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1 Phytochemical and Biological Evaluation of Two Vietnamese Phytochemical and Biological Evaluation of Two Vietnamese Plants, Indigofera spicata and Millettia caerulea Dissertation 1 Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Lynette Bueno Pérez Graduate Program in Pharmacy The Ohio State University 2014 Dissertation Committee: A. Douglas Kinghorn, Advisor David M. Lucas Robert W. Brueggemeier 2 Copyright by Lynette Bueno Pérez 2014 Abstract Cancer continues to be a leading cause of death in the United States. Natural products obtained from plants have been the source of many approved anticancer drugs. This dissertation study is part of a multi-institutional collaborative program project entitled “Discovery of Anticancer Agents of Diverse Natural Origin”. The overall aim of ii this project is the discovery of new natural product anticancer lead compounds from aquatic cyanobacteria, filamentous fungi, and tropical plants. The work presented herein focuses on the discovery of new anticancer lead agents from tropical plants. Two tropical plants of the family Fabaceae (Indigofera spicata and Millettia caerulea), collected in Vietnam, were investigated as possible sources of anticancer lead compounds. Cytotoxicity-guided isolation of the chloroform extract of the combined flowers, fruits, leaves, and twigs of I. spicata resulted in the purification of four new flavanones (67, 71, 74, and 76) and six known compounds inclusive of three rotenoids (68, 70, and 73), two flavanones (69 and 72), and a chalcone (75), in addition to a semi-synthetic chalcone (77). Three cytotoxic compounds (68, 70, and 73) were identified with 50% inhibitory concentration (IC50) values of less than 10 µM. cis-(6aβ,12aβ)- Hydroxyrotenone (68) and rotenone (70) showed submicromolar activities against HT-29 and 697 cells. Compounds 68 and 70 were non-toxic to normal colon cells. Compound 68 was investigated in an in vivo hollow fiber assay. Nine (68, 70-77) out of ten compounds ii evaluated in a quinone reductase induction assay were active, each with a concentration required to double (CD) quinone reductase activity value of less than 10 µM. The new compound, (+)-5-methoxypurpurin (74), was identified as a possible lead agent for cancer chemoprevention, with a CD value of 0.2 µM and no cytoxicity to the host cells. Cytotoxicity-guided isolation of the chloroform extract of the fruits of M. caerulea resulted in the purification of one novel (143), two new (144-145), and eleven known rotenoids (68, 70, 73, 131-132, 135, 140-141, 146-148). The novel rotenoid, caeruleanone A (143), was found to contain an unprecedented arrangement of iii the D-ring and its structure was confirmed by single-crystal X-ray crystallographic analysis. As with I. spicata, cis-(6aβ,12aβ)-hydroxyrotenone (68) and rotenone (70) were isolated as the major cytotoxic components of the chloroform extract. The new compound, caeruleanone C (145), exhibited potent mitochondrial transmembrane potential (MTP) inhibition with an IC50 value of 0.07 µM, whereas deguelin (131) was active with an IC50 value of 3.3 µM. Also, tephrosin (73), showed nuclear factor kappa B (p65) inhibition with an IC50 value of 4.9 µM. Furthermore, seven (68, 70, 73, 141, 144- 145, and 148) out of thirteen compounds evaluated for quinone reductase induction activity displayed CD values of less than 10 µM. The new compounds, caeruleanone B (144) and C (145), showed potent activity with CD values of 0.9 and 1.0 µM, respectively, and exhibited no apparent cytoxicity to the host cells. In sum, investigation of I. spicata and M. caerulea collected in Vietnam, provided novel, new and active lead compounds for possible development to combat cancer. iii iv Dedication In honor and to the loving memory of my father, Cecilio Bueno Pintado (1945-2012). To my late grandmother, Paulita, who led a brave fight against thyroid cancer. iv Acknowledgments First of all, I want to express my most heartfelt and sincere gratitude to my advisor, Prof. A. Douglas Kinghorn for welcoming me in his laboratory, for his guidance, mentoring, encouragement and support in every step of my Ph.D. degree. Prof. Kinghorn was truly an exceptional advisor, and I will treasure in my continuing professional career v development his teachings in proper scientific writing and research excellence. Second, I want to express my deepest gratitude to Prof. David M. Lucas, who served as my co- advisor, provided very useful mentorship in biology research and allowed me to perform some biology experimental work in his laboratory, in addition to supplying constant support and encouragement. I also want to thank the members in Prof. Lucas laboratory, especially Dr. Sneha Gupta, Ms. Ellen Sass, Ms. Carolyn Cheney, and Mr. Ryan B. Edwards for training in cell culture techniques, the use of flow cytometry, and the MTT cytotoxicity, rhodamine and PI assays. Third, I want to express my profound gratitude to Prof. Robert W. Brueggemeier for being part of my dissertation committee, and to Profs. Karl A. Werbovetz and Tom Li, as members