The Chemopreventive Effect of the Dietary Compound Kaempferol on the MCF-7 Human Breast Cancer Cell Line Is Dependent on Inhibition of Glucose Cellular Uptake

REFERENCES

• Ban KA and Godellas CV: Epidemiology of breast cancer. Surg Oncol Clin N Am 23, 409–422, 2014.
   PubMed Web of Science ®Google Scholar
• DeSantis C, Ma J, Bryan L, and Jemal A: Breast cancer statistics, 2013. CA Cancer J Clin 64, 52–62, 2014.
   PubMed Web of Science ®Google Scholar
• Baena Ruiz R and Salinas Hernández P: Diet and cancer: risk factors and epidemiological evidence. Maturitas 77, 202–208, 2014.
   PubMed Web of Science ®Google Scholar
• Yeon JY, Suh YJ, Kim SW, Baik HW, Sung CJ, et al.: Evaluation of dietary factors in relation to the biomarkers of oxidative stress and inflammation in breast cancer risk. Nutr 27, 912–918, 2011.
   PubMed Web of Science ®Google Scholar
• Szablewski L: Expression of glucose transporters in cancers. Biochim Biophys Acta 1835, 164–169, 2012.
   Google Scholar
• López-Lázaro M: The warburg effect: why and how do cancer cells activate glycolysis in the presence of oxygen? Anticancer Agents Med Chem 8, 205–312, 2008.
   PubMed Web of Science ®Google Scholar
• Hanahan D and Weinberg R: The hallmarks of Cancer. Cell 144, 646–674, 2011.
   PubMed Web of Science ®Google Scholar
• Macheda ML, Rogers S, and Best JD: Molecular and cellular regulation of glucose transporters (GLUT) proteins in cancer. J Cell Physiol 202, 654–662, 2005.
   PubMed Web of Science ®Google Scholar
• Rodríguez-Enríquez S, Marín-Hernández A, Gallardo-Pérez JC, Carreño-Fuentes L, and Moreno-Sánchez R. Targeting of cancer energy metabolism. Mol Nutr Food Res 53, 29–48, 2009.
   PubMed Web of Science ®Google Scholar
• Pinheiro C, Sousa B, Albergaria A, Paredes J, Dufloth R, et al.: GLUT1 and CAIX expression profiles in breast cancer correlate with adverse prognostic factors and MCT1 overexpression. Histol Histopathol 26, 1279–1286, 2001.
   Google Scholar
• Krzeslak A, Wojcik-Krowiranda K, Forma E, Jozwiak P, Romanowicz H, et al.: Expression of GLUT1 and GLUT3 glucose transporters in endometrial and breast cancers. Pathol Oncol Res 18, 721–728, 2012
   PubMed Web of Science ®Google Scholar
• Furuta E, Okuda H, Kobayashi A, and Watabe K: Metabolic genes in cancer: their roles in tumor progression and clinical implications. Biochim Biophys Acta 1805, 141–152, 2010.
   Google Scholar
• Tennant DA, Durán RV, and Gottlieb E: Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 10, 267–277, 2010.
   PubMed Web of Science ®Google Scholar
• Heiden M: Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov 10, 671–684, 2011.
   PubMed Web of Science ®Google Scholar
• Manach C, Scalbert A, Morand C, Rémésy C, and Jiménez L. Polyphenols: food sources and bioavailability. Am J Clin Nutr 79, 727–747, 2004.
   PubMed Web of Science ®Google Scholar
• Nichenametla SN, Taruscio TG, Barney DL, and Exon JH. A review of the effects and mechanisms of polyphenolics in cancer. Crit Rev Food Sci Nutr 46, 161–183, 2006.
   PubMed Web of Science ®Google Scholar
• Wang J and Jiang YF: Natural compounds as anticancer agents: experimental evidence. World J Exp Med 20, 45–57, 2012.
   Google Scholar
• Lambert JD, Hong J, Yang GY, Liao J, and Yang CS: Inhibition of carcinogenesis by polyphenols: evidence from laboratory investigations. Am J Clin Nutr 81, 284–291, 2005.
