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Cytotoxic Alkaloids from Microcos Paniculata with Activity at Neuronal Nicotinic Receptors DISSERTATION Presented in Partial

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Cytotoxic Alkaloids from Microcos Paniculata with Activity at Neuronal Nicotinic Receptors DISSERTATION Presented in Partial Cytotoxic Alkaloids from Microcos paniculata with Activity at Neuronal Nicotinic Receptors DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy of the Graduate School of The Ohio State University By Patrick Colby Still Graduate Program in Pharmacy The Ohio State University 2013 Dissertation Committee: A. Douglas Kinghorn, Advisor Esperanza J. Carcache de Blanco Karl WerBovetz Edward J. Behrman Copyright by Patrick Colby Still 2013 Abstract Natural products have a long history of use as leads for drug discovery. The World Health Organization (WHO) estimates that in Africa for example, up to 80% of the population relies on plant-derived traditional medicines to help meet primary healthcare needs (WHO, 2002). In the area of cancer, of the 175 new chemical entities in the western drug market from the 1940s to 2010, 48.6% were a combination of unaltered natural products, semisynthetic natural product derivatives, or obtained by total synthesis inspired by a natural product skeleton (Newman and Cragg, 2012). The question of why secondary metabolites are Biosynthesized by organisms is still a topic of deBate. However, ecological research has suggested that these compounds play a role as defense agents and are used also in communication (Williams et al., 1989; Yi et al., 2003; Chen et al., 2009). This dissertation work emcompasses bioactive alkaloids from the plant Microcos paniculata collected in Vietnam. Microcos paniculata is a large shrub or small tree that grows in several countries in South and Southeast Asia. Three new piperidine alkaloids, microgrewiapines A-C, and a number of known compounds were isolated from cytotoxic fractions of the separate chloroform-soluble extracts of the stem bark, branches, and leaves of M. paniculata. Comprehensive structure elucidation techniques were used to elucidate and identify the structure of the new compounds. In addition, 1H -13C H2BC ii NMR spectroscopy and induced circular dichroism (ICD) were employed to confirm the structures of the known compounds maslinic acid and (-)-loliolide. A total synthesis of 2-methyl-3,6-(di-tert-Butyldimethylsilyl) piperidine was accomplished to investigate the structural requirements for biological activity. The isolated compounds exhiBited a range of cytotoxic potencies against the HT-29 human colon cancer cell line that was used to screen extracts, chromatographically purified fractions, and pure compounds. Structural similarities Between the isolated piperidine alkaloids and certain previously identified nicotinic receptor (nAChR) antagonists, along with growing evidence to support the involvement of nAChRs in various aspects of cancer, provided a rationale to examine the effects of the isolates on nAChRs (Egleton et al., 2008; Schuller, 2009; González-Cestari et al., 2009; Henderson et al., 2010). When evaluated for their effects on human 34 or 42 nAChRs, several of these compounds were shown to have antagonistic activity for both receptor subtypes. As a result of this dissertation work, Microcos paniculata was collected as a tropical plant in Vietnam in 2008, leading to pure compounds being characterized showing activity at the cellular and receptor levels. The cytotoxicity and nAChR modulatory activity of compounds isolated in this investigation represent the first time such bioactivies have been shown for the constituents of a plant in the genus Microcos. Contemporary structure elucidation techniques were used and a preliminary analysis of the structural features contributing to the bioactivity of the isolated compounds has been made. iii This dissertation is dedicated to my Dad, who from a young age instilled a desire in me to ask questions, and to look where I’m going, and not where I’ve been. iv Acknowledgments I would like to thank, first and foremost, my thesis dissertation advisor Dr. A. Douglas Kinghorn. Throughout my graduate work, he has cultivated in me a sense of scientific excellence and patience. His style and way of thinking represent a model for future challenges I will face as a scientist. I also wish to thank Dr. Li Pan. It was a great privilege to witness her keen ability to envision a natural product structure from the data presented in NMR spectra, and she is thanked for her patience in instilling that aBility within me. In addition, Dr. Esperanza J. Carcache de Blanco is thanked for her guidance and valued conversations about science and life, and for information on the mitochondrial memBrane potential assay. I also wish to thank Dr. James R. Fuchs for his guidance with the synthetic work contained in this thesis. His energy, encouragement