of my candidacy committee. I want to express my deepest thanks to Dr. Judith C. Gallucci of the Department of Chemistry and Biochemistry (OSU) for the X-ray diffraction analysis and to Prof. Steven M. Swanson and Mr. Daniel D. Lantvit at the Department of Medicinal Chemistry and Pharmacognosy (UIC) for the in vivo hollow fiber assay evaluation. Many thanks are v expressed to Dr. Chunhua Yuan for the 800 MHz NMR analysis. My most sincere thanks to Mr. Mark Apsega at the Mass Spectrometry & Proteomics Facility in the Biological Research Tower (OSU) for training in HRMS instrumental analysis. I also want to thank Prof. Esperanza Carcache de Blanco and Dr. Ulyana Muñoz Acuña for MTP and NF-κB testing, and to Dr. Hee-Byung Chai for HT-29 cytotoxicity evaluation. In addition, I thank Dr. Chai for teaching me some cell culture techniques and the SRB cytotoxicity assay. I thank also Dr. Jie Li for training and help with the quinone reductase induction assay. Special thanks go to Dr. Li Pan, from whom I learned most of what I now know vi about isolation, structure elucidation, use of the NMR instrumentations, and other analytical instrumentation used in this research, and for providing me with the essential skills and knowledge necessary to be self-sufficient and successful in phytochemical research. I wish to express my most profound gratitude to Prof. Djaja D. Soejarto at the Department of Medicinal Chemistry and Pharmacognosy (UIC) and Prof. Tran Ngoc Ninh at the Institute of Ecology and Biological Resources, Vietnamese Academy of Science and Technology (Vietnam) for the plant collections and taxonomic identifications. I also thank Prof. Soejarto for providing very nice photographs of the plants under study and for all his useful feedback during the writing of my papers. Thanks are expressed to the Director of Nui Chua National Park in Vietnam for permission to collect the plants. vi I also want to thank the past and present instrumentation directors at the College of Pharmacy (OSU), Mr. Jack Fowble and Dr. Craig McElroy, for maintainance of NMR spectrometers, polarimeters, UV and IR spectrometers used in the present study. My most sincere and deepest thanks to past and present colleagues and friends in Prof. Kinghorn’s group, Drs. Ah-Reum Han, Jie Li, Joshua N. Fletcher, Li Pan, Mark Bahar, Patrick Still, Ye Deng, Yong Soo Kwon, Yulin Ren, and Ms. Annecie Benatrehina, Mr. Ben Naman and Mr. Mathew Rogman. I am deeply grateful for the finantial support received for this dissertation study vii and during my Ph.D. degree. The main source of finantial funding was the program project grant P01 CA125066, awarded to Prof. Kinghorn from the U.S. National Cancer Institute (NCI), National Institutes of Health (NIH), Bethesda, MD. Other fundings received were from the Chemistry-Biology Interface Program (CBIP) Pre-doctoral Fellowship, supported by NIH (grant T32 GM008512), The Ohio State University (2009- 2011), and the Raymond W. Doskotch Fellowship in Natural Products Chemistry from the College of Pharmacy, The Ohio State University (2013-2014). Other financial fundings acknowledged are teaching and research assistanships, as well as from the Journal of Natural Products, sponsored by the American Society of Pharmacognosy, as part of my journal Administrator Assistant duties (2012-2014). In addition, I will like to give my most sincere thanks to my M.S. thesis advisor, Prof. Mikhail D. Antoun, Department of Medicinal Chemistry and Pharmacognosy, School of Pharmacy, (UPR-MSC) for encouraging me to continue graduate studies in vii natural products research and for his recommendation that led to me becoming part of Prof. Kinghorn’s group and a graduate student at The Ohio State University. Finally, but not least importantly, I want to express my deepest thanks and appreciation to my family and friends. First of all, to my parents, Lynette Pérez López and Cecilio Bueno Pintado, who installed in me, from an early age, to always strive for excellence, to work hard and to be responsibile, and for their unconditional love and support. To the rest of my family, especially my aunt and uncle, Inés and Yeyi, for always cheering me on, and celebrating my success. To all my friends in Columbus, who viii became my family away from home, and to those friends who remained in Puerto Rico, for their love, outstanding support and encouragement. viii Vita 1996................................................................Dorado Academy, High School, Dorado, Puerto Rico 2000................................................................B.S. Industrial Microbiology, University of Puerto Rico, Mayagüez Campus, Mayagüez ix 2008................................................................M.S. Pharmaceutical Sciences, University of Puerto Rico, Medical Sciences Campus, San Juan 2008-2014 .....................................................Ph.D. Graduate Student, Division of Medicinal Chemistry and Pharmacognosy, The Ohio State University Publications 1. Bueno Pérez, L.; Pan, L.; Muñoz Acuña, U.; Li, J.; Chai, H.-B.; Gallucci, J.
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