472
Views
29
CrossRef citations to date
0
Altmetric
Review Article

E-Cadherin/β-Catenin Complex: A Target for Anticancer and Antimetastasis Plants/Plant-derived Compounds

&
Pages 702-722 | Received 27 Apr 2016, Accepted 05 Apr 2017, Published online: 19 May 2017

References

  • Berx G and van Roy F: Involvement of members of the cadherin superfamily in cancer. Cold Spring Harbor Perspect Biol 1(6), a003129, 2009. doi: 10.1101/cshperspect.a003129
  • Harris TJC and Tepass U: Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 11, 502–514, 2010. doi: 10.1038/nrm2927
  • Howard S, Deroo T, Fujita Y, and Itasaki N: A positive role of cadherin in Wnt/beta-catenin signalling during epithelial-mesenchymal transition. PLoS One 6(8), 1–16, 2011. doi:10.1371/journal.pone.0023899
  • Meng W and Takeichi M: Adherens junction: Molecular architecture and regulation. Cold Spring Harbor Perspect Biol 1, a002899, 2009. doi: 10.1101/cshperspect.a002899
  • Halbleib JM and Nelson WJ: Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20, 3199–3214, 2006. doi: 10.1101/gad.1486806
  • Niessen C: Tight junctions-adherens junctions: basic structure and function. J Invest Dermatol 127, 2525–2532, 2007. doi:10.1038/sj.jid.5700865
  • Etienne-Manneville S: Adherens junctions during cell migration. Subcell Biochem 60, 225–249, 2012. doi: 10.1007/978-94-007-4186-7_10
  • Yang Z, Zhang H, and Kumar R: Regulation of E-cadherin. Breast Cancer Online 8(e15), 1–4, 2005. doi: 10.1017/S1470903105003159.
  • van Roy F and Berx G: The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci 65, 3756–3788, 2008. doi: 10.1007/s00018-008-8281-1
  • Russo GL: Ins and outs of dietary phytochemicals in cancer chemoprevention. Biochem Pharmacol 74, 533–544, 2007. doi:10.1016/j.bcp.2007.02.014
  • Hsing AW, Chokkalingam AP, Gao YT, Madigan MP, Deng J, et al.: Allium vegetables and risk of prostate cancer: A population-based study. J Natl Cancer Inst 94(21), 1648–1651, 2002.
  • Hirono I, Mori H, and Culvenor CC: Carcinogenic activity of coltsfoot, Tussilago farfara l. GANN Jpn J Cancer Res 67(1), 125–129, 1976.
  • Ryu SD and Chung WG: Induction of the procarcinogen-activating CYP1A2 by a herbal dietary supplement in rats and humans. Food Chem Toxicol 41(6), 861–866, 2003. doi: 10.1016/S0278-6915(03)00037-1
  • Chu Q, Ling M, Feng H, Cheung HW, Tsao SW, et al.: A novel anticancer effect of garlic derivatives: inhibition of cancer cell invasion through restoration of E-cadherin expression. Carcinogenesis 27(1), 2180–2189, 2006. doi:10.1093/carcin/bgl054
  • Kandouz M, Alachkar A, Zhang L, Dekhil H, Chehna F, et al.: Teucrium polium plant extract inhibits cell invasion and motility of human prostate cancer cells via the restoration of the E-cadherin/catenin complex. J Ethnopharmacol 129, 410–415, 2010. doi: 10.1016/j.jep.2009.10.035
  • Tafrihi M, Toosi S, Minaei T, Gohari AR, Niknam V, et al.: Anticancer properties of Teucrium persicum in PC-3 prostate cancer cells. Asia Pac J Cancer Prevent 15(2), 785–791, 2014. doi: https://doi.org/10.7314/APJCP.2014.15.2.785
  • Rose P, Huang Q, Ong CN, and Whitemann M: Broccoli and watercress suppress matrix metalloproteinase-9 activity and invasiveness of human MDA-MB-231 breast cancer cells. Toxicol Appl Pharmacol 209, 105–113, 2005. doi:10.1016/j.taap.2005.04.010
  • Su Y, de Lumen B, and Simmen CM: Soy component Genistein and Lunasin regulate E-cadherin and Wnt signaling in mammary epithelial cells. FASEB J 22, 700–701, 2008.
  • Su Y and Simmen RC: Soy isoflavone genistein upregulates epithelial adhesion molecule E-cadherin expression and attenuates β-catenin signaling in mammary epithelial cells. Carcinogenesis 30(2), 331–339, 2009. doi: 10.1093/carcin/bgn279
  • Kweon S, Park KA, and Choi H: Chemopreventive effect of garlic powder diet in diethylnitrosamine-induced rat hepatocarcinogenesis. Life Sci 73, 2515–2526, 2003. doi: 10.1016/S0024-3205(03)00660-X
  • Ma L, Wen Sh, Zhan Y, He Y, Liu X, et al.: Anticancer Effects of the Chinese Medicine Matrine on Murine Hepatocellular Carcinoma Cells. Planta Med 74(3), 245–251, 2008. doi: 10.1055/s-2008-1034304
  • He BC, Gao JL, Zhang BQ, Lou Q, Shi Q, et al.: Tetrandrine inhibits Wnt/β-catenin signaling and suppresses tumor growth of human colorectal cancer. Mol Pharmacol 79(2), 211–219, 2011. doi: 10.1124/mol.110.068668
  • Yagi T and Takeichi M: Cadherin superfamily genes: functions, genomic organization and neurologic diversity. Genes Dev 14, 1169–1180, 2000. doi: 10.1101/gad.14.10.1169
  • Pećina-Šlaus N: Tumor suppressor gene E-cadherin and its role in normal and malignant cells. Cancer Cell Int 3(1), 17, 2003. doi: 10.1186/1475-2867-3-17
  • Leckband D and Prakasam A: Mechanism and dynamics of cadherin adhesion. Annu Rev Biomed Eng 8, 259–287, 2006. doi: 10.1146/annurev.bioeng.8.061505.095753
  • Yoshida-Noro C, Suzuki N, and Takeichi M: Molecular nature of the calcium-dependent cell-cell adhesion system in mouse teratocarcinoma and embryonic cells studied with a monoclonal antibody. Dev Biol 101(1), 19–27, 1984. doi:10.1016/0012-1606(84)90112-X
  • Wheelock MJ and Johnson KR: Cadherins as modulators of cellular phenotype. Annu Rev Cell Dev Biol 19, 207–235, 2003. doi: 10.1146/annurev.cellbio.19.011102.111135
  • Pokutta S and Weis W: Structure and mechanism of cadherins and catenins in cell-cell contacts. Annu Rev Cell Dev Biol 23, 237–261, 2007. doi: 10.1146/annurev.cellbio.22.010305.104241
  • Takeichi M: The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102(4), 639–655, 1988.
  • Büyüktunçer D, Arisan S, and Özdilli K: E-cadherin molecular mechanism in prostate cancer. J Cell Mol Biol 2, 57–64, 2003.