   PubMed Web of Science ®Google Scholar
• Moreira L, Araújo I, Costa T, Correia-Branco A, Faria A, et al.: Quercetin and epigallocatechin gallate inhibit glucose uptake and metabolism by breast cancer cells by an estrogen receptor-independent mechanism. Exp Cell Res 319, 1784–1795, 2013.
   PubMed Web of Science ®Google Scholar
• Araújo JR, Gonçalves P, and Martel F. Chemopreventive effect of dietary polyphenols in colorectal cancer cell lines. Nutr Res 31, 77–87, 2011.
   PubMed Web of Science ®Google Scholar
• Araújo JR, Pereira AC, Correia-Branco A, Keating E, and Martel F: Oxidative stress induced by tert-butylhydroperoxide interferes with the placental transport of glucose: In vitro studies with BeWo cells. Eur J Pharmacol 720, 218–226, 2013.
   PubMed Web of Science ®Google Scholar
• Bergmeyer HU and Bernt E: Lactate dehydrogenase. In: Methods of Enzymatic Analysis, 2nd ed., ed. Bergmeyer HU (ed.). New York: Academic Press, 1974, pp. 574–579.
   Google Scholar
• Bradford M: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254, 1976.
   PubMed Web of Science ®Google Scholar
• Muzyka A, Radionov M, Novikov A, Moskalenko E, Vysotsky A, et al.: GraphPad Prism from Windows. Version 5.03, 2013.
   Google Scholar
• Wright EM, Martín MG, and Turk E. Intestinal absorption in health and disease-sugars. Best Pract Res Clin Gastroenterol 17, 943–956, 2013.
   Web of Science ®Google Scholar
• Dwarakanath B: Cytotoxicity, radiosensitization, and chemosensitization of tumor cells by 2-deoxy-D-glucose in vitro. J Cancer Res Ther 5(Suppl 1), S27–S31, 2009.
   PubMed Web of Science ®Google Scholar
• Shiomi K, Kuriyama I, Yoshida H, and Mizushina Y. Inhibitory effects of myricetin on mammalian DNA polymerase, topoisomerase and human cancer cell proliferation. Food Chem 139, 910–918, 2013.
   PubMed Web of Science ®Google Scholar
• Chen A and Chen Y: A review of the dietary flavonoid, kaempferol on human health and cancer chemopreventio. Food Chem 138, 2099–2107, 2013.
   PubMed Web of Science ®Google Scholar
• Stapel J, Oppermann C, Richter DU, Ruth W and Briese V. Polyphenol compounds with anti-carcinogenic qualities: Effects of quercetin (flavonol), chrysin (flavon), kaempferol (flavanol), naringenin (flavanon) and hesperidin (flavanoid) on in vitro breast cancer. J Med Plants Res 7, 2187–2196, 2013.
   Google Scholar
• Li Y, Chen H, Hardy TM, and Tollefsbol TO. Epigenetic regulation of multiple tumor-related genes leads to suppression of breast tumorigenesis by dietary genistein. PLoS One 8, 1–12, 2013.
   Web of Science ®Google Scholar
• Monteiro R, Calhau C, Silva AO, Pinheiro-Silva S, Guerreiro S, et al.: Xanthohumol inhibits inflammatory factor production and angiogenesis in breast cancer xenografts. J Cell Biochem 104, 1699–1707, 2008.
   PubMed Web of Science ®Google Scholar
• Su D, Cheng Y, Liu M, Liu D, Cui H, et al.: Comparision of piceid and resveratrol in antioxidation and antiproliferation Activities In Vitro. PLoS One 8, 1–13, 2013.
   Web of Science ®Google Scholar
• Kao J, Salari K, Bocanegra M, Choi Y, Girard L, et al.: Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 4, e6146, 2009.
   Google Scholar
• Filomeni G, Desideri E, Cardaci S, Graziani I, Piccirillo S, et al.: Carcinoma cells activate AMP-activated protein kinase-dependent autophagy as survival response to kaempferol-mediated energetic impairment. Autophagy 6, 202–216, 2010.
   PubMed Web of Science ®Google Scholar
• Klip A and Paquet M: Glucose Transport and glucose transporters in muscle and their metabolic regulation. Diabetes Care 13, 228–243, 1990.
