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Preclinical and Clinical Studies ANTICANCER RESEARCH 24: 2783-2840 (2004) Review Role of Resveratrol in Prevention and Therapy of Cancer: Preclinical and Clinical Studies BHARAT B. AGGARWAL1, ANJANA BHARDWAJ1, RISHI S. AGGARWAL1, NAVINDRA P. SEERAM2, SHISHIR SHISHODIA1 and YASUNARI TAKADA1 1Cytokine Research Laboratory, Department of Bioimmunotherapy, The University of Texas M. D. Anderson Cancer Center, Box 143, 1515 Holcombe Boulevard, Houston, Texas 77030; 2UCLA Center for Human Nutrition, David Geffen School of Medicine, 900 Veteran Avenue, Los Angeles, CA 90095-1742, U.S.A. Abstract. Resveratrol, trans-3,5,4'-trihydroxystilbene, was first and cervical carcinoma. The growth-inhibitory effects of isolated in 1940 as a constituent of the roots of white hellebore resveratrol are mediated through cell-cycle arrest; up- (Veratrum grandiflorum O. Loes), but has since been found regulation of p21Cip1/WAF1, p53 and Bax; down-regulation of in various plants, including grapes, berries and peanuts. survivin, cyclin D1, cyclin E, Bcl-2, Bcl-xL and cIAPs; and Besides cardioprotective effects, resveratrol exhibits anticancer activation of caspases. Resveratrol has been shown to suppress properties, as suggested by its ability to suppress proliferation the activation of several transcription factors, including NF- of a wide variety of tumor cells, including lymphoid and Î B, AP-1 and Egr-1; to inhibit protein kinases including IÎ B· myeloid cancers; multiple myeloma; cancers of the breast, kinase, JNK, MAPK, Akt, PKC, PKD and casein kinase II; prostate, stomach, colon, pancreas, and thyroid; melanoma; and to down-regulate products of genes such as COX-2, head and neck squamous cell carcinoma; ovarian carcinoma; 5-LOX, VEGF, IL-1, IL-6, IL-8, AR and PSA. These Correspondence to: Bharat B. Aggarwal, Cytokine Research growth factor receptor; HUVEC, human umbilical vein endothelial Laboratory, Department of Bioimmunotherapy, The University of cells; 8-OHdG, 8-hydroxydeoxyguanosine; TBARS, thiobarbituric acid- Texas M. D. Anderson Cancer Center, Box 143, 1515 Holcombe reactive substances; AAPH, 2,2'-azobis-(2-amidinopropane) Boulevard, Houston, Texas 77030, U.S.A. Tel: 713-792-3503/6459, dihydrochloride; IC50, concentration causing 50% inhibition; ICV, Fax: 713-794-1613, e-mail: [email protected] intracerebroventricular; STZ, streptozotocin; HMG, half-mustard gas; LLC, Lewis lung carcinoma; VEGF, vascular endothelial growth factor; Key Words: Resveratrol, cell signaling, chemoprevention, metastasis, BHA, butylated hydroxyanisole; ICAM, intracellular adhesion transformation, invasion, tumorigenesis, apoptosis, review. molecule; VCAM, vascular cell adhesion molecule; MMP, matrix metalloproteinase; IL, interleukin; PARP, poly(ADP-ribose) Abbreviations: TNF, tumor necrosis factor; NF-Î B, nuclear factor kappa polymerase; Egr, early growth response gene; ER, estrogen receptor; B; PKC, protein kinase C; UV, ultraviolet; NOS, nitric oxide synthase; CYP, cytochrome P450; IFN, interferon; NSAID, nonsteroidal anti- COX, cyclooxygenase; PMA, phorbol myristate acetate; LDL, low- inflammatory drug; H2O2, hydrogen peroxide; Cdk; cyclin-dependent density lipoprotein; PBMC, peripheral blood mononuclear cells; PMN, kinases; PDGF, platelet-derived growth factor; PSA, prostate-specific human polymorphonuclear leukocytes; GSH, reduced glutathione; AP-1, antigen; ACF, aberrant crypt foci; Ach, acetylcholine; MDA, activator protein-1; MAPK, mitogen-activated protein kinase; ERK, malondialdehyde; SHRSP, stroke-prone hypertensive rats; Ïmax, extracellular signal-regulated kinase; TGF, transforming growth factor; wavelength maxima; HPLC, high-pressure (performance) liquid PKA, protein kinase A; DMBA, 7,12-dimethylbenzoic acid; B[a]P, chromatography; MS, mass spectrometric; CoA, coenzyme A; NO, benzo[·]pyrene; BPDE, B[a]P diol epoxides; AhR, aryl hydrocarbon nitric oxide; AIF, apoptosis-inducing factor; AML, acute myeloid receptor; PhiP, 2-amino1-methyl-6-phenylimidazo[4,5-b]pyridine; AOM, leukemia; DISC, death-inducing signal complex; AR, androgen azoxymethane; NNK, 4-(methyl-nitrososamine)-1-(3-pyridyl)-1-butanone; receptor; ALL, acute lymphocytic leukemia; Rb, retinoblastoma; SPT, ODC, ornithine decarboxylase; B-CLL, B-cell chronic lymphocytic serine palmitoyltransferase; PDE, phosphodiesterase; AZT, leukemia; CTL, cytotoxic T lymphocyte; NQO, NAD(P)H quinone zidovudine; ddC, zalcitabine; ddI, didanosine; PKD, protein kinase D; oxidoreductase; HMG-CoA, 3-hydroxy-3-methylglutaryl coenzyme A; LPS, lipopolysaccharide; PI3K, phosphoinositide 3-kinase; TRAIL, SBP, systolic blood pressure; EWP, extract of wine phenolics ; SMC, tumor necrosis factor-related apoptosis-inducing ligand; FADD, Fas- smooth muscle cells; ROS, reactive oxygen species; EGFR, epidermal associated death domain. 