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Anthracene-Induced Mammary Carcinogenesis in Rats by Resveratrol: Role of Nuclear Factor-␬B, Cyclooxygenase 2, and Matrix Metalloprotease 9

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Anthracene-Induced Mammary Carcinogenesis in Rats by Resveratrol: Role of Nuclear Factor-␬B, Cyclooxygenase 2, and Matrix Metalloprotease 9 [CANCER RESEARCH 62, 4945–4954, September 1, 2002] Suppression of 7,12-Dimethylbenz(a)anthracene-induced Mammary Carcinogenesis in Rats by Resveratrol: Role of Nuclear Factor-␬B, Cyclooxygenase 2, and Matrix Metalloprotease 9 Sanjeev Banerjee, Carlos Bueso-Ramos, and Bharat B. Aggarwal1 Cytokine Research Laboratory, Departments of Bioimmunotherapy [S. B., B. B. A.] and Pathology [C. B-R.], The University of Texas M. D. Anderson Cancer Center, Houston, Texas 77030 ABSTRACT a role in reducing the risk of coronary heart disease and cancer (6–8). In addition, resveratrol intake has been reported to have anti-inflam- ؅ We have reported recently that resveratrol (trans-3,4 ,5-trihydroxystil- matory and anti-atherosclerosis functions and to modulate hepatic bene), a polyphenolic phytoalexin found in grapes, fruits, and root extracts alipoprotein and lipid synthesis, platelet aggregation, and production of the weed Polygonum cuspidatum, is a potent inhibitor of nuclear factor (NF)-␬B activation. Because NF-␬B suppression has been linked with of antiatherogenic eicosanoids by human platelets and neutrophils (7, chemoprevention, this prompted us to investigate the chemopreventive 9–11). Resveratrol has also been reported to inhibit the development potential of resveratrol by testing it against mammary carcinogenesis of preneoplastic lesions in carcinogen-treated mouse mammary organ induced by 7,12-dimethylbenz(a)anthracene (DMBA) in female Sprague cultures and the promotional stage of mouse skin carcinogenesis (7). Dawley rats. Dietary administration of resveratrol (10 ppm) had no effect Additionally, it mediates reduced aberrant colonic crypt foci forma- on body weight gain and tumor volume but produced striking reductions tion and inhibits of the growth of a wide variety of human-derived in the incidence (45%; P < 0.05), multiplicity (55%; P < 0.001), and tumor cells, including leukemic, prostate, breast, and endothelial cells extended latency period of tumor development relative to DMBA-treated (12–19). Other targeted cellular effects belonging to resveratrol in- animals. Histopathological analysis of the tumors revealed that DMBA induced ductal carcinomas and focal microinvasion in situ (7 of 7), volve inhibition of the enzymes protein kinase C, ribonucleotide whereas treatment with resveratrol suppressed DMBA-induced ductal reductase, cyclooxygenase, and nitric oxide synthase and inhibition of carcinoma. Immunohistochemistry and Western blot analysis revealed aryl hydrocarbon-induced cytochrome P-450 IAI (20–25). that resveratrol suppressed the DMBA-induced cyclooxygenase-2 and A close structural similarity exists between synthetic estrogen (4,4Ј- matrix metalloprotease-9 expression in the breast tumor. Gel shift analysis dihydroxy-trans-␣,␤-diethylstilbene) and resveratrol. It is unclear, showed suppression of DMBA-induced NF-␬B activation by resveratrol. however, whether resveratrol is an estrogen receptor agonist or an- Treatment of human breast cancer MCF-7 cells with resveratrol also tagonist. Estrogen agonists have been reported to exert protective suppressed the NF-␬B activation and inhibited proliferation at S-G -M 2 action against estrogen-dependent cancers, such as cancer of the phase. Overall, our results suggest that resveratrol suppresses DMBA- breast and endometrium; presumably, resveratrol interacts with estro- induced mammary carcinogenesis, which correlates with down-regulation of NF-␬B, cyclooxygenase-2, and matrix metalloprotease-9 expression. gen receptor to inhibit its activation (26). Lu and Serrano (26) reported that resveratrol acts as an estrogen receptor antagonist in the presence of estrogen, leading to inhibition of growth of human breast cancer INTRODUCTION cells. ␬ 2 Almost 600,000 new cases of breast cancer are identified each year In recent years, the importance of the transcription factor NF- B ␬ worldwide. In North America, breast cancer accounts for over one in promoting tumorigenesis has been well recognized. NF- B binds to quarter of all cancers in women and is second only to lung cancer as consensus elements within the promoter regions of a variety of tar- a cause of cancer-related deaths (1). Despite abundant information geted genes (27). Further investigations have revealed that the expres- ␬ about its etiopathogenesis and early detection, effective therapeutic sion of a multitude of critical genes are regulated by NF- B, including modalities for patients with advanced stages of the disease are still immunoreceptors, transcription factor-associated proteins (c-myc and