  • Baum B and Georgiou M: Dynamics of adherens junctions in epithelial establishment, maintenance and remodeling. J Cell Biol 192(6), 907–917, 2011. doi:10.1083/jcb.201009141
  • Thiery JP: Cell adhesion in cancer. C R Phys 4, 289–304, 2003. doi:10.1016/S1631-0705(03)00031-8
  • Nollet F, Berx G, and Molemans F: Genomic organization of the human β-catenin gene (CTNNB1). Genomics 23, 413–424, 1996. doi:10.1006/geno.1996.0136
  • Willert K and Nusse R: β-catenin: a key mediator of Wnt signaling. Curr Opin Genet Dev 8, 95–102, 1998. doi:10.1016/S0959-437X(98)80068-3
  • He TC, Sparks AB, Rago C, Hermeking H, Zawel L, et al.: Identification of c-MYC as a target of the APC pathway. Science 281, 1509–1512, 1998. doi: 10.1126/science.281.5382.1509
  • Polakis P: Wnt signaling and cancer. Genes Dev 14, 1837–1851, 2000. doi: 10.1101/gad.14.15
  • Fagotto F: Looking beyond the Wnt pathway for the deep nature of β-catenin. EMBO Rep 14, 422–433, 2013. doi:10.1038/embor.2013.45
  • Herbst A, Jurinovic V, Krebs S, Thieme SE, Blum H, et al.: Comprehensive analysis of β-catenin target genes in colorectal carcinoma cell lines with deregulated Wnt/β-catenin signaling. BMC Genomics 15(74), 1–15, 2014. doi:10.1186/1471-2164-15-74
  • Wodarz A and Nusse R: Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 14, 59–88, 1998. doi: 10.1146/annurev.cellbio.14.1.59
  • Huelsken J and Birchmeier W: New aspects of Wnt signaling pathways in higher vertebrates. Curr Opin Genet Dev 11, 547–553, 2001. doi:10.1016/S0959-437X(00)00231-8
  • Logan CY and Nusse R: The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20, 781–810, 2004. doi: 10.1146/annurev.cellbio.20.010403.113126
  • Kaplan D, Meigs TE, Kelly P, and Casey PJ: Identification of a role for β-catenin in the establishment of a bipolar mitotic spindle. J Biol Chem 279(12), 10829–10832, 2004. doi: 10.1074/jbc.C400035200
  • Huang P, Senga T, and Hamaguchi M: A novel role of phospho-β-catenin in microtubule regrowth at centrosome. Oncogene 26, 4357–4317, 007. doi: 10.1038/sj.onc.1210217
  • Bahmanyar S, Guiney EL, Hatch EM, Nelson WJ, and Barth AIM: Formation of extra centrosomal structures is dependent on β-catenin. J Cell Sci 123(18), 3125–3135, 2010. doi:10.1242/jcs.064782
  • Bahmanyar S, Kaplan D, DeLuca JG, Giddings TH, O'Toole ET, et al.: β-Catenin is a Nek2 substrate involved in centrosome separation. Genes Dev 22, 91–105, 2008. doi: 10.1101/gad.1596308
  • Murata T, Ishitsuka Y, Karouji K, Kaeda H, Toki H, et al.: β-catenin C429S mice exhibit sterility consequent to spatiotemporally sustained Wnt signalling in the internal genitalia. Sci Rep 4, 6959, 2014. doi: 10.1038/srep06959
  • MacDonald BT, Tamai K, and He X: Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev Cell 17(1), 9–26, 2009. doi: 10.1016/j.devcel.2009.06.016
  • Seidensticker MJ and Behrens J: Biochemical interactions in the Wnt pathway. Biochim Biophys Acta 1495, 168–182, 2000. doi:10.1016/S0167-4889(99)00158-5
  • Stamos JA and Weis W: The β-catenin destruction complex. Cold Spring Harbor Perspect Biol 5(1), a007898, 2013. doi: 10.1101/cshperspect.a007898
  • Sadot E, Conacci-Sorrel M, Zhurinski J, Shnizer D, Lando Z, et al.: Regulation of S33/S37 phosphorylated β-catenin in normal and transformed cells. J Cell Sci 115(13), 2771–2780, 2002.
  • Daugherty RL and Gottardi CJ: Phospho-regulation of β-catenin adhesion and signaling functions. Physiology 22, 303–309, 2007. doi:10.1152/physiol.00020.2007
  • Maher MT, Flozak AS, Stocker AM, Chenn A, and Gottardi CJ: Activity of the β-catenin phosphodestruction complex at cell–cell contacts is enhanced by cadherin-based adhesion. J Cell Biol 186(2), 219–228, 2009. doi: 10.1083/jcb.200811108
  • Aberle H, Bauer A, Stappert J, Kispert A, and Kemler R: β-catenin is a target for the ubiquitin–proteasome pathway. EMBO J 16(13), 3797–3804, 1997. doi: 10.1093/emboj/16.13.3797
  • Giles RH, van Es JH, and Clevers H: Caught up in a Wnt storm: Wnt signaling in cancer. Biochim Biophys Acta 1653(1), 1–24, 2003. doi:10.1016/S0304-419X(03)00005-2
  • Hino S, Tanji C, Nakayama KI, and Kikuchi A: Phosphorylation of β-catenin by cyclic AMP-dependent protein kinase stabilizes β-catenin through inhibition of its ubiquitination. Mol Cell Biol 25(20), 9063–9072, 2005. doi:10.1128/MCB.25.20.9063–9072.2005
  • Brudvik KW, Paulsen JE, Aandahl EM, Ronald B, and Tasken K: Protein kinase A antagonist inhibits β-catenin nuclear translocation, c-Myc and COX-2 expression and tumor promotion in ApcMin/+ mice. Mol Cancer 10(149), 1–7, 2011. doi:10.1186/1476-4598-10-149
  • Clevers H and Nusse R: Wnt/β-catenin signaling and disease. Cell 149, 1192–1205, 2012. doi: 10.1016/j.cell.2012.05.012
  • Kinzler KW, Nilbert MC, Su LK, Vogelstein B, Bryan T, et al.: Identification of FAP locus genes from chromosome 5q21. Science 253, 661–666, 1991. doi:10.1126/science.1651562
  • Groden J, Thliveris A, Samowitz W, Carlson M, Gelbert L, et al.: Identification and characterization of the familial adenomatous polyposis gene. Cell 66, 589–600, 1991. doi:10.1016/0092-8674(81)90021-0
  • Kinzler KW and Vogelstein B: Lessons from hereditary colorectal cancer. Cell 87, 159–170, 1996. doi: https://doi.org/10.1016/S0092-8674(00)81333-1
  • Clevers H: Wnt breakers in colon cancer. Cancer Cell 5(1), 5–6, 2004. doi: https://doi.org/10.1016/S1535-6108(03)00339-8
  • Oda H, Imai Y, Nakatsuru Y, Hata JI, and Ishikawa T: Somatic Mutation of the APC gene in sporadic hepatoblastomas. Cancer Res 56, 3320–3323, 1996.
  • Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, et al.: Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science 275, 1787–1790, 1997. doi:10.1126/science.275.5307.1787
  • Furuuchi K, Tada M, Yamada H, Kataoka A, et al.: Somatic mutations of the APC gene in primary breast cancers. Am J Pathol 156(6), 1997–2005, 2000. doi: https://doi.org/10.1016/S0002-9440(10)65072-9
  • Rowan AJ, Lamlum H, Ilyas M, Wheeler J, Straub J, et al.: APC mutations in sporadic colorectal tumors: A mutational “hotspot” and interdependence of the “two hits”. PNAS 97(7), 3352–3357, 2000. doi: 10.1073/pnas.97.7.3352
  • Fodde R: The APC gene in colorectal cancer. Eur J Cancer 38(7), 867–871, 2002. doi: https://doi.org/10.1016/S0959-8049(02)00040-0
  • Lee JH, Abraham SC, Kim HS, Nam JH, Choi C, et al.: Inverse Relationship between APC gene mutation in gastric adenomas and development of adenocarcinoma. Am J Pathol 161(2), 611–618, 2002. doi: https://doi.org/10.1016/S0002-9440(10)64216-2
  • Satio T, Oda Y, Sakamoto A, Kawaguchi KI, Tanaka K, et al.: APC mutations in synovial sarcoma. J Pathol 196(4), 445–449, 2002. doi: 10.1002/path.1066
  • Ahmed Y, Hayashi S, Levine A, and Wieschaus E: Regulation of armadillo by a Drosophila APC inhibits neuronal apoptosis during retinal development. Cell 93, 1171–1182, 1998. doi: https://doi.org/10.1016/S0092-8674(00)81461-0
  • Sheng H, Shao J, Williams CS, Pereira M, Taketo MM, et al.: Nuclear translocation of β-catenin in hereditary and carcinogen-induced intestinal adenomas. Carcinogenesis 19(4), 543–549, 1998. doi: 10.1093/carcin/19.4.543
  • Ishizaki Y, Ikeda S, Fujimori M, Shimizu Y, Kurihara T, et al.: Immunohistochemical analysis and mutational analyses of beta-catenin, Axin family and APC genes in hepatocellular carcinomas. Int J Oncol 24(5), 1077–1083, 2004. doi: 10.3892/ijo.24.5.1077
  • Iwai S, Katagiri W, Kong C, Amekawa S, Nakazawa M, et al.: Mutations of the APC, β-catenin, and axin 1 genes and cytoplasmic accumulation of β-catenin in oral squamous cell carcinoma. J Cancer Res Clin Oncol 131(12), 773–782, 2005. doi: 10.1007/s00432-005-0027-y
  • Jiang X, Hao HX, Growney JD, Woolfenden S, Bottiglio C, et al.: Inactivating mutations of RNF43 confer Wnt dependency in pancreatic ductal adenocarcinoma. PNAS 110(31), 12649–12654, 2013. doi:10.1073/pnas.1307218110
  • Fujimori M, Ikeda S, Shimizu Y, Okajima M, and Asahara T: Accumulation of β-catenin protein and mutations in exon 3 of β-catenin gene in gastrointestinal carcinoid tumor. Cancer Res 61(18), 6656–6659, 2001.
