3,3′-Diindolylmethane Inhibits TNF-α- and TGF-β-Induced Epithelial–Mesenchymal Transition in Breast Cancer Cells

References

• Siegel RL, Miller KD, and Jemal A: Cancer Statistics. CA Cancer J Clin 67, 7–30, 2017.
   PubMed Web of Science ®Google Scholar
• Weigelt B, Peterse JL, and van 't Veer LJ: Breast cancer metastasis: markers and models. Nat Rev Cancer 5, 591–602, 2005.
   PubMed Web of Science ®Google Scholar
• Etti IC, Abdullah R, Kadir A, Hashim NM, and Yeap SK: The molecular mechanism of the anticancer effect of Artonin E in MDA-MB 231 triple negative breast cancer cells. PLoS One 12, e0182357, 2017.
   PubMed Web of Science ®Google Scholar
• Musgrove EA, and Sutherland RL: Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 9, 631–643, 2009.
   PubMed Web of Science ®Google Scholar
• Tiwari N, Gheldof A, Tatari M, and Christofori G: EMT as the ultimate survival mechanism of cancer cells. Semin Cancer Biol 22, 194–207, 2012.
   PubMed Web of Science ®Google Scholar
• Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2, 76–83, 2000.
   PubMed Web of Science ®Google Scholar
• Bolós V, Peinado H, Pérez-Moreno MA, Fraga MF, Esteller M, et al. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci 116, 499–511, 2003.
   PubMed Web of Science ®Google Scholar
• Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, et al. The two-handed E box binding zinc finger protein SIP1 downregulates Ecadherin and induces invasion. Mol Cell 7, 1267–1278, 2001.
   PubMed Web of Science ®Google Scholar
• Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927–939, 2004.
   PubMed Web of Science ®Google Scholar
• Ouyang G, Wang Z, Fang X, Liu J, and Yang CJ: Molecular signaling of the epithelial to mesenchymal transition in generating and maintaining cancer stem cells. Cell Mol Life Sci 67, 2605–2618, 2010.
   PubMed Web of Science ®Google Scholar
• Siegel PM, Shu W, Cardiff RD, Muller WJ, and Massagué J: Transforming growth factor beta signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis. Proc Natl Acad Sci U S A 100, 8430–8435, 2003.
   PubMed Web of Science ®Google Scholar
• Balkwill F: Tumour necrosis factor and cancer. Nat Rev Cancer 9, 361–371, 2009.
   PubMed Web of Science ®Google Scholar
• Saito A, Suzuki HI, Horie M, Ohshima M, Morishita Y, et al. An integrated expression profiling reveals target genes of TGF-β and TNF-α possibly mediated by microRNAs in lung cancer cells. PLoS One 8, e56587, 2013.
   PubMed Web of Science ®Google Scholar
• Papadopoulou E, Anagnostopoulos K, Tripsianis G, Tentes I, Kakolyris S, et al. Evaluation of predictive and prognostic significance of serum TGF-beta1 levels in breast cancer according to HER-2 codon 655 polymorphism. Neoplasma 55, 229–238, 2008.
   PubMed Web of Science ®Google Scholar
• Papadopoulou E, Tripsianis G, Anagnostopoulos K, Tentes I, Kakolyris S, et al. Significance of serum tumor necrosis factor-alpha and its combination with HER-2 codon 655 polymorphism in the diagnosis and prognosis of breast cancer. Int J Biol Markers 25, 126–135, 2010.
   PubMed Web of Science ®Google Scholar
• Anderton MJ, Manson MM, Verschoyle RD, Gescher A, Lamb JH, et al. Pharmacokinetics and tissue disposition of indole-3-carbinol and its acid condensation products after oral administration to mice. Clin Cancer Res 10, 5233–5241, 2004.
   PubMed Web of Science ®Google Scholar
• Thomson CA, Ho E, and Strom MB : Chemopreventive properties of 3,3'-diindolylmethane in breast cancer: evidence from experimental and human studies. Nutr Rev 74, 432–443, 2016.