   PubMed Web of Science ®Google Scholar
• Loike JD, Hickman S, Kuang K, Xu M, Cao L, et al.: Sodium-glucose cotransporters display sodium- and phlorizin-dependent water permeability. Am J Physiol 271, 1774–1779, 1996.
   Web of Science ®Google Scholar
• Martin HJ, Kornmann F, and Fuhrmann GF: The inhibitory effects of flavonoids and antiestrogens on the Glut1 transporter in human erythrocytes. Chem Biol Interact 146, 225–235, 2003.
   PubMed Web of Science ®Google Scholar
• Vera JC, Reyes AM, Velásquez FV, Rivas CI, Zhang RH, Strobel P, et al.: Direct inhibition of the hexose transporter GLUT1 by tyrosine kinase inhibitors. Biochemistry 40, 777–790, 2001.
   PubMed Web of Science ®Google Scholar
• Strobel P, Allard C, Perez-Acle T, Calderon R, Aldunate R, et al.: Myricetin, quercetin and catechin-gallate inhibit glucose uptake in isolated rat adipocytes. Biochem J 386, 471–478, 2005.
   PubMed Web of Science ®Google Scholar
• Kwon O, Eck P, Chen S, Corpe CP, Lee JH, et al.: Inhibition of the intestinal glucose transporter GLUT2 by flavonoids. FASEB J 21, 366–377, 2007.
   PubMed Web of Science ®Google Scholar
• Johnston K, Sharp P, Clifford M, and Morgan L. Dietary polyphenols decrease glucose uptake by human intestinal Caco-2 cells. FEBS Lett 579, 1653–1657, 2005.
   PubMed Web of Science ®Google Scholar
• Wright DC, Geiger PC, Han DH, and Holloszy JO: Are tyrosine kinases involved in mediating contraction-stimulated muscle glucose transport?. Am J Physiol Endocrinol Metab 290, 123–128, 2006.
   Web of Science ®Google Scholar
• Nomura M, Takahashi T, Nagata N, Tsutsumi K, Kobayashi S, et al.: Inhibitory mechanisms of flavonoids on insulin-stimulated glucose uptake in MC3T3-G2/PA6 adipose Cells. Biol Pharm Bull 31, 1403–1409, 2008.
   PubMed Web of Science ®Google Scholar
• Park JB: Flavonoids are potential inhibitors of glucose uptake in U937 cells. Biochem Biophys Res Commun 260, 568–574, 1999.
   PubMed Web of Science ®Google Scholar
• Jung KH, Lee JH, Thien Quach CH, Paik JY, Oh H, et al.: Resveratrol suppresses cancer cell glucose uptake by targeting reactive oxygen species-mediated hypoxia-inducible factor-1α activation. J Nucl Med 54, 2161–2167, 2013.
   PubMed Web of Science ®Google Scholar
• Fang XK, Gao J, and Zhu DN: Kaempferol and quercetin isolated from Euonymus alatus improve glucose uptake of 3T3-L1 cells without adipogenesis activity. Life Sci 82, 615–622, 2008.
   PubMed Web of Science ®Google Scholar
• Calderón-Montaño JM, Burgos-Morón E, Pérez-Guerrero C, and López-Lázaro M: A review on the dietary flavonoid kaempferol. Mini Rev Med Chem 11, 298–344, 2011.
   PubMed Web of Science ®Google Scholar
• Lee KM, Lee DE, Seo SK, Hwang MK, Heo YS, et al.: Phosphatidylinositol 3-kinase, a novel target molecule for the inhibitory effects of kaempferol on neoplastic cell transformation. Carcinogenesis 31, 1338–1343, 2010.
   PubMed Web of Science ®Google Scholar
• Luo H, Rankin GO, Li Z, Depriest L, and Chen YC: Kaempferol induces apoptosis in ovarian cancer cells through activating p53 in the intrinsic pathway. Food Chem 128, 513–519, 2011.
   PubMed Web of Science ®Google Scholar
• Choi E and Ahn W: Kaempferol induced the apoptosis via cell cycle arrest in human breast cancer MDA-MB-453 cells. Nutr Res Pract 2, 322–325, 2008.
   PubMedGoogle Scholar
• Luo H, Rankin GO, Juliano N, Jiang B, and Chen YC: Kaempferol inhibits VEGF expression and in vitro angiogenesis through a novel ERK-NFjBcMyc- p21 pathway. Food Chem 130, 321–328, 2012.
