Anoikis induction by glycoprotein from Laminaria japonica in HT-29 cells

Hiroe Go, Hye-Jung Hwang, In-Hye Kim, Taek-Jeong Nam

.
Department of Food Science and Nutrition, Pukyong National University 599-1, Daeyeon 3-dong, Nam-gu, Busan 608-737 The Re-public of KOREA.

DOI: 10.4236/ojpm.2011.12008                

Abstract

We extracted a glycoprotein from the brown alga Laminaria japonica (LJGP). We previously demonstrated that LJGP induced apop- tosis in HT-29 colon cancer cells via the Fas- and the mitochondrial signaling pathway, and cell-cycle arrest. However, its effect on the cell membrane remained unknown. In this study, we identified the involvement of matrix metalloproteinase (MMP), integrin, and Epi- thelial (E)-cadherin in LJGP-induced apoptosis in HT-29 cells. LJGP treatment increased the expression and activity of MMP-2 and MMP-9. Furthermore, LJGP decreased the expression of integrin αν, β3, β5, β6 and E- cadherin. Consistent with a decreased expression of E-cadherin, LJGP inhibited the Wnt signaling pathway. Moreover, activation of downstream molecules of integrin, including focal adhesion kinase (FAK), the Src family of protooncogenic tyrosine kinases, extracellular signal-related kinase (ERK), and phosphatidyl inositol 3 kinase (PI-3K) were also decreased. These findings suggest that LJGP-induced apoptosis of HT-29 cells involves possible ECM disruption and cell detachment, which are executed principally through the activation of MMPs and by a decrease of adhesion molecules, contributing to a down-regulation of the PI-3K, MAPK, and Wnt signaling pathways. Apoptosis induced by ECM disruption or cell detachment is also known as anoikis. We can say that LJGP induces anoikis in HT-29 cells.