   PubMed Web of Science ®Google Scholar
• Liu X, and Lv K: Cruciferous vegetables intake is inversely associated with risk of breast cancer: a meta-analysis. Breast 22, 309–313, 2013.
   PubMed Web of Science ®Google Scholar
• Hong C, Firestone GL, and Bjeldanes LF : Bcl-2 family-mediated apoptotic effects of 3,3'-diindolylmethane (DIM) in human breast cancer cells. Biochem Pharmacol 63, 1085–1097, 2002.
   PubMed Web of Science ®Google Scholar
• Gong Y, Sohn H, Xue L, Firestone GL, and Bjeldanes LF : 3,3'-Diindolylmethane is a novel mitochondrial H(+)-ATP synthase inhibitor that can induce p21(Cip1/Waf1) expression by induction of oxidative stress in human breast cancer cells. Cancer Res 66, 4880–4887, 2006.
   PubMed Web of Science ®Google Scholar
• Fan S, Meng Q, Saha T, Sarkar FH, and Rosen EM: Low concentrations of diindolylmethane, a metabolite of indole-3-carbinol, protect against oxidative stress in a BRCA1-dependent manner. Cancer Res 69, 6083–6091, 2009.
   PubMed Web of Science ®Google Scholar
• Chen I, McDougal A, Wang F, and Safe S: Aryl hydrocarbon receptor-mediated antiestrogenic and antitumorigenic activity of diindolylmethane. Carcinogenesis 19, 1631–1639, 1998.
   PubMed Web of Science ®Google Scholar
• Ahmad A, Ali S, Wang Z, Ali AS, Sethi S, et al. 3,3'-Diindolylmethane enhances taxotere-induced growth inhibition of breast cancer cells through downregulation of FoxM1. Int J Cancer 129, 1781–1791, 2011.
   PubMed Web of Science ®Google Scholar
• Livak KJ, and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408, 2001.
   PubMed Web of Science ®Google Scholar
• Götte M, Kersting C, Radke I, Kiesel L, and Wülfing P: An expression signature of syndecan-1 (CD138), E-cadherin and c-met is associated with factors of angiogenesis and lymphangiogenesis in ductal breast carcinoma in situ. Breast Cancer Res 9, R8, 2007.
   PubMed Web of Science ®Google Scholar
• Fuxe J, and Karlsson MC: TGF-β-induced epithelial-mesenchymal transition: a link between cancer and inflammation. Semin Cancer Biol 22, 455–461, 2012.
   PubMed Web of Science ®Google Scholar
• Louie SM, Grossman EA, Crawford LA, Ding L, Camarda R, et al. GSTP1 is a driver of triple-negative breast cancer cell metabolism and pathogenicity. Cell Chem Biol 23, 567–578, 2016.
   PubMed Web of Science ®Google Scholar
• Ikushima H, and Miyazono K: TGFbeta signalling: a complex web in cancer progression. Nat Rev Cancer 10, 415–424, 2010.
   PubMed Web of Science ®Google Scholar
• Li CW, Xia W, Huo L, Lim SO, Wu Y, et al. Epithelial-mesenchymal transition induced by TNF-α requires NF-κB-mediated transcriptional upregulation of Twist1. Cancer Res 72, 1290–1300, 2012.
   PubMed Web of Science ®Google Scholar
• Bates RC, and Mercurio AM: Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids. Mol Biol Cell 14, 1790–1800, 2003.
   PubMed Web of Science ®Google Scholar
• Heldin CH, Vanlandewijck M, and Moustakas A: Regulation of EMT by TGFβ in cancer. FEBS Lett 586, 1959–1970, 2012.
   PubMed Web of Science ®Google Scholar
• Betapudi V, Licate LS, and Egelhoff TT: Distinct roles of nonmuscle myosin II isoforms in the regulation of MDA-MB-231 breast cancer cell spreading and migration. Cancer Res 66, 4725–4733, 2006.
