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Discovery of Anticancer Agents of Diverse Natural Origin By Discovery of Anticancer Agents of Diverse Natural Origin By: Douglas Kinghorn, Esperanza J. Carcache De Blanco, David M. Lucas, H. Liva Rakotondraibe, Jimmy Orjala, D. Doel Soejarto, Nicholas H. Oberlies, Cedric J. Pearce, Mansukh C. Wani, Brent R. Stockwell, Joanna E. Burdette, Steven M. Swanson, James R. Fuchs, Mitchell A. Phelps, Lihui Xu, Xiaoli Zhang, and Young Yongchun Shen “Discovery of Anticancer Agents of Diverse Natural Origin.” Douglas Kinghorn, Esperanza J. Carcache De Blanco, David M. Lucas, H. Liva Rakotondraibe, Jimmy Orjala, D. Doel Soejarto, Nicholas H. Oberlies, Cedric J. Pearce, Mansukh C. Wani, Brent R. Stockwell, Joanna E. Burdette, Steven M. Swanson, James R. Fuchs, Mitchell A. Phelps, Lihui Xu, Xiaoli Zhang, and Young Yongchun Shen. Anticancer Research, 2016, 36 (11), 5623-5637. Made available courtesy of the International Institute of Anticancer Research: http://ar.iiarjournals.org/content/36/11/5623 ***© 2016 International Institute of Anticancer Research. Reprinted with permission. No further reproduction is authorized without written permission from International Institute of Anticancer Research. *** Abstract: Recent progress is described in an ongoing collaborative multidisciplinary research project directed towards the purification, structural characterization, chemical modification, and biological evaluation of new potential natural product anticancer agents obtained from a diverse group of organisms, comprising tropical plants, aquatic and terrestrial cyanobacteria, and filamentous fungi. Information is provided on how these organisms are collected and processed. The types of bioassays are indicated in which initial extracts, chromatographic fractions, and purified isolated compounds of these acquisitions are tested. Several promising biologically active lead compounds from each major organism class investigated are described, and these may be seen to be representative of a very wide chemical diversity. Keywords: Natural products | tropical plants | cyanobacteria | fungi | potential anticancer activity | review Article: ***Note: Full text of article below ANTICANCER RESEARCH 36 : 5623-5638 (2016) doi:10.21873/anticanres.11146 Review Discovery of Anticancer Agents of Diverse Natural Origin A. DOUGLAS KINGHORN 1,2 , ESPERANZA J. CARCACHE DE BLANCO 1, DAVID M. LUCAS 2,3 , H. LIVA RAKOTONDRAIBE 1, JIMMY ORJALA 4, D. DOEL SOEJARTO 4,5 , NICHOLAS H. OBERLIES 6, CEDRIC J. PEARCE 7, MANSUKH C. WANI 8, BRENT R. STOCKWELL 9,10 , JOANNA E. BURDETTE 4, STEVEN M. SWANSON 11 , JAMES R. FUCHS 1, MITCHELL A. PHELPS 1,2 , LIHUI XU 2, XIAOLI ZHANG 2,3 and YOUNG YONGCHUN SHEN 12 1College of Pharmacy, 2Comprehensive Cancer Center, and 3College of Medicine, The Ohio State University, Columbus, OH, U.S.A.; 4College of Pharmacy, University of Illinois at Chicago, Chicago, IL, U.S.A.; 5Field Museum of Natural History, Chicago, IL, U.S.A.; 6Department of Chemistry and Biochemistry, University of North Carolina at Greensboro, Greensboro, NC, U.S.A.; 7Mycosynthetix, Inc., Hillsborough, NC, U.S.A.; 8Research Triangle Institute, Research Triangle Park, NC, U.S.A.; Departments of 9Biological Sciences and 10 Department of Chemistry, Columbia University, New York, NY, U.S.A.; 11 School of Pharmacy, University of Wisconsin-Madison, Madison, WI, U.S.A.; 12 Eisai Inc., Andover, MA, U.S.A. Abstract. Recent progress is described in an ongoing Despite recent improvements in survival rates due to collaborative multidisciplinary research project directed advances in early detection and the quality of treatment towards the purification, structural characterization, available, cancer remains a major public health hazard in chemical modification, and biological evaluation of new countries all over the world (1, 2). For example, in the case potential natural product anticancer agents obtained from a of the United States in 2016, nearly 1.7 million new cases of diverse group of organisms, comprising tropical plants, cancer are predicted to occur, in addition to over 595,000 aquatic and terrestrial cyanobacteria, and filamentous fungi. cancer deaths (1). The three most common types of cancer in Information is provided on how these organisms are females in the U.S. are those of the breast, uterine corpus, and collected and processed. The types of bioassays are indicated colon and rectum, while those of males are prostate, colon in which initial extracts, chromatographic fractions, and and rectum, and melanoma (2). Unfortunately, death rates are purified isolated compounds of these acquisitions are tested. increasing for cancer of the liver, pancreas, and uterine corpus Several promising biologically active lead compounds from (1). In the People’s Republic of China, with a much larger each major organism