  • Tafrihy M, Mohammadzadeh R, Jahanzad E, and Arab Najafi SM: Mutations in the β-catenin gene in gastric and esophageal cancers: an analysis in Iranian patients. JSUT 32(4), 161–167, 2006.
  • Clements WM, Wang J, Sarnaik A, Kim OJ, MacDonald J, et al.: β-catenin mutation is a frequent cause of Wnt pathway activation in gastric cancer. Cancer Res 62, 3503–3506, 2002.
  • Park WS, Oh RR, Park JY, Lee SH, Shin MS, et al.: Frequent somatic mutations of the β-catenin gene in intestinal-type gastric cancer. Cancer Res 59, 4257–4260, 1999.
  • Takahashi M, Nakatsugi S, Sugimura T, and Wakabayashi K: Frequent mutations of the β-catenin gene in mouse colon tumors induced by azoxymethane. Carcinogenesis 21(6), 1117–1120, 2000. doi: 10.1093/carcin/21.6.1117
  • Tong JHM, To KF, Ng EKW, Lau JYW, Lee TL, et al.: Somatic β-catenin mutation in gastric carcinoma - an infrequent event that is not specifc for microsatellite instability. Cancer Lett 163, 125–130, 2001. doi: https://doi.org/10.1016/S0304-3835(00)00681-9
  • Johnson V, Volikos E, Halford SE, Eftekhar Sadat ET, Popat S, et al.: Exon 3 β-catenin mutations are specifically associated with colorectal carcinomas in hereditary non-polyposis colorectal cancer syndrome. Gut 54, 264–267, 2005. doi:10.1136/gut.2004.048132
  • Orsulic S, Huber O, Aberle H, Arnold S, and kemler R: E-cadherin binding prevents β-catenin nuclear localization and β-catenin/LEF-1-mediated transactivation. J Cell Sci 112, 1237–1245, 1999.
  • Sellin J, Umar S, Xiao J, and Morris A: Increased β-catenin expression and nuclear translocation accompany cellular hyperproliferation in vivo. Cancer Res 61(7), 2899–2906, 2001.
  • Anna CH, Iida M, Sills RC, and Devereux TR: Expression of potential β-catenin targets, cyclin D1, c-Jun, c-Myc, E-cadherin, and EGFR in chemically induced hepatocellular neoplasms from B6C3F1 mice. Toxicol Appl Pharmacol 190, 135–145, 2003. doi:10.1016/S0041-008X(03)00170-4
  • Ishida K, Ito S, Wada N, Deguchi H, Hata T, et al.: Nuclear localization of β-catenin involved in precancerous change in oral leukoplakia. Mol Cancer 6(62), 62–68, 2007. doi: 10.1186/1476-4598-6-62.
  • Austinat M, Dunsch R, Wittekind C, Tannafel A, Gebhardt R, et al.: Correlation between β-catenin mutations and expression of Wnt-signaling target genes in hepatocellular carcinoma. Mol Cancer 7(21), 1–9, 2008. doi: 10.1186/1476-4598-7-21
  • Dietrich C, Scherwat J, Faust D, and Oesch F: Subcellular localization of β-catenin is regulated by cell density. Biochem Biophys Res Commun 292, 195–199, 2002. doi: 10.1006/bbrc.2002.6625
  • Toualbi K, Güller MC, Mauriz JL, Labalette C, Buendia MA, et al.: Physical and functional cooperation between AP-1 and β-catenin for the regulation of TCF-dependent gene. Oncogene 26, 3492–3502, 2007. doi:10.1038/sj.onc.1210133
  • Shibuya M, Yokota J, and Ueyama Y: Amplification and expression of a cellular oncogene (c-myc) in human gastric adenocarcinoma cells. Mol Cell Biol 5(2), 414–418, 1985. doi: 10.1128/MCB.5.2.414
  • Yochum GS: Multiple Wnt/ß-catenin responsive enhancers align with the myc promoter through long-range chromatin loops. PLoS ONE 6(4), e18966, 2011. doi: 10.1371/journal.pone.0018966
  • Dang CV: MYC on the path to cancer. Cell 149, 22–35, 2012. doi: 10.1016/j.cell.2012.03.003
  • Li YJ, Gao Q, Yin G, Ding X, and Hao J: WNT/β-catenin-signaling pathway stimulates the proliferation of cultured adult human sertoli cells via upregulation of c-myc expression. Reprod Sci 19(11), 1232–1240, 2012. doi: 10.1177/1933719112447126
  • Zhang S, Li YJ, Wu Y, Shi K, Bing L, et al.: Wnt/β-catenin signaling pathway upregulates c-myc expression to promote cell proliferation of P19 Teratocarcinoma Cells. Anat Rec 295, 2104–2113, 2012. doi: 10.1002/ar.22592
  • Lowy AM, Clements WM, Bishop J, Kong L, Bonney T, et al.: β-catenin/Wnt signaling regulates expression of the membrane type 3 matrix metalloproteinase in gastric cancer. Cancer Res 66(9), 4734–4741, 2006. doi:10.1158/0008-5472.CAN-05-4268
  • Ingraham CA, Park GC, Maarenkova HP, and Crossin KL: Matrix metalloproteinase (MMP)-9 induced by Wnt signaling increases the proliferation and migration of embryonic neural stem cells at low O2 levels. J Biol Chem 286(20), 17649–17657, 2011. doi: 10.1074/jbc.M111.229427
  • Park KS, Kim SJ, Kim KH, and Kim JC: Clinical characteristics of TIMP2, MMP2, and MMP9 gene polymorphisms in colorectal cancer. J Gastroenterol Hepatol 26(2), 391–397, 2011. doi: 10.1111/j.1440-1746.2010.06504.x
  • Vidya Priyadarsini R, Murugan RS, and Nagini S: Aberrant activation of Wnt/β-catenin signaling pathway contributes to the sequential progression of DMBA-induced HBP carcinomas. Oral Oncol 48, 33–39, 2012. doi: 10.1016/j.oraloncology.2011.08.008
  • Lee MA, Park J, Rhyu S, Oh S, Kang W, et al.: Wnt3a expression is associated with MMP-9 expression in primary tumor and metastatic site in recurrent or stage IV colorectal cancer. BMC Cancer 14, 125–131, 2014. doi: 10.1186/1471-2407-14-125
  • Kessenbrock K, Dijkgraaf D, Lawson D, Littlepage L, Shahi P, et al.: A role for matrix metalloproteinases in regulating mammary stem cell function via the Wnt signaling pathway. Cell Stem Cell 13(3), 300–313, 2013. doi: 10.1016/j.stem.2013.06.005
  • Brabletz T, Jung A, Dag S, Hlubek F, and Kirchner T: β-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am J Pathol 155(4), 1033–1038, 1999. doi: https://doi.org/10.1016/S0002-9440(10)65204-2
  • Li YJ, Wei ZM, Meng YX, and Ji XR: β-catenin up-regulates the expression of cyclinD1, c-myc and MMP-7 in human pancreatic cancer: Relationships with carcinogenesis and metastasis. World Gastroenterol 11(14), 2117–2123, 2005. doi: 10.3748/wjg.v11.i14.2117
  • Hlubek F, Spaderna S, Jung A, Kirchner T, and Brabletz T: β-Catenin activates a coordinated expression of the proinvasive factors laminin-5 γ 2 chain and MT1-MMP in colorectal carcinomas. Int J Cancer 108, 321–326, 2004. doi: 10.1002/ijc.11522
  • Ahokas K, Skoog T, Suomela S, Jeskanen L, Impola U, et al.: Matrilysin-2 (Matrix Metalloproteinase-26) is upregulated in keratinocytes during wound repair and early skin carcinogenesis. J Invest Dermatol 124, 849–856, 2005. doi: 10.1111/j.0022-202X.2005.23640.x
  • Marchenko ND, Marchenko GN, Weinberg RN, Lindsey JD, Kyshtoobayeva A, et al.: β-catenin regulates the gene of MMP-26, a novel matrix metalloproteinase expressed both in carcinomas and normal epithelial cells. Int J Biochem Cell Biol 36, 942–956, 2004. doi: 10.1016/j.biocel.2003.12.007
  • Mann B, Gelos M, Siedow A, Hanski M, Gratchev A, et al.: Target genes of β-catenin-T-cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. PNAS 96(4), 1603–1609, 1999. doi: 10.1073/pnas.96.4.1603
  • Correa S, Binato R, Du Rocher B, Castelo-Branco MT, Pizzatti L, et al.: Wnt/β-catenin pathway regulates ABCB1 transcription in chronic myeloid leukemia. BMC Cancer 12(303), 2012. doi: 10.1186/1471-2407-12-303
  • Seike M, Kondo T, Mori Y, Gemma A, Kudoh S, et al.: Proteomic analysis of intestinal epithelial cells expressing stabilized β-catenin. Cancer Res 63, 4641–4647, 2003.