   PubMed Web of Science ®Google Scholar
• Rahman KM, Ali S, Aboukameel A, Sarkar SH, Wang Z, et al. Inactivation of NF-kappaB by 3,3'-diindolylmethane contributes to increased apoptosis induced by chemotherapeutic agent in breast cancer cells . Mol Cancer Ther 6, 2757–2765, 2007.
   PubMed Web of Science ®Google Scholar
• Marques M, Laflamme L, Benassou I, Cissokho C, Guillemette B, and Gaudreau L: Low levels of 3,3'-diindolylmethane activate estrogen receptor α and induce proliferation of breast cancer cells in the absence of estradiol. BMC Cancer 14, 524, 2014.
   PubMed Web of Science ®Google Scholar
• Wang Z, Yu BW, Rahman KM, Ahmad F, and Sarkar FH: Induction of growth arrest and apoptosis in human breast cancer cells by 3,3-diindolylmethane is associated with induction and nuclear localization of p27kip. Mol Cancer Ther 7, 341–349, 2008.
   PubMed Web of Science ®Google Scholar
• Hong C, Kim HA, Firestone GL, and Bjeldanes LF3: 3'-Diindolylmethane (DIM) induces a G(1) cell cycle arrest in human breast cancer cells that is accompanied by Sp1-mediated activation of p21(WAF1/CIP1) expression. Carcinogenesis 23, 1297–1305, 2002.
   PubMed Web of Science ®Google Scholar
• Banerjee S, Kong D, Wang Z, Bao B, Hillman GG, et al. Attenuation of multi-targeted proliferation-linked signaling by 3,3'-diindolylmethane (DIM): from bench to clinic. Mutat Res 728, 7–66, 2011.
   Web of Science ®Google Scholar
• Panagakos FS, and Kumar S: Modulation of proteases and their inhibitors in immortal human osteoblast-like cells by tumor necrosis factor-alpha in vitro. Inflammation 18, 243–265, 1994.
   PubMed Web of Science ®Google Scholar
• Massagué J: TGFbeta in Cancer. Cell 134, 215–230, 2008.
   PubMed Web of Science ®Google Scholar
• Ivanović V, Todorović-Raković N, Demajo M, Nesković-Konstantinović Z, Subota V, et al. Elevated plasma levels of transforming growth factor-beta 1 (TGF-beta 1) in patients with advanced breast cancer: association with disease progression. Eur J Cancer 39, 454–461, 2003.
   PubMed Web of Science ®Google Scholar
• Kalluri R, and Weinberg RA: The basics of epithelial-mesenchymal transition. J Clin Invest 119, 1420–1428, 2009.
   PubMed Web of Science ®Google Scholar
• Schmalhofer O, Brabletz S, and Brabletz T: E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 28, 151–166, 2009.
   PubMed Web of Science ®Google Scholar
• Bellovin DI, Bates RC, Muzikansky A, Rimm DL, and Mercurio AM: Altered localization of p120 catenin during epithelial to mesenchymal transition of colon carcinoma is prognostic for aggressive disease. Cancer Res 65, 10938–10945, 2005.
   PubMed Web of Science ®Google Scholar
• Kasai H, Allen JT, Mason RM, Kamimura T, and Zhang Z : TGF-beta1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir Res 6, 562005.
   PubMed Web of Science ®Google Scholar
• Yamauchi Y, Kohyama T, Takizawa H, Kamitani S, Desaki M, et al. Tumor necrosis factor-alpha enhances both epithelial-mesenchymal transition and cell contraction induced in A549 human alveolar epithelial cells by transforming growth factor-beta1. Exp Lung Res 36, 12–24, 2010.
   PubMed Web of Science ®Google Scholar
• Kamitani S, Yamauchi Y, Kawasaki S, Takami K, Takizawa H, et al. Simultaneous stimulation with TGF-b1 and TNF-a induces epithelial mesenchymal transition in bronchial epithelial cells. Int Arch Allergy Immunol 155, 119–128, 2011.