   PubMed Web of Science ®Google Scholar
• Luo H, Jiang B, Li B, Li Z, Jiang BH, et al.: Kaempferol nanoparticles achieve strong and selective inhibition of ovarian cancer cell viability. Int J Nanomedicine 7, 3951–3959, 2012.
   PubMed Web of Science ®Google Scholar
• Lee S, Kim YJ, Kwon S, Lee Y, Choi SY, et al.: Inhibitory effects of flavonoids on TNF-a-induced IL-8 gene expression in HEK 293 cells. BMB Rep 42, 265–270, 2009.
   PubMed Web of Science ®Google Scholar
• Ulrich CM, Bigler J, and Potter JD: Non-steroidal anti-inflammatory drugs for cancer prevention: promise, perils and pharmacogenetics. Nat Rev Cancer 6, 130–140, 2006.
   PubMed Web of Science ®Google Scholar
• Phromnoi K, Yodkeeree S, Anuchapreeda S, and Limtrakul P: Inhibition of MMP-3 activity and invasion of the MDA-MB-231 human invasive breast carcinoma cell line by bioflavonoids. Acta Pharmacol Sin 30, 1169–1176, 2009.
   PubMed Web of Science ®Google Scholar
• Chinnam N, Dadi PK, Sabri SA, Ahmad M, Kabir MA, et al.: Dietary bioflavonoids inhibit Escherichia coli ATP synthase in a differential manner. Int J Biol Macromol 46, 478–486, 2010.
   PubMed Web of Science ®Google Scholar
• Huang WW, Chiu YJ, Fan MJ, Lu HF, Yeh HF, et al.: Kaempferol induced apoptosis via endoplasmic reticulum stress and mitochondria-dependent pathway in human osteosarcoma U-2 OS cells. Mol Nutr Food Res 54, 1585–1595, 2010.
   PubMed Web of Science ®Google Scholar
• Brusselmans K, Vrolix R, Verhoeven G, and Swinnen JV. Induction of cancer cell apoptosis by flavonoids is associated with their ability to inhibit fatty acid synthase activity. J Biol Chem 280, 5636–5645, 2005.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Chen AY, Li M, Chen C, and Yao Q. Ginkgo biloba extract kaempferol inhibits cell proliferation and induces apoptosis in pancreatic cancer cells. J Surg Res 148, 17–23, 2008.
   PubMed Web of Science ®Google Scholar
• Wang Q and Morris M: Flavonoids modulate monocarboxylate transporter-1-mediated transport of gamma-hydroxybutyrate in vitro and in vivo. Drug Metab Dispos 35, 201–208, 2007.
   PubMed Web of Science ®Google Scholar
• Schulze A and Harris AL: How cancer metabolism is tuned for proliferation and vulnerable to disruption. Nature 491, 364–373, 2012.
   PubMed Web of Science ®Google Scholar
• Webb BA, Chimenti M, Jacobson MP, and Barber DL: Dysregulated pH: a perfect storm for cancer progression. Nat Rev Cancer 11, 671–677, 2011.
   PubMed Web of Science ®Google Scholar
• Sonveaux P, Végran F, Schroeder T, Wergin MC, Verrax J, et al.: Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice J Clin Invest 118, 3930–3942, 2008.
   PubMed Web of Science ®Google Scholar
• Mathupala SP, Colen CB, Parajuli P, and Sloan AE: Lactate and malignant tumors: a therapeutic target at the end stage of glycolysis. J Bioenerg Biomembr 39, 73–77, 2007.
   PubMed Web of Science ®Google Scholar
• Morais-Santos F, Miranda-Gonçalves V, Pinheiro S, Vieira AF, Paredes J, et al.: Differential sensitivities to lactate transport inhibitors of breast cancer cell lines. Endocr Relat Cancer 21, 27–38, 2014.
   PubMed Web of Science ®Google Scholar
• Feron O: Pyruvate into lactate and back: from the Warburg effect to symbiotic energy fuel exchange in cancer cells. Radiother Oncol 92, 329–333, 2009.
   PubMed Web of Science ®Google Scholar