Soy Isoflavone Genistein-Mediated Downregulation of miR-155 Contributes to the Anticancer Effects of Genistein

References

• Lampe JW, Nishino Y, Ray RM, Wu C, Li W, et al.: Plasma isoflavones and fibrocystic breast conditions and breast cancer among women in Shanghai, China. Cancer Epidemiol.Biomarkers Prev 16, 2579–2586, 2007.
   PubMed Web of Science ®Google Scholar
• Goodman MT, Shvetsov YB, Wilkens LR, Franke AA, Le ML, et al.: Urinary phytoestrogen excretion and postmenopausal breast cancer risk: the multiethnic cohort study. Cancer Prev Res (Phila) 2, 887–894, 2009.
   PubMed Web of Science ®Google Scholar
• Constantinou AI, Lantvit D, Hawthorne M, Xu X, van Breemen RB, et al.: Chemopreventive effects of soy protein and purified soy isoflavones on DMBA-induced mammary tumors in female Sprague-Dawley rats. Nutr Cancer 41, 75–81, 2001.
   PubMed Web of Science ®Google Scholar
• Hilakivi-Clarke L, Andrade JE, and Helferich W: Is soy consumption good or bad for the breast? J Nutr 140, 2326S–2334S, 2010.
   PubMed Web of Science ®Google Scholar
• Khan SA, Chatterton RT, Michel N, Bryk M, Lee O, et al.: Soy Isoflavone supplementation for breast cancer risk reduction: a randomized Phase II trial. Cancer Prev.Res.(Phila) 5, 309–319, 2012.
   PubMed Web of Science ®Google Scholar
• Taylor CK, Levy RM, Elliott JC, and Burnett BP: The effect of genistein aglycone on cancer and cancer risk: a review of in vitro, preclinical, and clinical studies. Nutr Rev 67, 398–415, 2009.
   PubMed Web of Science ®Google Scholar
• Cederroth CR and Nef S: Soy, phytoestrogens and metabolism: A review. Mol Cell Endocrinol 304, 30–42, 2009.
   PubMed Web of Science ®Google Scholar
• Okabe Y, Shimazu T, and Tanimoto H: Higher bioavailability of isoflavones after a single ingestion of aglycone-rich fermented soybeans compared with glucoside-rich non-fermented soybeans in Japanese postmenopausal wome. J Sci Food Agric 91, 658–663, 2011.
   PubMed Web of Science ®Google Scholar
• Adlercreutz H, Markkanen H, and Watanabe S: Plasma concentrations of phyto-oestrogens in Japanese men. Lancet 342, 1209–1210, 1993.
   PubMed Web of Science ®Google Scholar
• Chau MN, El Touny LH, Jagadeesh S, and Banerjee PP: Physiologically achievable concentrations of genistein enhance telomerase activity in prostate cancer cells via the activation of STAT3. Carcinogenesis 28, 2282–2290, 2007.
   PubMed Web of Science ®Google Scholar
• Messina M: A brief historical overview of the past two decades of soy and isoflavone research. J Nutr 140, 1350S–1354S, 2010.
   PubMed Web of Science ®Google Scholar
• van Duursen MB, Nijmeijer SM, de Morree ES, de Jong PC, and van den BM: Genistein induces breast cancer-associated aromatase and stimulates estrogen-dependent tumor cell growth in in vitro breast cancer model. Toxicology 289, 67–73, 2011.
   PubMed Web of Science ®Google Scholar
• Du M, Yang X, Hartman JA, Cooke PS, Doerge DR, et al.: Low-dose dietary genistein negates the therapeutic effect of tamoxifen in athymic nude mice. Carcinogenesis 33, 895–901, 2012.
   PubMed Web of Science ®Google Scholar
• Martinez-Montemayor MM, Otero-Franqui E, Martinez J, De LM-P, Cubano LA, et al.: Individual and combined soy isoflavones exert differential effects on metastatic cancer progression. Clin Exp Metastasis 27, 465–480, 2010.
   PubMed Web of Science ®Google Scholar
• Whitsett TG, Jr. and Lamartinier CA.: Genistein and resveratrol: mammary cancer chemoprevention and mechanisms of action in the rat. Expert Rev Anticancer Ther 6, 1699–1706, 2006.