   PubMed Web of Science ®Google Scholar
• Sethi S, Li Y, and Sarkar FH: Regulating miRNA by natural agents as a new strategy for cancer treatment. Curr Drug Targets 14, 1167–1174, 2013.
   PubMed Web of Science ®Google Scholar
• Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10, 593–601, 2008.
   PubMed Web of Science ®Google Scholar
• Li Y, VandenBoom TG II, Kong D, Wang Z, Ali S, Philip PA, and Sarkar PH. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res 69, 6704–6712, 2009.
   PubMed Web of Science ®Google Scholar
• Lamouille S, Xu J, and Derynck R : Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 15, 178–196, 2014.
   PubMed Web of Science ®Google Scholar
• Sánchez-Tilló E, Liu Y, de Barrios O, Siles L, Fanlo L, et al. EMT-activating transcription factors in cancer: beyond EMT and tumor invasiveness. Cell Mol Life Sci 69, 3429–3456, 2012.
   PubMed Web of Science ®Google Scholar
• Itoh S, and ten Dijke P: Negative regulation of TGF-beta receptor/Smad signal transduction. Curr Opin Cell Biol 19, 176–184, 2007.
   PubMed Web of Science ®Google Scholar
• Mu Y, Gudey SK, and Landström M: Non-Smad signaling pathways. Cell Tissue Res 347, 11–20, 2012.
   PubMed Web of Science ®Google Scholar
• Neuzillet C, Tijeras-Raballand A, Cohen R, Cros J, Faivre S, et al. Targeting the TGFβ pathway for cancer therapy. Pharmacol Ther 147, 22–31, 2015.
   PubMed Web of Science ®Google Scholar
• Nola S, Sin S, Bonin F, Lidereau R, and Driouch K: A methodological approach to unravel organ-specific breast cancer metastasis. J Mammary Gland Biol Neoplasia 17, 135–145, 2012.
   PubMed Web of Science ®Google Scholar
• Muraoka RS, Koh Y, Roebuck LR, Sanders ME, Brantley-Sieders D, et al. Increased malignancy of Neu-induced mammary tumors overexpressing active transforming growth factor beta1. Mol Cell Biol 23, 8691–8703, 2003.
   PubMed Web of Science ®Google Scholar
• Gupta P, and Srivastava SK: HER2 mediated de novo production of TGFβ leads to SNAIL driven epithelial-to-mesenchymal transition and metastasis of breast cancer. Mol Oncol 8, 1532–1547, 2014.
   PubMed Web of Science ®Google Scholar
• Muraoka-Cook RS, Shin I, Yi JY, Easterly E, Barcellos-Hoff MH, et al. Activated type I TGFbeta receptor kinase enhances the survival of mammary epithelial cells and accelerates tumor progression. Oncogene 25, 3408–3423, 2006.
   PubMed Web of Science ®Google Scholar
• Wolczyk D, Zaremba-Czogalla M, Hryniewicz-Jankowska A, Tabola R, Grabowski K, et al. TNF-α promotes breast cancer cell migration and enhances the concentration of membrane-associated proteases in lipid rafts. Cell Oncol (Dordr) 39, 353–363, 2016.
   PubMed Web of Science ®Google Scholar
• Kong D, Li Y, Wang Z, Banerjee S, and Sarkar FH : Inhibition of angiogenesis and invasion by 3,3'-diindolylmethane is mediated by the nuclear factor-kappaB downstream target genes MMP-9 and uPA that regulated bioavailability of vascular endothelial growth factor in prostate cancer. Cancer Res 67, 3310–3319, 2007.
   PubMed Web of Science ®Google Scholar
• Nicastro HL, Firestone GL, and Bjeldanes LF: 3,3'-diindolylmethane rapidly and selectively inhibits hepatocyte growth factor/c-Met signaling in breast cancer cells. J Nutr Biochem 24, 1882–1888, 2013.
   PubMed Web of Science ®Google Scholar