  • Miwa N, Furuse M, Tsukita S, Niikawa N, Nakamura Y, et al.: Involvement of claudin-1 in β-catenin/TCF signaling pathway and its frequent upregulation in human colorectal cancers. Oncol Res 12, 469–476, 2001. doi: 10.3727/096504001108747477.
  • Xu L, Corcoran R, Welsh J, Pennica D, and Levine A: WISP-1 is a Wnt-1- and β-catenin-responsive oncogene. Genes Dev 14(5), 585–595, 2000. doi: 10.1101/gad.14.5.585
  • Renard C, Labalette C, Armengol C, Cougot D, Wei Y, et al.: Tbx3 is a downstream target of the Wnt/β-catenin pathway and a critical mediator of β-catenin survival functions in liver cancer. Cancer Res 67(3), 901–910, 2007. doi: 10.1158/0008-5472.CAN-06-2344
  • Leow CC, Romero MS, Ross S, Polakis P, and Gao WQ: Hath1, down-regulated in colon adenocarcinomas, inhibit proliferation and tumorigenesis colon cancer cells. Cancer Res 64, 6050–6057, 2004. doi: 10.1158/0008-5472.CAN-04-0290
  • Koh TJ, Bulitta CJ, Fleming JV, Dockray GJ, Varro A, et al.: Gastrin is a target of the β-catenin/TCF-4 growth-signaling. J Clin Invest 106(4), 533–539, 2000. doi: 10.1172/JCI9476
  • Kim PJ, Plescia J, Clevers H, Fearon ER, and Altieri DC: Survivin and molecular pathogenesis of colorectal cancer. Lancet 19(362), 205–209, 2003. doi: https://doi.org/10.1016/S0140-6736(03)13910-4
  • Gambini J, Inglés M, Olaso G, Lopez-Grueso R, Bonet-Costa V, et al.: Properties of resveratrol: In vitro and in vivo studies about metabolism, bioavailability, and biological effects in animal models and humans. Oxid Med Cell Longev 2015, 837042, 2015. doi: 10.1155/2015/837042
  • Nifli AP, Kampa M, Alexaki VI, Notas G, and Castanas E: Polyphenol interaction with the T47D human breast cancer cell line. J Dairy Res 72, 44–50, 2005. doi: 10.1017/S0022029905001172
  • Abourashed EA: Bioavailability of plant-derived antioxidants. Antioxidants 2(4), 309–325, 2013. doi: 10.3390/antiox2040309
  • Gonzales GB: In vitro bioavailability and cellular bioactivity studies of flavonoids and flavonoid-rich plant extracts: questions, considerations and future perspectives. Proc Nutr Soc, 75, 1–7, 2016. doi: 10.1017/S0029665116002858.
  • Walgren RA, Walle UK, and Walle T: Transport of quercetin and its glucosides across human intestinal epithelial Caco-2 cells. Biochem Pharmacol 55(10), 1721–1727, 1998.
  • Fridlender M, Kapulnik Y, and Koltai H: Plant derived substances with anti-cancer activity: from folklore to practice. Front Plant Sci 6, 799, 2015. doi: 10.3389/fpls.2015.00799
  • Miri A, Monsef-Esfahani H, Amini M, Amanzadeh Y, Hadjiakhoondi A, et al.: Comparative chemical composition and antioxidant properties of the essential oils and aromatic water from Teucrium persicum boiss. Iran J Pharm Res 11(2), 573–581, 2012.
  • Kadifkova Panovska T, Kulevanova S, and Stefova M: In vitro antioxidant activity of some Teucrium species (Lamiaceae). Acta Pharm 55, 207–214, 2005.
  • Rajabalian S: Methanolic extract of Teucrium polium L. potentiates the cytotoxic and apoptotic effects of anticancer drugs of vincristine, vinblastine and doxorubicin against a panel of cancerous cell lines. Exp Oncol 30(2), 133–138, 2008.
  • Stankovic MS, Curcic MG, Zizic JR, Topuzovic MD, Solujic SR, et al.: Teucrium plant species as natural sources of novel anticancer compounds: antiproliferative, proapoptotic and antioxidant properties. Int J Mol Sci 12, 4190–4205, 2011. doi: 10.3390/ijms12074190
  • Moghtader M: Chemical composition of the essential oil of Teucrium polium L. from Iran. Am-Eurasian J Agric Environ Sci 5(6), 843–846, 2009.
  • Menichini F, Conforti F, Rigano D, Formisano C, Piozzi F, et al.: Phytochemical composition, anti-inflammatory and antitumour activities of four Teucrium essential oils from Greece. Food Chem 115(2), 679–686, 2009. doi:10.1016/j.foodchem.2008.12.067
  • Jana S, Patra K, Sarkar S, Jana J, Mukherjee G, et al.: Antitumorigenic potential of linalool is accompanied by modulation of oxidative stress: an in vivo study in sarcoma-180 solid tumor model. Nutr Cancer 66(5), 835–848, 2014. doi: 10.1080/01635581.2014.904906
  • Russo EB and Taming THC: Potential cannabis synergy and phytocannabinoid-terpenoid entourage effects. Br J Pharmacol 163(7), 1344–1364, 2011. doi: 10.1111/j.1476-5381.2011.01238.x
  • Gunaseelan S, Balupillai A, Govindasamy K, Muthusamy G, Ramasamy K, et al.: The preventive effect of linalool on acute and chronic UVB-mediated skin carcinogenesis in Swiss albino mice. Photochem Photobiol Sci 15(7), 851–860, 2016. doi: 10.1039/c6pp00075d
  • Kusuhara M, Urakami K, Masuda Y, Zangiacomi V, Ishi H, et al.: Fragrant environment with α-pinene decreases tumor growth in mice. Biomed Res 33(1), 57–61, 2012.
  • Amirghofran Z, Zand F, Javidnia K, and Miri R: The cytotoxic activity of various herbals against different tumor cells: an in vitro study. IRCMJ 12(3), 260–265, 2010.
  • Nieto MA: The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu Rev Cell Dev Biol 27, 347–376, 2011. doi: 10.1146/annurev-cellbio-092910-154036
  • Borek C: Antioxidant health effects of aged garlic extract. J Nutr 131(3s), 1010S–1015S, 2001.
  • Knowles LM AND Milner JA: Possible mechanism by which allyl sulfides suppress neoplastic cell proliferation. J Nutr 131(3s), 1061S–1066S, 2001.
  • Imai J, Ide N, Nagae S, Moriguchi T, Matsuura H, and Itakura Y: Antioxidant and radical scavenging effects of aged garlic extract and its constituents. Planta Med 60(5), 417–420, 1994. doi: 10.1055/s-2006-959522
  • Nagae S, Ushijima M, Hatono S, Imai J, Kasuga S, et al.: Pharmacokinetics of the garlic compound S-allylcysteine. Planta Med 60(3), 214–217, 1994. doi: 10.1055/s-2006-959461
  • Amagase H, Petesch BL, Matsuura H, Kasuga S, Itakura Y: Intake of garlic and its bioactive components. J Nutr 131(3s), 955S–962S, 2001.
  • Lawson LD, Ransom DK, and Hughes BG: Inhibition of whole blood platelet-aggregation by compounds in garlic clove extracts and commercial garlic products. Thromb Res 65(2), 141–156, 1992.