0250-7005/2004 $2.00+.40 2783 ANTICANCER RESEARCH 24: 2783-2840 (2004) activities account for the suppression of angiogenesis by this C1h. Suppression of NO/NOS by resveratrol stilbene. Resveratrol also has been shown to potentiate the C1i. Suppression of growth factor protein tyrosine kinases apoptotic effects of cytokines (e.g., TRAIL), chemotherapeutic by resveratrol agents and Á-radiation. Phamacokinetic studies revealed that C1j. Suppression of COX-2 and lipooxygenase by the target organs of resveratrol are liver and kidney, where it is resveratrol concentrated after absorption and is mainly converted to a C1k. Suppression of cell-cycle proteins by resveratrol sulfated form and a glucuronide conjugate. In vivo, resveratrol C1l. Suppression of adhesion molecules by resveratrol blocks the multistep process of carcinogenesis at various C1m. Suppression of androgen receptors by resveratrol stages: it blocks carcinogen activation by inhibiting aryl C1n. Suppression of PSA by resveratrol hydrocarbon-induced CYP1A1 expression and activity, and C1o. Suppression of inflammatory cytokine expression by suppresses tumor initiation, promotion and progression. resveratrol Besides chemopreventive effects, resveratrol appears to exhibit C1p. Suppression of angiogenesis, invasion and metastasis therapeutic effects against cancer. Limited data in humans by resveratrol have revealed that resveratrol is pharmacologically quite safe. C1q. Effect of resveratrol on bone cells Currently, structural analogues of resveratrol with improved C1r. Effects of resveratrol on expression of cytochrome bioavailability are being pursued as potential therapeutic p450 and metabolism of carcinogens agents for cancer. C1s. Suppression of inflammation by resveratrol C1t. Antioxidant effects of resveratrol Contents C1u. Suppression of transformation by resveratrol C1v. Induction of cellular differentiation by resveratrol Introduction C1w. Estrogenic/antiestrogenic effects of resveratrol A. Source of resveratrol C1x. Effect of resveratrol on normal cells B. Chemistry of resveratrol C1y. Suppression of mutagenesis by resveratrol C. Preclinical Studies C1z. Radioprotective and radiosensitive effect of resveratrol C1. In vitro effects C1aa. Chemosensitization by resveratrol C1a. Antiproliferative effects of resveratrol C1ab. Direct targets of resveratrol B-cell lymphoma C1ac. Immunomodulatory effects of resveratrol T-cell lymphoma C1ad. Modulation of gene expression by resveratrol Myeloid leukemia C2. In vivo animal studies of resveratrol Breast cancer C2a. Metabolism, pharmacokinetics, tissue distribution and Colon cancer clearance of resveratrol Pancreatic cancer C2b. Chemopreventive effects of resveratrol in animals Gastric cancer C2c. Antitumor effects of resveratrol in animals Prostate cancer D. Clinical studies with resveratrol Melanoma Lung cancer Conclusion Liver cancer Thyroid and head and neck cancers References Ovarian and endometrial tumors C1b. Resveratrol induces apoptosis Introduction Fas/CD95 pathway Mitochondrial pathway The history of resveratrol can be traced back thousands of Rb-E2F/DP pathway years. Perhaps the first known use of grape extracts for p53 activation pathway human health can be dated over 2000 years ago, to Ceramide activation pathway "darakchasava", a well-known Indian herbal preparation of Tubulin polymerization pathway which the main ingredient is Vitis vinifera L. This Adenylyl-cyclase pathway "Ayurvedic" medicine is prescribed as a cardiotonic and also C1c. Suppression of NF-Î B activation by resveratrol given for other disorders (1). The use of dried grapes (also C1d. Suppression of AP-1 by resveratrol called manakka) as a cardiotonic is well documented. High- C1e. Suppression of Egr-1 by resveratrol performance liquid choromatography (HPLC) analysis of C1f. Suppression of mitogen-activated protein kinases by darakchasava revealed polyphenols such as resveratrol and resveratrol pterostilbene. This age-old formulation became interesting C1g. Suppression of protein kinases by resveratrol in the light of recently acquired knowledge on resveratrol. 2784 Aggarwal et al: Resveratrol Inhibits Tumorigenesis Figure 1. Sources of resveratrol from different plants. Resveratrol (3,5,4’-trihydroxystilbene) is a naturally synthase gene from grapevine, transferred it into tobacco, occurring phytoalexin produced by a wide variety of plants, and found that regenerated tobacco plants containing this such as grapes (Vitis vinifera), peanuts (Arachis hypogea), gene are more resistant to infection by Botrytis cinerea (2). and mulberries in response to stress, injury, ultraviolet (UV) Resveratrol was first identified in 1940 as a constituent of irradiation, and fungal (e.g., Botrytis cinerea) infection. the roots of white hellebore
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