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Acacia Honey and Chrysin Reduce Proliferation of Melanoma Cells Through Alterations in Cell Cycle Progression

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Acacia Honey and Chrysin Reduce Proliferation of Melanoma Cells Through Alterations in Cell Cycle Progression 973-981.qxd 19/8/2010 11:20 Ì ™ÂÏ›‰·973 INTERNATIONAL JOURNAL OF ONCOLOGY 37: 973-981, 2010 973 Acacia honey and chrysin reduce proliferation of melanoma cells through alterations in cell cycle progression ELENA PICHICHERO1, ROSELLA CICCONI2, MAURIZIO MATTEI2, MARCO GALLINELLA MUZI3 and ANTONELLA CANINI1 1Department of Biology, Honey Research Center, University of Rome ‘Tor Vergata’ Via della Ricerca Scientifica 1; 2Centro di Servizi Interdipartimentale Stazione per la Tecnologia Animale - STA University of Rome ‘Tor Vergata’, Via Montpellier 1; 3Department of Surgery, University Hospital Tor Vergata, Viale Oxford 81, I-00133 Rome, Italy Received February 25, 2010; Accepted April 28, 2010 DOI: 10.3892/ijo_00000748 Abstract. Honey has long been used in medicine for different category of ‘nutraceuticals’ or ‘therapeutic’ food. In fact it purposes. Only recently, however, its antioxidant property satisfies both the classical concept of ‘nutritionally adequate and preventive effects against different diseases, such as food’, which is a food that provides nutrients in sufficient cancer, have been highlighted. Chrysin (5,7-dihydroxyflavone) quantities to satisfy particular organic needs, and the concept is a natural flavone commonly found in acacia honey. It has of ‘optimal nutritional food’, which includes, besides the previously been shown to be an anti-tumor agent. In this above, potential of food to promote health, improve general study, we investigated the antiproliferative role of honey or well-being, and reduce the risk of developing certain illnesses chrysin on human (A375) and murine (B16-F1) melanoma (4,5). Honey has a long tradition of use in folk medicine for cell lines. The results of the 3-(4,5-Dimethylthiazol-2-yl)- various purposes and has been referred to extensively in the 2,5-diphenyl tetrazolium bromide (MTT) assay and the medical literature of Egypt, and Greece (6,7). Recent times trypan blue exclusion test showed that both the tested have seen a revival of interest in the medical properties of compounds were able to induce an antiproliferative effect on honey-bee products, because they are thought to exhibit a melanoma cells in a dose- and time-dependent manner. Flow broad spectrum of biological activities, including antibacterial, cytometry analysis indicated that cytotoxicity induced by antifungal, cytostatic, wound healing, antitumor and anti- honey or chrysin was mediated by G0/G1 cell cycle arrest and inflammatory effects (8-10). An important property of honey induction of hyperploid progression. Our results suggest that is its antioxidant capacity; this is mainly due to the presence the anti-proliferative effects of honey are due mainly to the of flavonoids and phenolic acids, although the exact action presence of chrysin. Chrysin may therefore be considered a mechanism is unknown. Among the mechanisms proposed are potential candidate for both cancer prevention and treatment. free radical sequestration, hydrogen donation, or a combination Further investigation is needed to validate the contribution of of these acting as substrates for radicals such as superoxide chrysin in tumor therapy in vivo. and hydroxyl (11-13). The antioxidant activity of honey is linked to the observed anticancer and antiatherosclerosis Introduction effects of honey. Until 1990, the chemopreventive action of honey was attributed to its hydrogen peroxide releasing Honey is the natural sweet substance produced by honeybees properties, through induction of cell apoptosis, although recent from nectar or from the secretion of living part of plants. It is finding point to a complementary role of the phytochemical composed of at least 300 compounds and is basically a antioxidant which can act either with or independently from solution supersatured in sugars, fructose and glucose being the the release of H2O2 (14,15). Chrysin (5,7-dihydroxyflavone) most important. In addition, there is a great variety of minor is a secondary metabolite of the class of flavones, this natural components, including phenolic acids and flavonoids, different compound is a marker of acacia honey because it represents enzymes, carotenoids, organic acids and proteins (1-3). Honey the largest fraction of flavonoids present in this unifloral may be considered a ‘functional’ food, also coming under the honey (16,17). Flavones are a subclass of flavonoids, these compounds being widely present in fruits, vegetables, bever- _________________________________________ ages, cereals and herbs. Many experiments have strongly demonstrated that flavones possess many useful properties Correspondence to: Dr Antonella Canini, Department of Biology, for human health care, these including enzymes inhibition Honey Research Center, University of Rome ‘Tor Vergata’, Via as well as anti-inflammatory, antioxidant, and cytotoxic della