  • Hong Y, Ham Y, Choi J, and Kim J: Effects of allyl sulfur compounds and garlic extract on the expressions of Bcl-2, Bax, and p53 in non small cell lung cancer cell lines. Exp Mol Med 32(3), 127–134, 2000. doi:10.1038/emm.2000.22
  • Xiao D, Pinto JT, Gundersen GG, and Weinstein IB: Effects of a series of organosulfur compounds on mitotic arrest and induction of apoptosis in colon cancer cells. Mol Cancer Ther 4(9), 1388–1398, 2005. doi: 10.1158/1535-7163.MCT-05-0152
  • Martino AD, Filomeni G, Aquilano K, Ciriolo MR, and Rotilio G: Effects of water garlic extracts on cell cycle and viability of HepG2 hepatoma cells. J Nutr Biochem 17, 742–749, 2006. doi: 10.1016/j.jnutbio.2005.12.005
  • Reddy B, Rao C, Rivenson A, and Kelloff G: Chemoprevention of colon carcinogenesis by organosulfur compounds. Cancer Res 53, 3493–3498, 1993.
  • Sundaram S and Milner J: Diallyl disulfide induces apoptosis of human colon tumor cells. Carcinogenesis 17, 669–673, 1996. doi: 10.1093/carcin/17.4.669
  • Chu Q, Ling M, Feng H, Cheung HW, Tsao SW, et al.: A novel anticancer effect of garlic derivatives: inhibition of cancer cell invasion through restoration of E-cadherin expression. Carcinogenesis 27(1), 2180–2189, 2006. doi:10.1093/carcin/bgl054
  • Lund T, Stokke T, Olsen Ø, and Fodstad Ø: Garlic arrests MDA-MB-435 cancer cells in mitosis, phosphorylates the proapoptotic BH3-only protein BimEL and induces apoptosis. Br J Cancer 92, 1773–1781, 2005. doi: 10.1038/sj.bjc.6602537
  • Wu X, Kassie F, and Mersch-Sundermann V: Induction of apoptosis in tumor cells by naturally occurring sulfur-containing compounds. Mutat Res 589, 81–102, 2005. doi:10.1016/j.mrrev.2004.11.001
  • Nian H, Delage B, Pinto JT, and Dashwood RH: Allyl mercaptan, a garlic-derived organosulfur compound, inhibits histone deacetylase and enhances Sp3 binding on the P21WAF1 promoter. Carcinogenesis 29(9), 1816–1824, 2008. doi: 10.1093/carcin/bgn165
  • Ng KT, Guo DY, Cheng Q, Geng W, Ling CC, et al.: A garlic derivative, s-allylcysteine (SAC), suppresses proliferation and metastasis of hepatocellular carcinoma. PLoS ONE 7(2), 31655, 2012. doi: 10.1371/journal.pone.0031655
  • Katsuki T, Hirata K, Ishikawa H, Matsuura N, Sumi SI, and Itoh H: Aged garlic extract has chemopreventative effects on 1, 2-dimethylhydrazine-induced colon tumors in rats. J Nutr 136(3), 847s–851s, 2006.
  • Chu Q, Lee DT, Tsao SW, Wang X, and Wong YC: S-allylcysteine, a water-soluble garlic derivative, suppresses the growth of a human androgen-independent prostate cancer xenograft, CWR22R, under in vivo conditions. BJU Int 99(4), 925–932, 2007. doi: 10.1111/j.1464-410X.2006.06639.x
  • Tang H, Kong Y, Guo J, Tang Y, Xie X, et al.: Diallyl disulfide suppresses proliferation and induces apoptosis in human gastric cancer through Wnt-1 signaling pathway by up-regulation of miR-200b and miR-22. Cancer Lett 340(1), 72–81, 2013. doi: 10.1016/j.canlet.2013.06.027
  • Huang J, Yang B, Xiang T, Peng W, Qiu Z, et al.: Diallyl disulfide inhibits growth and metastatic potential of human triple-negative breast cancer cells through inactivation of the β-catenin signaling pathway. Mol Nutr Food Res 59(6), 1063–1075, 2015. doi: 1002/mnfr.201400668.
  • Singh SV, Powolny AA, Stan SD, Xiao D, Arlotti JA, et al.: Garlic constituent diallyl trisulfide prevents development of poorly differentiated prostate cancer and pulmonary metastasis multiplicity in TRAMP mice. Cancer Res 68(22), 9503–9510, 2008. doi: 10.1158/0008-5472.CAN-08-1677
  • Wang C, Fu M, and Pestell RG: Histone acetylation/deacetylation as a regulator of cell cycle gene expression. Methods Mol Biol 241, 207–216, 2004. doi: 10.1385/1-59259-646-0:207
  • Verdone L, Caserta M, and Ci Moure E: Role of histone acetylation in the control of gene expression. Biochem Cell Biol 83(3), 344–353, 2005. doi: 10.1139/o05-041
  • Taddei A, Roche D, Bickmore WA, and Almouzni G: The effects of histone deacetylase inhibitors on heterochromatin: implications for anticancer therapy? EMBO Rep 6(6), 520–524, 2005. doi: 10.1038/sj.embor.7400441
  • Marchino D and Münster P: Development of histone deacetylase inhibitors for cancer treatment. Expert Rev Anticancer Ther 7(4), 583–598, 2007. doi: 10.1586/14737140.7.4.583
  • Peinado H, Ballestar E, Esteller M, and Cano A: Snail mediates E-cadherin repression by the recruitment of the sin3a/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol 24(1), 306–319, 2004. doi: 10.1128/MCB.24.1.306-319.2004
  • Von Burstin J, Eser S, Paul MC, Seidler B, Brandl M, and Messer M: E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex. Gastroenterology 137, 361–371, 2009. doi: 10.1053/j.gastro.2009.04.004
  • ten Berge D, Koole W, Fuerer C, Fish M, Eroglu E, et al.: Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 3(5), 508–518, 2008. doi: 10.1016/j.stem.2008.09.013
  • Yook JI, Li XY, Ota I, Fearon ER, and Weiss SJ: Wnt-dependent regulation of the E-cadherin repressor snail. J Biol Chem 280(12), 11740–11748, 2005. doi: 10.1074/jbc.M413878200
  • Galva JA, Astudillo A, Vallina A, Fonseca PJ, Gómez-Izquierdo L, et al.: Epithelial-mesenchymal transition markers in the differential diagnosis of gastroenteropancreatic neuroendocrine tumors. Am J Clin Pathol 140, 61–72, 2013. doi: 10.1309/AJCPIV40ISTBXRAX
  • Billin AN, Thirwell H, and Ayer DE: β-catenin–histone deacetylase interactions regulate the transition of LEF1 from a transcriptional repressor to an activator. Mol Cell Biol 20(18), 6882–6890, 2000. doi: 10.1128/MCB.20.18.6882-6890.200
  • Anupama M, Murgan SS, and Murthy PB: Broccoli flower head extract reduces mitomycin-C induced sister chromatid exchange in cultured human lymphocytes. Food Chem Toxicol 46, 3351–3353, 2008. doi: 10.1016/j.fct.2008.08.009
  • Tarozzi A, Angeloni C, Malaguti M, Morroni F, Hrelia S, et al.: Sulforaphane as a potential protective phytochemical against neurodegenerative diseases. Oxid Med Cell Longev 2013, 1–10, 2013. doi: https://doi.org/10.1155/2013/415078
  • Clarke JD, Dashwood RH, and Ho E: Multi-targeted prevention of cancer by sulforaphane. Cancer Lett 269(2), 291–304, 2008. doi: 10.1016/j.canlet.2008.04.018
  • Zhang Y and Tang L: Discovery and development of sulforaphane as a cancer chemopreventive phytochemical. Acta Pharmacol Sin 28(9), 1343–1354, 2007. doi: 10.1111/j.1745-7254.2007.00679.x
  • Myzak MC, Karplus PA, Chung FL, and Dashwood RH: A novel mechanism of chemoprotection by sulforaphane: inhibition of histone deacetylase. Cancer Res 64, 5767–5774, 2004. doi: 10.1158/0008-5472.CAN-04-1326
  • Singh AV, Xiao D, Lew KL, Dhir R, and Singh SV: Sulforaphane induces caspase-mediated apoptosis in cultured PC-3 human prostate cancer cells and retards growth of PC-3 xenografts in vivo. Carcinogenesis 25(1), 83–90, 2004. doi: 10.1093/carcin/bgg178
  • Iglesias JM, Beloqui I, Garcia-Garcia F, Leiz O, Vazquez-Martin A, et al.: Mammosphere formation in breast carcinoma cell lines depends upon expression of E-cadherin. PLoS ONE 8(10), e77281, 2013. doi: 10.1371/journal.pone.0077281
  • Raha D, Wilson TR, Peng J, Peterson D, Yue P, et al.: The cancer stem cell marker aldehyde dehydrogenase is required to maintain a drug-tolerant tumor cell subpopulation. Cancer Res 74(13), 3579–3590, 2014. doi: 10.1158/0008-5472.CAN-13-3456