and outstanding teaching aBility were inspirational. Dr. Karl WerBovetz and Dr. Edward Behrman are also thanked for taking the time to review this work, and for being a part of this dissertation committee. Microcos paniculata samples were collected in Vietnam under the terms of an agreement between the University of Illinois at Chicago (UIC) and the Institute of Ecology and Biological Resources (IEBR) of the Vietnam Academy of Science and Technology, Hanoi, Vietnam. I wish to thank Dr. Djaja Djendoel Soejarto (UIC) for v providing three parts of M. paniculata for this dissertation work, and for his enthusiastic and knowledgeable discussions about plant taxonomy. I am grateful to Mr. John Fowble and Dr. Craig McElroy, College of Pharmacy, The Ohio State University (OSU), and Dr. Chunhua Yuan, for many discussions and practical guidance on NMR spectroscopy, as well as Ms. Nan Kleinholz, Mr. Mark Apsega, and Dr. Kari Green-Church, Mass Spectrometry and Proteomics Facility, OSU for assisting with LC-MS dereplication and mass spectrometry. I am grateful to Dr. Heebyung Chai for HT-29 human colon cancer cell cytotoxicity testing, and the mutual satisfaction we shared after determining the main active compound of M. paniculata using bioactivity-guided fractionation. I also wish to thank Dr. Dennis McKay, Dr. Tatiana F. González-Cestari, and Ms. Bitna Yi, Division of Pharmacology, College of Pharmacy, OSU for their guidance in the use of pharmacological assays on nicotinic receptor subtypes and for their collaboration. Working in their laboratory broadened my scope of knowledge and took my isolated compounds to new heights. Emeritus Professor Dr. Popat Patil, Division of Pharmacology, College of Pharmacy, OSU is thanked for his inspiration and guidance throughout the pharmacological investigation. Sources of financial support for this dissertation work are gratefully acknowledged. These sources of support include the Raymond Doskotch Fellowship in Natural Products Chemistry (Division of Medicinal Chemistry and Pharmacognosy, College of Pharmacy, OSU; 2010-2011), grant P01CA125066 awarded to Dr. A. Douglas Kinghorn, from the National Cancer Institute, National Institutes of Health (NCI, NIH), vi Bethesda, Maryland (2007-2012), and an American Society of Pharmacognosy 2012 Student Travel Grant. I am privileged to have worked with many colleagues throughout this dissertation work who provided support each step of the way. In particular, I wish to thank Dr. Mark Bahar, Ms. Annecie Benetrehina, Ms. Lynette Bueno, Dr. Joshua Fletcher, Dr. Brandon Henderson, Dr. Nivedita Jena, Dr. Chenglong Li, Mr. Jie Li, Mr. Ben Naman, Mr. Pretiq Patel, Mr. Ryan Pavlovicz, Dr. Yulin Ren, and Mr. John Woodard. I also wish to acknowledge my family and closest friends for the encouragement and pride they have shown me. This dissertation work honors the scientific accomplishments of two family memBers, Both with their own achievements in the field of Pharmacognosy. James Still (1812-1885), one of my ancestors and a self-taught healer who travelled the New Jersey pinelands, and saw patients from across the Philadelphia region, practiced herbal medicine in the formative years of the United States of America. My cousin, the late Dr. Cecil C. Still, Department of Biochemistry and Microbiology, Cook College, Rutgers University, catalogued the medicinal plants of New Jersey and the Philadelphia region in his book, Botany and Healing. I cherish the personally signed copy of his book, and remember his pride in me for continuing in the family tradition of Pharmacognosy. I thank my grandmother, Mrs. Delores Hawkins, for teaching me aBout gardening, which formed the Basis of my appreciation for plant natural products. My good friends, Mr. Ryan P. Mouton and Mr. Julian Richard, are sincerely thanked for their endless encouragement, and helping me to recognize the best parts of myself. vii Vita EDUCATION 2003................................................................Colonial Forge High School, Stafford, Virginia 2007................................................................B.S. Chemistry, Cum Laude, Virginia Commonwealth University, Richmond, Virginia 2007-2013 ......................................................Ph.D. Student, College of Pharmacy, The Ohio State University, Columbus, Ohio HONORS AND AWARDS 1. David F. Ingraham Fellowship in Chemistry, Department of Chemistry, Virginia Commonwealth University, Richmond, Virginia, 2006. 2. Raymond W. Doskotch Fellowship in Natural Products Chemistry, College of Pharmacy, The Ohio State University, Columbus, Ohio, 2010. 3. American Chemical Society Certificate of Innovation, Graduate Student Summer Institute on Technology Development, Washington, DC, 2010. 4. The Mary Frances Picciano, Dietary Supplement Research Practicum, National Institutes of Health, Bethesda, Maryland, 2012. viii 5. American Society
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