   PubMed Web of Science ®Google Scholar
• Pavese JM, Farmer RL, and Bergan RC: Inhibition of cancer cell invasion and metastasis by genistein. Cancer Metastasis Rev 29, 465–482, 2010.
   PubMed Web of Science ®Google Scholar
• Farina HG, Pomies M, Alonso DF, and Gomez DE: Antitumor and antiangiogenic activity of soy isoflavone genistein in mouse models of melanoma and breast cancer. Oncol Rep 16, 885–891, 2006.
   PubMed Web of Science ®Google Scholar
• Zava DT and Duwe G: Estrogenic and antiproliferative properties of genistein and other flavonoids in human breast cancer cells in vitro. Nutr Cancer 27, 31–40, 1997.
   PubMed Web of Science ®Google Scholar
• Messina M, Watanabe S, and Setchell KD: Report on the 8th International Symposium on the Role of Soy in Health Promotion and Chronic Disease Prevention and Treatment. J Nutr 139, 796S–802S, 2009.
   PubMed Web of Science ®Google Scholar
• Kikuno N, Shiina H, Urakami, S, Kawamoto K, Hirata H, et al.: Genistein mediated histone acetylation and demethylation activates tumor suppressor genes in prostate cancer cells. Int J Cancer 123, 552–560, 2008.
   PubMed Web of Science ®Google Scholar
• Rahal OM and Simmen RC: PTEN and p53 cross-regulation induced by soy isoflavone genistein promotes mammary epithelial cell cycle arrest and lobuloalveolar differentiation. Carcinogenesis 31, 1491–1500, 2010.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Wang CZ, Du GJ, Qi LW, Calway T, et al.: Genistein induces G2/M cell cycle arrest and apoptosis via ATM/p53-dependent pathway in human colon cancer cells. Int J Oncol 43, 289–296, 2013.
   PubMed Web of Science ®Google Scholar
• Privat M, Aubel C, Arnould S, Communal Y, Ferrara M, et al.: AKT and p21 WAF1/CIP1 as potential genistein targets in BRCA1-mutant human breast cancer cell lines. Anticancer Res 30, 2049–2054, 2010.
   PubMed Web of Science ®Google Scholar
• Pan H, Zhou W, He W, Liu X, Ding Q, et al.: Genistein inhibits MDA-MB-231 triple-negative breast cancer cell growth by inhibiting NF-kappaB activity via the Notch-1 pathway. Int J Mol Med 30, 337–343, 2012.
   PubMed Web of Science ®Google Scholar
• Rajah TT, Peine KJ, Du N, Serret CA, and Drews NR: Physiological concentrations of genistein and 17beta-estradiol inhibit MDA-MB-231 breast cancer cell growth by increasing BAX/BCL-2 and reducing pERK1/2. Anticancer Res 32, 1181–1191, 2012.
   PubMed Web of Science ®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, e54369, 2013.
   PubMed Web of Science ®Google Scholar
• Qi W, Weber CR, Wasland K, and Savkovic SD: Genistein inhibits proliferation of colon cancer cells by attenuating a negative effect of epidermal growth factor on tumor suppressor FOXO3 activity. BMC Cancer 11, 219, 2011.
   PubMed Web of Science ®Google Scholar
• Zhang Y and Chen H: Genistein attenuates WNT signaling by up-regulating sFRP2 in a human colon cancer cell line. Exp Biol Med (Maywood.) 236, 714–722, 2011.
   PubMed Web of Science ®Google Scholar
• Majid S, Dar AA, Ahmad AE, Hirata H, Kawakami K, et al.: BTG3 tumor suppressor gene promoter demethylation, histone modification and cell cycle arrest by genistein in renal cancer. Carcinogenesis 30, 662–670, 2009.
   PubMed Web of Science ®Google Scholar
• Majid S, Kikuno N, Nelles J, Noonan E, Tanaka Y, et al.: Genistein induces the p21WAF1/CIP1 and p16INK4a tumor suppressor genes in prostate cancer cells by epigenetic mechanisms involving active chromatin modification. Cancer Res 68, 2736–2744, 2008.
   PubMed Web of Science ®Google Scholar
• Nicoloso MS, Spizzo R, Shimizu M, Rossi S, and Calin GA: MicroRNAs—the micro steering wheel of tumour metastases. Nat Rev Cancer 9, 293–302, 2009.