Ricerca Scientifica, 1-00133 Rome, Italy antitumor activity. Antioxidant scavenging activity is linked to E-mail: [email protected] the prevention of many chronic and age-dependent pathological conditions like cancer, diabetes, atherosclerosis, cataract and Key words: acacia honey, chrysin, hyperploid cells, melanoma chronic neurological conditions (18-21). Like other flavones, such as apigenin and luteolin, chrysin also shows benefical 973-981.qxd 19/8/2010 11:20 Ì ™ÂÏ›‰·974 974 PICHICHERO et al: EFFECTS OF ACACIA HONEY AND CHRYSIN ON MELANOMA CELLS effect on health. Chrysin has been shown to be a potent plates were incubated at 37˚C and 5% CO2 for 24, 48 and inhibitor of the enzyme aromatase (22), and to modulate 72 h. After treatment time, floating cells in the medium of GABAA and GABAC receptors (23). Chrysin also possesses each well were transferred to centrifuge tubes; adherent cells anti-inflammatory activity related to the the pro-inflammatory were washed with PBS, collected by trypsinization and mixed activities of COX-2 (24). It has been found to possess cancer with the corresponding floating cells before centrifugation. chemopreventive properties through inhibiting malignant cell Cells were stained with 0.4% of trypan blue and counted in growth, as well as inducing cell death and perturbing cell triplicate by optic microscope to estimate the number of live cycle progression (25-27). and dead cells. Cancer cells that grow uncontrollably, such as melanoma, are largely resistant to chemotherapy. One of the strategies Cell cycle analysis by FACS (fluorescence-activated cell of cancer management is to inhibit cell proliferation. Since sorting) analysis. B16 and A375 cell were seeded at density research in melanoma cancer therapy is focused on the of 2x104 cells/well in 24-well plates. After 24 h cells were discovery of novel drugs able to reduce melanomas pro- treated with honey or chrysin as previously described. After liferative capacity, in this study we have investigated the 24-, 48- and 72-h treatment and incubation at 37˚C and 5% antiproliferative activity of honey and chrysin in murine B16 CO2, cells were washed with PBS harvested with trypsin and human A375 melanoma cell lines. and cetrifuged. Cells were stained with propidium iodide (PI) soltion (50 μg/ml PI, 0.5% RNAse A and 0,1% Triton X-100) Materials and methods and incubated for 30 min at 4˚C in the dark. After this period of incubation cells were fixed with paraformaldehyde (PFA) 1% Materials. An acacia honey sample was obtained directly in PBS for 15 min. Cell cycle distribution was analyzed by flow from beekepers during the 2006-2007 harvest. The floral cytometry on a FACSCalibur (Becton-Dickinson, Mountain origin was specified by pollen analysis carried out in our View, CA). PI was excited at 488 nm, and fluorescence laboratory. Chrysin was purchased from Sigma (St. Louis, analyzed at 620 nm. A total of 10,000 events in each sample MO). The purity of Chrysin was about 96.0% (HPLC). was acquired. Using CellquestPro software, the percentages of cells at different phases of the cell cycle were determined. Cell cultures and treatments. A B16-F1 mouse melanoma cell line and a A375 human melanoma cell line were purchased Results from American Type Culture Collection. The cells were grown in RPMI-1640 medium supplemented with 10% (v/v) fetal Honey and chrysin reduces metabolic activity of melanoma bovine serum (FBS). 1% (v/v) L-glutamine, 100 U penicillin cells. In the first set of experiments, the anti-neoplastic activity and 100 μg/ml streptomycin at 37˚C in a humidified atmo- of honey or chrysin in melanoma cell lines was measured sphere with 5% CO2 and 95% air. The cells were passaged using MTT assay in basic culture conditions. All the doses of twice weekly. Acacia honey or chrysin were added to cells in honey used in this assay were able to induce a significant complete medium after 24 h of growth. Honey was diluted at reduction of metabolic activity of both melanoma cell lines. a final concentration of 0.01, 0.02, 0.025, 0.03, 0.05, 0.1 and The inhibitory effect was observed in a time- and dose- 0.2 g/ml, while chrysin was diluted in methanol at the final dependent manner (Fig. 1A and B). The estimated IC50 value concentration of 10, 25, and 50 μM. Cells were also treated was equal to about 0.02 g/ml of acacia honey for both human with a solution of sugar or with methanol as solvent control, and murine cell lines. Honey significantly reduced the for honey and chrysin treatments, respectively. metabolic activity of tested cells after only 24-h exposure time; in fact the intermediate doses inhibited cellular growth MTT assay. The effect on cell proliferation, of honey or of 50 and 40% in B16 and A375 cells, respectively. In B16-F1 chrysin, was measured using MTT colorimetric assay as cells the highest doses tested (0.2 and 0.1 g/ml) showed a described by Mosman (28). In breef, 2x104 cells/well, both cytotoxic effect on cells. Indeed, a reduction of metabolic human and murine melanoma cells, were grown in 96-well activity of >90% was observed after only 24-h treatment.
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