needed. Adjuvant therapy after ablative surgery is effective only when p53), cell adhesion molecules (intracellular adhesion molecule, vas- the tumor is detected early. Accumulating evidence derived from cular cell adhesion molecule 1, and endothelial leukocyte adhesion laboratory studies and study cohorts drawn from the general popula- molecule 1), and enzymes involved in tumor metastasis (COX-2, tion have led to the search for “chemoprotection” agents to attenuate inducible nitric oxide synthase, and MMP-9). Under normal condi- ␬ the risk of breast cancer based on observation that most human tions, NF- B is retained in the cytoplasm of cells, where it is bound ␬ cancers are associated with a long period of latency (2, 3). Several by inhibitory proteins known as I Bs. It has also been documented nonnutritive phytochemicals found in natural products and associated that during carcinogenesis, NF-␬B has the potentiality to mediate with pharmacological attributes reveal evidence that they inhibit, several of the events associated with multistep processes including delay, and/or reverse cancer evoked by either environmental insults acquisition of features such as promotion of cell survival and dys- and/or lifestyle (4, 5). Several of these chemopreventive agents act at regulation of normal control of proliferation, metastasis, and angio- the initiation, promotion, and/or progression stages conceptually as- genesis (27–29). The constitutive activity of NF-␬B has been shown sociated with the ontogeny of multistage carcinogenesis. to be essential for proliferation of several cell types, e.g., smooth Resveratrol (3,4Ј-trihydroxystilbene), a natural phytoalexin present muscle cells and hepatocytes during liver regeneration after partial in grapes and many other natural sources, has been suggested to play hepatectomy or toxic damage (30, 31). Previous reports from our laboratory and another have demon- ␬ Received 3/26/02; accepted 7/1/02. strated the ability of resveratrol to down-regulate NF- B expression in The costs of publication of this article were defrayed in part by the payment of page vitro (32, 33), leading to speculation that it would in turn inhibit charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. 1 To whom requests for reprints should be addressed, at Department of Bioimmuno- 2 The abbreviations used are: NF-␬B, nuclear factor ␬B; TNF, tumor necrosis factor; therapy, The University of Texas M. D. Anderson Cancer Center, Box 143, 1515 Hol- I␬B, inhibitory subunit of NF-␬B; EMSA, electrophoretic mobility shift assay; MTT, combe Boulevard, Houston, TX 77030. Phone: (713) 792-3503, 6459; Fax: (713) 794- 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide; COX, cyclooxygenase; 1613; E-mail: [email protected]. DMBA, 7,12-dimethylbenz(a)anthracene; MMP, matrix metalloprotease. 4945 Downloaded from cancerres.aacrjournals.org on September 30, 2021. © 2002 American Association for Cancer Research. RESVERATROL BLOCKS MAMMARY CARCINOGENESIS cellular genes regulated by NF-␬B and those involved in multistage belonging to group III were treated with resveratrol (100 ␮g/rat) in the diet. tumorigenesis. In the present study, we evaluated the effect of res- The dose of resveratrol was computed based on average food intake, which veratrol in inhibiting chemically induced mammary carcinogenesis in approximated 12–15 g/rat/day. Resveratrol was dissolved in 70% ethanol and a rat model. This is the first report to indicate that resveratrol has a then added into the diet 1 day in advance and left at room temperature for 1 chemopreventive effect on breast tumorigenesis in vivo. Given the day. After ethanol evaporation, food was then given to the rats. Food cups were changed two times a week. progressive aberrant expression of constitutive NF-␬B factor with Chemoprevention Study Design. Rats belonging to the appropriate ex- progression of the disease (34), we hypothesize that resveratrol inter- perimental group were given the chemopreventive agent beginning at day 45 ␬ feres with cognate signaling by inhibiting of NF- B activity during of age. One week later (day 0), rats belonging to groups II and III were given the mammary tumorigenesis cascade. We therefore used immunohis- 10 mg of DMBA by gavage in sesame oil. This dose of DMBA is suboptimal tochemical and Western blot methods to examine the expression of to produce sufficient tumors to allow evaluation of both reduction and increase two enzymes, COX-2 and MMP-9, both of whose promoter sequences in the end point of carcinogenicity. Rats were weighed weekly, palpated for contain binding sites for NF-␬B. Additionally, we investigated the mammary tumors once/week (starting 4 weeks after DMBA treatment), and effect of resveratrol on NF-␬B activation and cell growth in MCF-7 monitored daily for signs of toxicity. The study was terminated at 120 days breast adenocarcinoma cells. after DMBA
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