   PubMed Web of Science ®Google Scholar
• Calin GA and Croce CM: MicroRNA signatures in human cancers. Nat Rev Cancer 6, 857–866, 2006.
   PubMed Web of Science ®Google Scholar
• Parker LP, Taylor DD, Kesterson J, Metzinger DS, and Gercel-Taylor C.:Modulation of microRNA associated with ovarian cancer cells by genistein. Eur J Gynaecol Oncol 30, 616–621, 2009.
   PubMed Web of Science ®Google Scholar
• Rabiau N, Trraf HK, Adjakly M, Bosviel R, Guy L, et al.: miRNAs differentially expressed in prostate cancer cell lines after soy treatment. In Vivo 25, 917–921, 2011.
   PubMed Web of Science ®Google Scholar
• Chen Y, Zaman MS, Deng G, Majid S, Saini S, et al.: MicroRNAs 221/222 and genistein-mediated regulation of ARHI tumor suppressor gene in prostate cancer. Cancer Prev Res (Phila) 4, 76–86, 2011.
   PubMed Web of Science ®Google Scholar
• Chiyomaru T, Yamamura S, Zaman MS, Majid S, Deng G, et al.: Genistein suppresses prostate cancer growth through inhibition of oncogenic microRNA-151. PLoS One 7, e43812, 2012.
   PubMed Web of Science ®Google Scholar
• Xu L, Xiang J, Shen J, Zou X, Zhai S, et al.: Oncogenic microRNA-27a is a target for genistein in ovarian cancer cells. Anticancer Agents Med Chem 13, 1126–1132, 2013.
   Web of Science ®Google Scholar
• Hirata H, Ueno K, Nakajima K, Tabatabai ZL, Hinoda Y, et al.: Genistein downregulates onco-miR-1260b and inhibits Wnt-signalling in renal cancer cells. Br J Cancer 108, 2070–2078, 2013.
   PubMed Web of Science ®Google Scholar
• Sun Q, Cong R, Yan H, Gu H, Zeng Y, et al.: Genistein inhibits growth of human uveal melanoma cells and affects microRNA-27a and target gene expression. Oncol Rep 22, 563–567, 2009.
   PubMed Web of Science ®Google Scholar
• Xia J, Duan Q, Ahmad A, Bao B, Banerjee S, et al.: Genistein inhibits cell growth and induces apoptosis through up-regulation of miR-34a in pancreatic cancer cells. Curr Drug Targets 13, 1750–1756, 2012.
   PubMed Web of Science ®Google Scholar
• Chiyomaru T, Yamamura S, Fukuhara S, Yoshino H, Kinoshita T, et al.: Genistein inhibits prostate cancer cell growth by targeting mir-34a and oncogenic HOTAIR. PLoS One 8, e70372, 2013.
   PubMed Web of Science ®Google Scholar
• Hirata H, Hinoda Y, Shahryari V, Deng G, Tanaka, Y, et al.: Genistein downregulates onco-miR-1260b and upregulates sFRP1 and Smad4 via demethylation and histone modification in prostate cancer cells. Br J Cancer 110, 1645–1654, 2014.
   PubMed Web of Science ®Google Scholar
• Chiyomaru T, Yamamura S, Fukuhara S, Hidaka H, Majid S, et al.: Genistein up-regulates tumor suppressor microRNA-574-3p in prostate cancer. PLoS One 8, e58929, 2013.
   PubMed Web of Science ®Google Scholar
• Ma J, Cheng L, Liu H, Zhang J, Shi Y, et al.: Genistein down-regulates miR-223 expression in pancreatic cancer cells. Curr Drug Targets 14, 1150–1156, 2013.
   PubMed Web of Science ®Google Scholar
• Xia J, Cheng L, Mei C, Ma J, Shi Y, et al.: Genistein inhibits cell growth and invasion through regulation of miR-27a in pancreatic cancer cells. Curr PharmDes 20, 5348--5353, 2014.
   Web of Science ®Google Scholar
• Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, et al.: MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65, 7065–7070, 2005.
   PubMed Web of Science ®Google Scholar
• Zhang C, Zhao J, and Deng H: 17beta-Estradiol up-regulates miR-155 expression and reduces TP53INP1 expression in MCF-7 breast cancer cells. Mol Cell Biochem 379, 201–211, 2013.