  • Ma I and Allan AL: The role of human aldehyde dehydrogenase in normal and cancer stem cells. Stem Cell Rev Rep 7, 292–306, 2011. doi: 10.1007/s12015-010-9208-4
  • Li Y, Zhang T, Korkaya H, Liu S, Lee HF, et al.: Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res 16(9), 2580–2590, 2010. doi: 10.1158/1078-0432.CCR-09-2937
  • Hu R, Khor TO, Shen G, Jeong WS, Hebbar V, et al.: Cancer chemoprevention of intestinal polyposis in ApcMin/+ mice by sulforaphane, a natural product derived from cruciferous vegetable. Carcinogenesis 27(10), 2038–2046, 2006. doi: 10.1093/carcin/bgl049
  • Shan Y, Zhang L, Bao Y, Li B, He C, et al.: Epithelial-mesenchymal transition, a novel target of sulforaphane via COX-2/MMP2, 9/Snail, ZEB1 and miR-200c/ZEB1 pathways in human bladder cancer cells. J Nutr Biochem 24, 1062–1069, 2013. doi: 10.1016/j.jnutbio.2012.08.004
  • Park SM, Gaur AB, Lengyel E, and Peter ME: The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22, 894–907, 2008. doi: 10.1101/gad.1640608
  • Meng Q, Goldberg ID, Rosen EM, and Fan S: Inhibitory effects of Indole-3-carbinol on invasion and migration in human breast cancer cells. Breast Cancer Res Treat 63, 147–152, 2000. doi: 10.1023/A:1006495824158
  • Meng Q, Qi M, Chen D, Yuan R, Goldberg G, et al.: Suppression of breast cancer invasion and migration by indole-3-carbinol: associated with up-regulation of BRCA1 and E-cadherin/catenin complexes. J Mol Med 78, 155–165, 2000. doi:10.1007/s001090000088
  • Yang Z, Kulkarni K, Zhu W, and Hu M: Bioavailability and pharmacokinetics of genistein: mechanistic studies on its ADME. Anticancer Agents Med Chem 12(10), 1264–1280, 2012. doi: 10.2174/187152012803833107
  • Yang X, Belosay A, Hartman JA, Song H, Zhang Y, et al.: Dietary soy isoflavones increase metastasis to lungs in an experimental model of breast cancer with bone micro-tumors. Clin Exp Metastasis 32(4), 323–333, 2015. doi: 10.1007/s10585-015-9709-2
  • Andrade JE, Ju YH, Baker C, Doerge DR, and Helferich WG: Long-term exposure to dietary sources of genistein induces estrogen-independence in the human breast cancer (MCF-7) xenograft model. Mol Nutr Food Res 59(3), 413–423, 2014. doi: 10.1002/mnfr.201300780
  • 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(4), 895–901, 2012. doi: 10.1093/carcin/bgs017
  • Nakamura A, Aizawa J, Sakayama K, Kidani T, Takata T, et al.: Genistein inhibits cell invasion and motility by inducing cell differentiation in murine osteosarcoma cell line LM8. BMC Cell Biol 13(24), 2012. doi: 10.1186/1471-2121-13-24
  • Gu Y, Zhu CF, Iwamoto H, Chen JS: Genistein inhibits invasive potential of human hepatocellular carcinoma by altering cell cycle, apoptosis, and angiogenesis. World J Gastroenterol 11(41), 6512–6517, 2005. doi: 10.3748/wjg.v11.i41.6512
  • deVere White RW1, Hackman RM, Soares SE, Beckett LA, Li Y, et al.: Effects of a genistein-rich extract on PSA levels in men with a history of prostate cancer. Urology 63(2), 259–263, 2004. doi: 10.1016/j.urology.2003.09.061
  • Kidani T, Nakamura A, Kamei S, Norimatsu Y, Miura H, et al.: Overexpression of cytoplasmic β-catenin inhibits the metastasis of the murine osteosarcoma cell line LM8. Cancer Cell Int 14(31), 2014. doi:10.1186/1475-2867-14-31.
  • Zhang J, Cao H, Zhang B, Cao H, Xu X, et al.: Berberine potently attenuates intestinal polyps growth in ApcMin mice and familial adenomatous polyposis patients through inhibition of Wnt signalling. J Cell Mol Med 17(11), 1484–1493, 2013. doi: 10.1111/jcmm.12119
  • Liu C, Tang W, Sia P, Huang C, Yang P, et al.: Berberine inhibits the metastatic ability of prostate cancer cells by suppressing epithelial-to-mesenchymal transition (EMT)-associated genes with predictive and prognostic relevance. Int J Med Sci 12(1), 63–71, 2015. doi:10.7150/ijms.9982
  • Misikangas M, Pajari A, Päivärinta E, Oikarinen SI, Rajakangas J, et al.: Three nordic berries inhibit intestinal tumorigenesis in multiple intestinal neoplasia/+ mice by modulating beta-catenin signaling in the tumor and transcription in the mucosa. J Nutr, 137(10), 2285–2290, 2007.
  • Lee S, Richardson RL, Dashwood RH, and Baek SJ: Capsaicin represses transcriptional activity of β-catenin in human colorectal cancer cells. J Nutr Biochem 23, 646–655, 2012. doi: 10.1016/j.jnutbio.2011.03.009
  • Wutka A, Palagani V, Barat S, Chen X, El Khatib M, et al.: Capsaicin treatment attenuates cholangio carcinoma carcinogenesis. PLoS ONE 9(4), e95605, 2014. doi: 10.1371/journal.pone.0095605
  • Anitha P, Priyadarsini RV, Kavitha K, Thiyagarajan P, and Nagini S: Ellagic acid coordinately attenuates Wnt/β-catenin and NF-κB signaling pathways to induce intrinsic apoptosis in an animal model of oral oncogenesis. Eur J Nutr 52, 75–84, 2013. doi: 10.1007/s00394-011-0288-y
  • Way T, Huang J, Chou C, Huang C, Yang M, et al.: Emodin represses TWIST1-induced epithelial–mesenchymal transitions in head and neck squamous cell carcinoma cells by inhibiting the β-catenin and Akt pathways. Eur J Cancer 50, 366–378, 2014. doi: 10.1016/j.ejca.2013.09.025
  • Yang G, Liao J, Kim K, Yurkow EJ, and Yang CS: Inhibition of growth and induction of apoptosis in human cancer cell lines by tea polyphenols. Carcinogenesis 19(4), 611–616, 1998. doi: 10.1093/carcin/19.4.611
  • Zhang G, Miura Y, and Yagasaki K: Induction of apoptosis and cell cycle arrest in cancer cells by in vivo metabolites of teas. Nutr Cancer 38(2), 265–273, 2000. doi: 10.1207/S15327914NC382_16
  • Khan N, Afaq F, Saleem M, Ahmad N, and Mukhtar H: Targeting multiple signaling pathways by green tea polyphenol (−)-Epigallocatechin-3-Gallate. Cancer Res 66(5), 2500–2505, 2006. doi: 10.1158/0008-5472.CAN-05-3636
  • Belguise K, Guo S, and Sonenshein G: Activation of FOXO3a by the green tea polyphenol epigallocatechin-3-gallate induces estrogen receptor A expression reversing invasive phenotype of breast cancer cells. Cancer Res 67(12), 5763–5770, 2007. doi: 10.1158/0008-5472.CAN-06-4327
  • Oh S, Gwak J, Park SM, and Yang C: Green tea polyphenol EGCG suppresses Wnt/β-catenin signaling by promoting GSK-3β- and PP2A-independent β-catenin phosphorylation/degradation. Biofactors 40(6), 586–595, 2014. doi: 10.1002/biof.1185
  • Ray S, Chattopadhyay N, Mitra A, Siddiqi M, and Chatterjee A: Curcumin exhibits antimetastatic properties by modulating integrin receptors, collagenase activity, and expression of Nm23 and E-cadherin. J Environ Pathol Toxicol Oncol 22(1), 49–58, 2003. doi: 10.1615/JEnvPathToxOncol.v22.i1.50
  • Chen H, Lee J, Huang J, Wang C, Chen W, et al.: Curcumin inhibits lung cancer cell invasion and metastasis through the tumor suppressor HLJ1. Cancer Res 68(18), 7428–7438, 2008. doi: 10.1158/0008-5472.CAN-07-6734
  • Goel A, Kunnumakkara AB, and Aggarwal BB: Curcumin as ′‘Curecumin′': From kitchen to clinic. Biochem Pharmacol 75, 787–809, 2008. doi:10.1016/j.bcp.2007.08.016
  • Basile V, Ferrari E, Lazzari S, Belluti S, Pignedoli F, et al.: Curcumin derivatives: Molecular basis of their anti-cancer activity. Biochem Pharmacol 78, 1305–1315, 2009. doi: 10.1016/j.bcp.2009.06.105
  • Lee SJ, Krauthauser C, Maduskuie V, Fawcett PT, Olson JM, and Rajasekaran SA: Curcumin-induced HDAC inhibition and attenuation of medulloblastoma growth in vitro and in vivo. BMC Cancer 11(144), 2011. doi: 10.1186/1471-2407-11-144.
