHILDREN, ERIC AND DIEGO This work is for, and because of you and all the generations to come. It is dedicated to all our journeys in learning to thrive. TO MY MOTHER LIZBETH AND PARENTS IN-LAW ROGER AND FLOR Thank you for loving us and showing us how to live in an ever changing world while keeping our values unchanged. TO ALL MY FAMILY AND FRIENDS For their invaluable support throughout all these years. TO THOSE WHO BELIEVE IN THEMSELVES ii ACKNOWLEDGEMENTS This collaborative project between the Department of Pharmacology, University of Saskatchewan, and the National Research Council of Canada - Plant Biotechnology Institute, would not have been successful without the support of a number of people from both institutions and to whom I am greatly indebted. To my supervisors Dr. Robert (Bob) Hickie (U of S) and Dr. John Balsevich (NRC-PBI) for their encouragement, comments, guidance, support, patience and criticism throughout the entire course of this investigation. Their help will always be deeply appreciated. To the members of my thesis advisory committee, Dr. Lily Wu, Dr. John Tuchek, Dr. Rob Warrington, Dr. Jonathan Dimmock, Dr. Bob McNeill and Dr. V. Gopal, for their help, criticism and suggestions. To Ms. Donna Dunlop for all her invaluable technical assistance, hard work and contributions to the success of this investigation. It has always been a pleasure working with you. To the Faculty members and staff of the Department of Pharmacology for making me feel like a part of ‘one big family’. Your patience, time and dedication in my transition from chemistry to pharmacology will always be treasured. To Ms. Donna Dodge, Ms. Cindy Wruck and Mr. Bob Wilcox for their support in all aspects during my time in the Department of Pharmacology. All my gratitude goes to you. To Mr. Greg Bishop and Mrs. Leah Deibert from the NRC-PBI‘s Plant Natural Products group for all their help in the analytical chemistry and cytotoxic studies of this thesis. Their friendship is also highly appreciated. iii To Dr. Patrick Covello and the members of the Plant Natural Products research team at the NRC-PBI for all their support and advice. It has been a pleasure working with you all. To Dr. Sue Abrams from the Signalling and Plant Metabolism Group of the NRC-PBI for all her help throughout these years, but especially for having introduced me to Dr. John Balsevich. To Dr. Kutty Kartha, Dr. Wilf Keller and all the people from the NRC-PBI who contributed and that continue contributing to the success of my scientific career. Thank you so much for believing in my research. To the Cancer Research Centre of the Royal University Hospital for technical assistance and their contribution of the cancer cell lines used in this study. To the Department of Pharmacology (U of S) for a Teaching and a Research Assistantship; as well as to the Government of Saskatchewan through the Agriculture Development Fund, and the Maunders McNeil Foundation of Calgary for financial support. I wish to thank Dr. John T. Arnason for accepting the role of the external advisor. My experience at the University would not have been a good one without the company of friends with whom I could share opinions, ideas, frustrations and complicity and have a good time. To all of them, big thanks. I would also like to thank Dr. Paul Arnison, Dr. Michael Oelk, Dr. Nienke Lindeboom, Mrs. Jane Fiala and all my colleagues from work at Saponin Inc. for their support in the final stage of this thesis. iv Loving thanks to all my friends in Saskatoon; my family-friends. You know who you are. I love you and treasure every minute of your company. To my music buddies. Music is food for the soul. Let’s keep on playin’! I am also very grateful to my friends from the Hispanic Catholic Community of Saskatoon for their emotional support and guidance. To my loving family, Claudia, Eric and Diego. For their unconditional love. v ABSTRACT Medicinal plants have provided important advances in the treatment of numerous diseases and many plant-derived drugs are currently in use or under investigation for the treatment of many ailments including cancer. A phytochemical analysis of the methanol extract from the seed of Saponaria vaccaria L. cultivated in Saskatchewan was performed which resulted in the detection of several bisdesmosidic saponins. A high-performance liquid chromatographic method using photodiode array and single quadrupole electrospray mass detection for analysis and profiling was developed. Due to their structural similarities, purification of bisdesmosidic saponins was challenging. However, monodesmosidic saponin Vaccaroside B and cyclopeptides Segetalin A, Segetalin B, and a new cyclopeptide, segetalin I [whose structure was proposed to be cyclo(Gly1-Pro2-Tyr3-Tyr4-Pro5-Phe6)], were purified employing various chromatographic techniques such as HPLC, VLC, PTLC). Crude methanol extracts of S. vaccaria seed were evaluated for cytotoxic activity using the methyl-thiazol-tetrazolium non-radioactive cell proliferation assay (MTT assay). Various concentrations of the extract (2-50 μg/mL) were tested against a series of four human cancer cell lines (WiDr, colon; MDA-MB-231, breast; NCI-417, lung and PC-3, prostate). The human foreskin (BJ)-derived normal human fibroblast cell line CRL-2522 was included as a non-cancerous control. Results showed that cytotoxic activities from the seed extract were greater than commercially available Quillaja saponaria saponin. vi The human cancer cell lines were also exposed to fractions containing high titers of saponins as well as semi-purified saponins (ca. 80%). All bisdesmosidic saponins and fractions thereof showed cytotoxicity against the cell lines studied. The effect was particularly strong in breast and prostate cancer cell lines with IC50 values in the range 1–4 μg/mL. Monodesmosidic saponins, phenolics and cyclopeptides did not show activity even at the highest concentration (50 μg/mL) tested in this study. Chemical modifications of the saponin structures resulted in an overall decrease in activity, but an increase in selectivity in comparison to CRL-2522. Time and concentration-dependent studies using the nuclear stains propidium iodide and Hoechst 33342, demonstrated that the stimulation of apoptosis was the mechanism of cytotoxic action. When breast and prostate cell lines were exposed to small amounts (4-7 μM) of bisdesmosidic saponins Segetalin H (MW 1448) and Segetalin I (MW 1464), it was observed that apoptosis was induced at an early incubation time (4-10 h). Activation of caspases and changes in membrane potential were determined by flow cytometry. As a result of this study, we propose that triterpene bisdesmosidic saponins from the seed of Saponaria vaccaria L. represent a new type of drug having potential antitumor/anticancer activity due to their ability to induce apoptosis
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