   PubMed Web of Science ®Google Scholar
• Sun Y, Wang M, Lin G, Sun S, Li X, et al.: Serum microRNA-155 as a potential biomarker to track disease in breast cancer. PLoS One 7, e47003, 2012.
   PubMed Web of Science ®Google Scholar
• Mattiske S, Suetani RJ, Neilsen PM, and Callen DF: The oncogenic role of miR-155 in breast cancer. Cancer Epidemiol.Biomarkers Prev 21, 1236–1243, 2012.
   PubMed Web of Science ®Google Scholar
• Kong W, He L, Richards EJ, Challa S, Xu CX, et al.: Upregulation of miRNA-155 promotes tumour angiogenesis by targeting VHL and is associated with poor prognosis and triple-negative breast cancer. Oncogene 33, 679--689, 2013.
   Web of Science ®Google Scholar
• Gasparini P, Cascione L, Fassan M, Lovat F, Guler G, et al.: microRNA expression profiling identifies a four microRNA signature as a novel diagnostic and prognostic biomarker in triple negative breast cancers. Oncotarget 15, 1174--1184, 2014.
   Web of Science ®Google Scholar
• Higgs G and Slack F: The multiple roles of microRNA-155 in oncogenesis. J Clin Bioinforma 3, 17, 2013.
   PubMedGoogle Scholar
• Deng N, Puetter A, Zhang, K, Johnson K, Zhao Z, et al.: Isoform-level microRNA-155 target prediction using RNA-seq. Nucleic Acids Res 39, e61, 2011.
   PubMed Web of Science ®Google Scholar
• Lossner C, Meier J, Warnken U, Rogers MA, Lichter P, et al.: Quantitative proteomics identify novel miR-155 target proteins. PLoS One 6, e22146, 2011.
   PubMed Web of Science ®Google Scholar
• Tili E, Michaille JJ, Alder H, Volinia S, Delmas D, et al.: Resveratrol modulates the levels of microRNAs targeting genes encoding tumor-suppressors and effectors of TGFbeta signaling pathway in SW480 cells. Biochem.Pharmacol 80, 2057–2065, 2010.
   PubMed Web of Science ®Google Scholar
• Chambers AF: MDA-MB-435 and M14 cell lines: identical but not M14 melanoma? Cancer Res 69, 5292–5293, 2009.
   PubMed Web of Science ®Google Scholar
• Castillo-Pichardo L, Martinez-Montemayor MM, Martinez JE, Wall KM, Cubano LA, et al.: Inhibition of mammary tumor growth and metastases to bone and liver by dietary grape polyphenols. Clin Exp Metastasis 26, 505–516, 2009.
   PubMed Web of Science ®Google Scholar
• de la PC, Otero-Franqui E, Martinez-Montemayor M, and Dharmawardhane S: The soy isoflavone equol may increase cancer malignancy via upregulation of eukaryotic protein synthesis initiation factor eIF4G. J Biol Chem 287, 41640--41650, 2012.
   Web of Science ®Google Scholar
• Fang MZ, Chen D, Sun Y, Jin Z, Christman JK, et al.: Reversal of hypermethylation and reactivation of p16INK4a, RARbeta, and MGMT genes by genistein and other isoflavones from soy. Clin Cancer Res 11, 7033–7041, 2005.
   PubMed Web of Science ®Google Scholar
• Mai Z, Blackburn GL, and Zhou JR: Genistein sensitizes inhibitory effect of tamoxifen on the growth of estrogen receptor-positive and HER2-overexpressing human breast cancer cells. Mol Carcinog 46, 534–542, 2007.
   PubMed Web of Science ®Google Scholar
• Kong W, He L, Coppola M, Guo J, Esposito NN, et al.: MicroRNA-155 regulates cell survival, growth, and chemosensitivity by targeting FOXO3a in breast cancer. J Biol. Chem 285, 17869–17879, 2010.
   PubMed Web of Science ®Google Scholar
• Lu C, Huang, X, Zhang X, Roensch K, Cao Q, et al.: miR-221 and miR-155 regulate human dendritic cell development, apoptosis, and IL-12 production through targeting of p27kip1, KPC1, and SOCS-1. Blood 117, 4293–4303, 2011.