  • Mukherjee S, Mazumdar M, Chakarborty S, Manna A, Saha S, et al.: Curcumin inhibits breast cancer stem cell migration by amplifying the E-cadherin/β-catenin negative feedback loop. Stem Cell Res Ther 5(116), 2014. doi: 10.1186/scrt506
  • Sartippour MR, Seerman NP, Rao JY, Moro A, Harris DM, et al.: Ellagitannin-rich pomegranate extract inhibits angiogenesis in prostate cancer in vitro and in vivo. Int J Oncol 32, 475–480, 2008. doi: 10.3892/ijo.32.2.475
  • Wang L, Alcon A, Yuan H, Ho J, Li Q, et al.: Cellular and molecular mechanisms of pomegranate juice-induced anti-metastatic effect on prostate cancer cells. Integr Biol 3(7), 742–754, 2011. doi: 10.1039/c0ib00122h
  • Nair HK, Rao KV, Aalinkeel R, Mahajan S, Chawda R, et al.: Inhibition of prostate cancer cell colony formation by the flavonoid quercetin correlates with modulation of specific regulatory genes. Clin Diagn Lab Immunol 11(1), 63–69, 2004. doi: 10.1128/CDLI.11.1.63-69.2004
  • Park CH, Chang JY, Hahn ER, Park S, Kim H, et al.: Quercetin, a potent inhibitor against β-catenin/Tcf signaling in SW480 colon cancer cells. Biochem Biophys Res Commun 328, 227–234, 2005. doi: 10.1016/j.bbrc.2004.12.151
  • Amado NG, Predes D, Fonseca BF, Cerqueira DM, Reis AH, et al.: Isoquercitrin suppresses colon cancer cell growth in vitro by targeting the Wnt/β-catenin signaling pathway. J Biol Chem 289(51), 35456–35467, 2014. doi: 10.1074/jbc.M114.621599
  • Slater M, Brown D, and Husband A: In the prostatic epithelium, dietary isoflavones from red clover significantly increase estrogen receptor β and E-cadherin expression but decrease transforming growth factor β1. Prostate Cancer Prostatic Dis 5, 16–21, 2002. doi: 10.1038/sj.pcan.4500546
  • Zhang L, Li L, Wu D, Fan J, Li X, et al.: A novel anti-cancer effect of genistein: reversal of epithelial mesenchymal transition in prostate cancer cells. Acta Pharmacol Sin 29(9), 1060–1068, 2008. doi: 10.1111/j.1745-7254.2008.00831.x
  • Yuan-Jing F, Nan-Shan H, and Lian X: Genistein synergizes with RNA interference inhibiting survivin for inducing DU-145 of prostate cancer cells to apoptosis. Cancer Lett 284, 189–197, 2009. doi: 10.1016/j.canlet.2009.04.024
  • Liss MA, Schlicht M, Kahler A, Fitzgerald R, Thomassi T, et al.: Characterization of soy-based changes in Wnt-frizzled signaling in prostate cancer. Cancer Genomics Proteomics 7(5), 245–252, 2010.
  • Brack ME, Boterberg T, Depypere HT, Stove C, Leclercq G, et al.: The citrus methoxyflavone tangeretin affects human cell-cell interactions. Adv Exp Med Biol 505, 135–139, 2002. doi: 10.1007/978-1-4757-5235-9_12
  • Pan M, Chen W, Lin-Shiau S, Ho C, and Lin J: Tangeretin induces cell-cycle G1 arrest through inhibiting cyclin-dependent kinases 2 and 4 activities as well as elevating Cdk inhibitors p21 and p27 in human colorectal carcinoma cells. Carcinogenesis 23(10), 1677–1684, 2002. doi: 10.1093/carcin/23.10.1677
  • Shankar S, Nall D, Tang S, Meeker D, Passarini J, et al.: Resveratrol inhibits pancreatic cancer stem cell characteristics in human and KrasG12D transgenic mice by inhibiting pluripotency maintaining factors and epithelial-mesenchymal transition. PLoS ONE 6(1), e16530, 2011. doi: 10.1371/journal.pone.0016530
  • Chen HJ, Hsu LS, Lin MW, and Lin CM: The β-catenin/TCF complex as a novel target of resveratrol in the Wnt/β-catenin signaling pathway. Biochem Pharmacol 84(9), 1143–1153, 2012. doi:10.1016/j.bcp.2012.08.011
  • Ji Q, Liu X, Fu X, Zhang L, Sui H, et al.: Resveratrol inhibits invasion and metastasis of colorectal cancer cells via MALAT1 mediated Wnt/β-catenin signal pathway. PLoS ONE 8(11), e78700, 2013. doi: 10.1371/journal.pone.0078700
  • Saleem M, Murtaza I, Tarapore RS, Suh Y, Adhami VM, et al.: Lupeol inhibits proliferation of human prostate cancer cells by targeting β-catenin signaling. Carcinogenesis 30(5), 808–817, 2009. doi: 10.1093/carcin/bgp044
  • Tarapore RS, Siddiqui IA, Adhami VM, Spiegelman VS, and Mukhtar H: The dietary terpene lupeol targets colorectal cancer cells with constitutively active Wnt/β-catenin signaling. Mol Nutr Food Res 57(11), 1950–1958, 2013. doi: 10.1002/mnfr.201300155
  • Wertz K: Lycopene effects contributing to prostate health. Nutr Cancer 61(6), 775–783, 2009. doi: 10.1080/01635580903285023
  • El-Rouby D: Histological and immunohistochemical evaluation of the chemopreventive role of lycopene in tongue carcinogenesis induced by 4-nitroquinoline-1-oxide. Arch Oral Biol 56(7), 664–671, 2011. doi: 10.1016/j.archoralbio.2010.12.007
  • Tang FY, Pai MH, and Wang XD: Consumption of lycopene inhibits the growth and progression of colon cancer in a mouse xenograft model. J Agric Food Chem 59(16), 9011–9021, 2011. doi: 10.1021/jf2017644
  • Zhang LR, Chen W, and Li X: A novel anticancer effect of butein: Inhibition of invasion through the ERK1/2 and NF-κB signaling pathways in bladder cancer. FEBS Lett 582, 1821–1828, 2008. doi: 10.1016/j.febslet.2008.04.046
  • Moran AE, Carothers AM, Weyant MJ, Redston M, and Bertagnolli MM: Carnosol inhibits β-catenin tyrosine phosphorylation and prevents adenoma formation in the C57BL/6J/Min/+ (Min/+) mouse. Cancer Res 65(3), 1097–1104, 2005.
  • de La Roche M, Rutherford TJ, Gupta D, Veprintsev DB, Saxty B, et al.: An intrinsically labile α-helix abutting the BCL9-binding site of β-catenin is required for its inhibition by carnosic acid. Nat Commun 3(680), 2012. doi: 10.1038/ncomms1680.