class investigated are described, and population than the U.S., nearly three million cancer deaths these may be seen to be representative of a very wide were projected to occur in 2015, with lung cancer being the chemical diversity. major cause, and stomach, esophageal and liver cancer also commonly occurring (3). Natural products have played a major beneficial role in cancer chemotherapy for over 50 years, both in terms of providing established drugs and new lead compounds for Τhis article is freely accessible online. synthetic optimization, and in furnishing substances for probing cellular and molecular mechanisms of action relevant to cancer Correspondence to: A. Douglas Kinghorn, Ph.D., D.Sc., Division inhibition (4-6). Thus, out of a total of 175 small-molecule of Medicinal Chemistry and Pharmacognosy, College of Pharmacy, anticancer drugs introduced into therapy in Western countries The Ohio State University, Columbus, OH 43210, U.S.A. Tel. +1 6142478094, Fax: +1 6142478119, e-mail [email protected] over an approximately 70-year period, about 49% were either obtained from organisms directly or were derived from natural Key Words: Natural products, tropical plants, cyanobacteria, fungi, products (5). Currently, a considerable number of natural potential anticancer activity, review. products of terrestrial microbial origin are used in cancer 0250-7005/2016 $2.00+.40 5623 ANTICANCER RESEARCH 36 : 5623-5638 (2016) chemotherapy, including actinomycin D, several anthracycline In this review, recent progress in an ongoing multi- derivatives (inclusive of daunorubicin, doxorubicin, epirubicin, institutional collaborative project funded by the U.S. National idarubicin, and valrubicin), bleomycin, actinomycin D, Cancer Institute (NCI), National Institutes of Health (NIH), mitomycin C, and mitoxantrone HCl (4). In turn, four main Bethesda, MD, USA will be described. This research program classes of higher plant-derived anticancer agents are used is funded through the ‘Program Project’ (P01) mechanism and clinically in the U.S. and Europe, namely, the vinca has been reviewed previously (17, 18). Currently, there are (Catharanthus ) bisindole alkaloids (vinblastine, vincristine, three primary academic groups involved: The Ohio State vinorelbine, vinflunine), the semi-synthetic epipodophyllotoxins University (OSU), the University of Illinois at Chicago (etoposide, teniposide, and etoposide phosphate), the taxanes (UIC), and the University of North Carolina at Greensboro (paclitaxel and paclitaxel albumin-stabilized nanoparticule UNCG), with the participation of a fungus biotechnology formulation, docetaxel, cabizitaxel), and the camptothecin company, Mycosynthetix, Inc. (Hillsborough, NC, USA) and derivatives (irinotecan and topotecan) (4). In the last few years, a pharmaceutical company (Eisai Inc., Andover, MA, USA). the first small-molecule anticancer agents of marine origin have Several other senior investigators in the project team are been introduced into the market, including trabectedin (ET-743), based at other academic institutions and a private non-profit a partially synthesized version of a marine tunicate constituent research institute. The overall administration of the program (a DNA-binding agent via an effect on transcription; for soft project is as previously published, with focus being on the tissue sarcoma) (6, 7). Also included in this category are isolation, structural characterization, and biological evaluation eribulin mesylate, a synthetic derivative of the marine polyether of lead anticancer compounds from tropical plants, freshwater macrolide, halichondrin B (an inhibitor of microtubule and terrestrial cyanobacteria, and filamentous fungi (17). In dynamics; for metastatic breast cancer) (5, 6, 8), and the following paragraphs, the potential of each of these three brentuximab vedotin, a conjugate of an antibody–marine major types of organisms is mentioned. compound derivative (a binding agent to CD30 cells that As indicated above, plants (of both temperate and tropical interacts with tubulin; for Hodgkin’s lymphoma and anaplastic origin) have already afforded several clinically used large-cell lymphoma) (5, 6, 9). Additional recently approved oncological agents, and are a proven resource for further natural product anticancer agents are romidepsin, from a soil research in anticancer drug discovery. In addition to various bacterium (a histone deacetylase inhibitor; for T-cell lymphoma) camptothecin, podophyllotoxin, taxane, and vinblastine (6, 10), and the terrestrial microbial semi-synthetic derivatives derivatives, compounds based on other structural types of ixabepilone (a microtubulin inhibitor; for locally advanced and plant-derived secondary metabolites are currently in clinical metastatic breast cancer) and temsirolimus
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