   PubMed Web of Science ®Google Scholar
• Yamanaka Y, Tagawa H, Takahashi N, Watanabe A, Guo YM, et al.: Aberrant overexpression of microRNAs activate AKT signaling via down-regulation of tumor suppressors in natural killer-cell lymphoma/leukemia. Blood 114, 3265–3275, 2009.
   PubMed Web of Science ®Google Scholar
• Banerjee S, Li Y, Wang Z, and Sarkar FH: Multi-targeted therapy of cancer by genistein. Cancer Lett 269, 226–242, 2008.
   PubMed Web of Science ®Google Scholar
• Zhang P, Bill K, Liu J, Young E, Peng T, et al.: MiR-155 is a liposarcoma oncogene that targets casein kinase-1alpha and enhances beta-catenin signaling. Cancer Res 72, 1751–1762, 2012.
   PubMed Web of Science ®Google Scholar
• Khan N, Adhami VM, and Mukhtar H: Apoptosis by dietary agents for prevention and treatment of prostate cancer. Endocr Relat Cancer 17, R39–R52, 2010.
   PubMed Web of Science ®Google Scholar
• Li Y, Bhuiyan M, and Sarkar FH: Induction of apoptosis and inhibition of c-erbB-2 in MDA-MB-435 cells by genistein. Int J Oncol 15, 525–533, 1999.
   PubMed Web of Science ®Google Scholar
• Choi EJ, Jung JY, and Kim GH: Genistein inhibits the proliferation and differentiation of MCF-7 and 3T3-L1 cells via the regulation of ERalpha expression and induction of apoptosis. Exp Ther Med 8, 454–458, 2014.
   PubMed Web of Science ®Google Scholar
• Prietsch RF, Monte LG, da Silva FA, Beira FT, Del Pino FA, et al.:. Genistein induces apoptosis and autophagy in human breast MCF-7 cells by modulating the expression of proapoptotic factors and oxidative stress enzymes. Mol Cell Biochem 390, 235–242, 2014.
   PubMed Web of Science ®Google Scholar
• Tsuboy MS, Marcarini JC, de Souza AO, de Paula NA, Dorta DJ, et al.: Genistein at maximal physiologic serum levels induces G0/G1 arrest in MCF-7 and HB4a cells, but not apoptosis. J Med Food 17, 218–225, 2014.
   PubMed Web of Science ®Google Scholar
• Pons D G, Nadal-Serrano M, Del MB-R, Sastre-Serra J, Oliver J, et al.: Genistein modulates proliferation and mitochondrial functionality in breast cancer cells depending on ERalpha/ERbeta ratio. J Cell Biochem 115, 949--958, 2014.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Gong P, Madak-Erdogan Z, Martin T, Jeyakumar M, et al.: Mechanisms enforcing the estrogen receptor beta selectivity of botanical estrogens. FASEB J 27, 4406–4418, 2013.
   PubMed Web of Science ®Google Scholar
• Tome Y, Uehara F, Mii S, Yano S, Zhang L, et al.: 3-dimensional tissue is formed from cancer cells in vitro on Gelfoam(R), but not on Matrigel. J Cell Biochem 115, 1362–1367, 2014.
   PubMed Web of Science ®Google Scholar
• Geller J, Sionit L, Partido C, Li L, Tan X, et al.: Genistein inhibits the growth of human–patient BPH and prostate cancer in histoculture. Prostate 34, 75–79, 1998.
   PubMed Web of Science ®Google Scholar
• Zheng SR, Guo GL, Zhang W, Huang G.L., Hu XQ, et al.: Clinical significance of miR-155 expression in breast cancer and effects of miR-155 ASO on cell viability and apoptosis. Oncol Rep, 27, 1149--1155, 2012.
   Web of Science ®Google Scholar
• Nagaraju GP, Zafar SF, and El-Rayes BF: Pleiotropic effects of genistein in metabolic, inflammatory, and malignant diseases. Nutr Rev 71, 562–572, 2013.
   PubMed Web of Science ®Google Scholar
• ZhangY Li Q, Zhou D, and Chen H: Genistein, a soya isoflavone, prevents azoxymethane-induced up-regulation of WNT/beta-catenin signalling and reduces colon pre-neoplasia in rats. Br J Nutr 109, 33–42, 2013.
   PubMed Web of Science ®Google Scholar