  • Thakur R and Mishra DP: Pharmacological modulation of beta-catenin and its applications in cancer therapy. J Cell Mol Med 17(4), 449–456, 2013. doi: 10.1111/jcmm.12033
  • Weng J, Tsai C, Kulp SK, and Chen C: Indole-3-carbinol as a chemopreventive and anti-cancer agent. Cancer Lett 262, 153–163, 2008. doi: 10.1016/j.canlet.2008.01.033
  • Jeong YM, Li H, Kim SY, Yun HY, Baek KJ, et al.: Indole-3-carbinol inhibits prostate cancer cell migration via degradation of β-Catenin. Oncol Res 19(5), 237–243, 2011. doi: https://doi.org/10.3727/096504011×12970940207922
  • Mauro L, Catalano S, Bossi G, Pellegrino M, Barone I, et al.: Evidences that leptin up-regulates E-cadherin expression in breast cancer: effects on tumor growth and progression. Cancer Res 67(7), 3412–3421, 2007. doi: 10.1158/0008-5472.CAN-06-2890
  • Pan H, Guo J, and Su Z: Advances in understanding the interrelations between leptin resistance and obesity. Physiol Behav 130, 157–169, 2014. doi: 10.1016/j.physbeh.2014.04.003
  • Jiang WG, Hiscox S, Hallett MB, Horrobin DF, Mansel RE, et al.: Regulation of the expression of E-cadherin on human cancer cells by γ-linolenic acid (GLA). Cancer Res 55, 5043–5048, 1995.
  • Zhou Q, Yan B, Hu X, Li X, Zhang J, et al.: Luteolin inhibits invasion of prostate cancer PC3 cells through E-cadherin. Mol Cancer Ther 8(6), 1684–1691, 2009. doi: 10.1158/1535-7163.MCT-09-0191
  • Pandurangan AK, Dharmalingam P, Sadagopan SK, Ramar M, Munusamy A, et al.: Luteolin induces growth arrest in colon cancer cells through involvement of Wnt/β-catenin/GSK-3β signaling. J Environ Pathol Toxicol Oncol 32(2), 131–139, 2013. doi: 10.1615/JEnvironPatholToxicolOncol.2013007522
  • Pandurangan AK, Dharmalingam P, Sadagopan SK, et al.: Luteolin inhibits matrix metalloproteinase 9 and 2 in azoxymethane-induced colon carcinogenesis. Hum Exp Toxicol 33(11), 1176–1185, 2014. doi: 10.1177/0960327114522502
  • Pandurangan AK and Esa NM: Luteolin, a bioflvonoid inhibits colorectal cancer through modulation of multiple signaling pathways: a review. APJCP 15, 5501–5508, 2014. doi: https://doi.org/10.7314/APJCP.2014.15.14.5501
  • Deep G, Gangar SC, Agarwal C, and Agarwal R: Role of E-cadherin in antimigratory and antiinvasive efficacy of silibinin in prostate cancer cells. Cancer Prev Res 4(8), 1222–1232, 2011. doi: 10.1158/1940-6207.CAPR-10-0370
  • Wu K, Zeng J, Li L, Fan J, Zhang D, et al.: Silibinin reverses epithelial-to-mesenchymal transition in metastatic prostate cancer cells by targeting transcription factors. Oncol Rep 23, 1545–1552, 2010. doi: 10.3892/or_00000794
  • Vaid M, Prasad R, Sun Q, and Kartiyar SK: Silymarin targets β-catenin signaling in blocking migration/invasion of human melanoma cells. PLoS ONE 6(7), e23000, 2011. doi: 10.1002/mc.22092
  • Cufi S, Bonavia R, Vazquez-Martin A, Corominas-Faja B, Oliveras-Ferraros C, et al.: Silibinin meglumine, a water-soluble form of milk thistle silymarin, is an orally active anti-cancer agent that impedes the epithelial-to-mesenchymal transition (EMT) in EGFR-mutant non-small-cell lung carcinoma cells. Food Chem Toxicol 60, 360–368, 2013. doi: 10.1016/j.fct.2013.07.063
  • Mateen S, Raina K, Agarwal C, Chan D, and Agarwal R: Silibinin synergizes with histone deacetylase and DNA methyltransferase inhibitors in upregulating E-cadherin expression together with inhibition of migration and invasion of human non-small cell lung cancer cells. J Pharmacol Exp Ther 345, 206–214, 2013. doi: 10.1124/jpet.113.203471
  • Suh Y, Afaq F, Johnson JJ, and Mukhtar H: A plant flavonoid fisetin induces apoptosis in colon cancer cells by inhibition of COX2 and Wnt/EGFR/NF- kB-signaling pathways. Carcinogenesis 30(2), 300–307, 2009. doi: 10.1093/carcin/bgn269
  • Pal HC, Sharma S, Strickland LR, Katiyar SK, Ballestas ME, et al.: Fisetin inhibits human melanoma cell invasion through promotion of mesenchymal to epithelial transition and by targeting MAPK and NF-κB signaling pathways. PLoS ONE 9(1), e86338, 2014. doi: 10.1371/journal.pone.0086338
  • Lampen A, Leifheit M, Voss J, and Nau H: Molecular and cellular effects of cis-9, trans-11-conjugated linoleic acid in enterocytes: Effects on proliferation, differentiation, and gene expression. Biochim Biophys Acta 1735(1), 30–40, 2005. doi:10.1016/j.bbalip.2005.01.007
  • Bozzo F, Bocca C, Colombatta S, and Miglietta A: Antiproliferative effect of conjugated linoleic acid in caco-2 cells: Involvement of PPAR γ and APC/β-catenin pathways. Chem Biol Interact 169, 110–121, 2007. doi:10.1016/j.cbi.2007.05.010
  • Wang W, Liu H, Wang S, Hao X, and Li L: A diterpenoid derivative 15-oxospiramilactone inhibits Wnt/β-catenin signaling and colon cancer cell tumorigenesis. Cell Res 21, 730–740, 2011. doi:10.1038/cr.2011.30
  • Yan Z, Zhu Z, Wang J, Sun J, Chen Y, et al.: Synthesis, characterization, and evaluation of a novel inhibitor of WNT/β-catenin signaling pathway. Mol Cancer 12(1), 116, 2013. doi: 10.1186/1476-4598-12-116
  • Jiang M, Liao C, and Lee P: Aspirin inhibits matrix metalloproteinase-2 activity, increases E-cadherin production, and inhibits in vitro invasion of tumor cells. Biochem Biophys Res Commun 282, 671–677, 2001. doi:10.1006/bbrc.2001.4637
  • Goel A, Chang DK, Ricciardiello L, Gasche C, and Boland CR: A novel mechanism for aspirin-mediated growth inhibition of human colon cancer cells. Clin Cancer Res 9, 383–390, 2003.
  • Langley RE, Burdett S, Tierney JF, Cafferty F, Parmar MK, et al.: Aspirin and cancer: has aspirin been overlooked as an adjuvant therapy? Br J Cancer, 105(8), 1–7, 2011. doi: 10.1038/bjc.2011.289.
  • de Freitas Junior JC, Silva Bdu R, de Souza WF, de Arau´jo WM, Abdelhay ES, et al.: Inhibition of N-linked glycosylation by tunicamycin induces E-cadherin-mediated cell–cell adhesion and inhibits cell proliferation in undifferentiated human colon cancer cells. Cancer Chemother Pharmacol 68, 227–238, 2011. doi: 10.1007/s00280-010-1477-8
  • Waaler J, Machon O, von Kries JP, Wilson SR, Lundenes E, et al.: Novel synthetic antagonists of canonical Wnt signaling inhibit colorectal cancer cell growth. Cancer Res 71, 197–205, 2011. doi: 10.1158/0008-5472.CAN-10-1282
  • Palmer HG, González-Sancho JM, Espada J, Berciano MT, Puig I, et al.: Vitamin D3 promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition of β-catenin signaling. J Cell Biol 154(2), 369–387, 2001. doi: 10.1083/jcb.200102028
  • Li Y, Wu R, Wang X, and Chen W: Effects of retinoic acid on the β-catenin/TCF pathway in cultured porcine tracheobronchial epithelial cells. J Huazhong Univ Sci Technol Med Sci 24(5), 421–423, 2004. doi: 10.1007/BF02831097
  • Dillard AC and Lane MA: Retinol decreases β-catenin protein levels in retinoic acid-resistant colon cancer cell lines. Mol Carcinog 46, 315–329, 2004. doi: 10.1002/mc.20280
  • Yasuhara R, Yuasa T, Williams JA, Byers SW, Shah S, et al.: Wnt/β-Catenin and retinoic acid receptor signaling pathways interact to regulate chondrocyte function and matrix turnover. J Biol Chem 285(1), 317–327, 2010. doi: 10.1074/jbc.M109.053926.a

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.