Keywords

Anoikis; Glycoprotein; Integrin; Laminaria Japonica; MMP; Seaweed

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Chou, K.C. (2002) A new branch of proteomics: predict Lee, H.Y., You, H.J., Won, J.Y., Youn, S.W., Cho, H.J., Park, K.W., Park, W.Y., Seo, J.S., Park, Y.B., Walsh, K., Oh, B.H., Kim, H.S. (2008) Forkhead factor, FOXO3a, induces apoptosis of endothelial cells through activation of matrix metalloproteinases. Am Heart J, 28, 302-308.
[2]	Kim, JB., Yu, JH., Ko, E., Lee, K.W., Song, A.K., Park, S.Y., Shin, I., Han, E., Noh, D.Y. (2010) The alkaloid berberine inhibits the growth of anoikis-resistant MCF-7 and MDA-MB-231 breast cancer cell lines by including cell cycle arrest. Phytomedicine, 17, 436-440.
[3]	Michel, J.B. (2003) Anoikis in the cardiovascular system known and unknown extracellular mediators. Am Heart J, 23, 2146-2154.
[4]	Coates, J.M., Galante, J.M., Bold, R.J. (2010) Cancer therapy beyond apoptosis: autophagy and anoikis as mechanisms of cell death. J Surg Res, 164, 301-308.
[5]	Chiarugi, P., Giannoni, E. (2008) Anoikis: A necessary death program for anchorage-dependent cells. Biochem Pharmacol, 76, 1352-1364.
[6]	Sakamoto, S., Kyprianou, N. (2010) Targeting anoikis resistance in prostate cancer metastasis. Mol Aspects Med, 31, 205-214.
[7]	Grossmann, J. (2002) Molecular mechanisms of “detachment-induced apoptosis-Anoikis”. Apoptosis, 7, 247-260.
[8]	Duxbury, M.S., Ito, H., Zinner, M.J., Ashley, S.W., Whang, E.E. (2004) Focal adhesion kinase gene silenceing promotes anoikis and suppresses metastasis of human pancreatic adenocarcinoma cells. Surgery, 135, 555-562.
[9]	Aplin, A.E., Howe, A., Alahari, S.K., Juliano, R.L. (1998) Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol Rev, 50, 197-263.
[10]	Peng, C., Liu, X., Liu, E., Xu, K., Niu, W., Chen, R., Wang, J., Zhang, Z., Lin, P., Wang, J., Agrez, M., Niu, J. (2009) Norcantharidin induces HT-29 colon cancer cell apoptosis through the ανβ6-extracellular signal-related kinase signaling pathway. Cancer Sci, 100, 2302-2308.
[11]	Maity, G., Fahreen, S., Banerji, A., Choudhury, P.R., Sen, T., Dutta, A., Chatterjee, A. (2010) Fibronectin–integrin mediated signaling in human cervical cancer cells (SiHa). Mol Cell Biochem, 336, 65-74.
[12]	Lee, BJ., Senevirathne, M., Kim, J.S., Kim, Y.M., Lee, M.S., Jeong, M.H., Kang, Y.M., Kim, J.I., Nam, B.H., Ahn, C.B, Je, J.Y. (2010) Protective effect of fermented sea tangle against ethanol and carbon tetrachloride-induced hepatic damage in Sprague-Dawley rats. Food Chem Toxicol, 48, 1123-1128.
[13]	Wagenaar-Miller, R.A., Gorden, L., Matrisian, L.M. (2004) Matrix metalloproteinases in colorectal cancer: Is it worth talking about? Cancer Metastasis Rev, 23, 119-135.
[14]	Li, L.N., Zhang, H.D., Yuan, S.J., Yang, D.X., Wang, L., Sun, Z.X. (2008) Differential sensitivity of colorectal cancer cell lines to artesunate is associated with expression of beta-catenin and E-cadherin. Eur J Pharmacol, 588, 1-8.
[15]	Oloumi, A., McPhee, T., Dedhar, S. (2004) Regulation of E-cadherin expression and β-catenin/Tcf transcriptional activity by the integrin-linked kinase. Biochim Biophys Acta, 1691, 1-15.
[16]	Go, H., Hwang, H.J., Nam, T.J. (2009) Glycoprotein extraction from Laminaria japonica promotes IEC-6 cell proliferation. Int J Mol Med, 24, 819-824.
[17]	Go, H., Hwang, H.J., Nam, T.J. (2010) A glycoprotein from Laminaria japonica induces apoptosis in HT-29 colon cancer cells. Toxicol in Vitro, 24, 1546-1553.
[18]	Ikeda, H., Suzuki, Y., Suzuki, M., Koike, M., Tamura, J., Nomura, M., Itoh, G. (1998) Apoptosis is a major mode of cell death caused by ischaemia and ischaemia/ reperfusion injury to the rat intestinal epithelium. Gut, 42, 530-537.
[19]	Kuphal, S., Bauer, R., Bosserhoff, A.K. (2005) Integrin signaling in malignant melanoma. Cancer Metastasis Rev, 24, 195-222.
[20]	Schlaepfer, D.D., Hanks, S.K., Hunter, T., van der Geer, P. (1994) Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature, 372, 786-791.
[21]	Calalb, M.B., Polte, T.R., Hanks, S.K. (1995) Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity. Mol Cell Biol, 15, 954-963.
[22]	Golubovskaya, V.M., Gross, S., Kaur, A.S., Wilson, R.I., Xu, L.H., Yang, X.H., Cance, W.G. (2003) Simultaneous inhibition of focal adhesion kinase and SRC enhances detachment and apoptosis in colon cancer cell lines. Mol Cancer Res, 1, 755-764.
[23]	Fizazi, K. (2007) The role of Src in prostate cancer. Ann Oncol, 18, 1765-1774.
[24]	Jones, R.J., Brunton, V.G., Frame, M.C. (2000) Adhesion-linked kinases in cancer; emphasis on Src, focal adhesion kinase and PI 3-kinase. Eur J Cancer, 36, 1595-1606.
[25]	Murillo, C.A., Rychahou, P.G., Evers, B.M. (2004) Inhibition of alpha5 integrin decreases PI3K activation and cell adhesion of human colon cancers. Surgery, 136, 143-149.
[26]	Dai, R.Y., Chen, S.K., Yan, D.M., Chen, R., Lui, Y.P., Duan, C.Y., Li, J., He, T., Li, H. (2010) PI3K/Akt promotes GRP78 accumulation and inhibits endoplasmic reticulum stress-induced apoptosis in HEK293 cells. Folia Biol, 56, 37-46.
[27]	Jiang, H., Fan, D., Zhou, G., Li, X., Deng, H. (2010) Phosphatidylinositol 3-kinase inhibitor (LY294002) induces apoptosis of human nasopharyngeal carcinoma in vitro and in vivo. J Exp Clin Cancer Res, 29, 34.
[28]	Li, Q., Wu, J., Zheng, H., Liu, K., Guo, T.L., Liu, T., Eblen, S.T., Grant, S., Zhang, S. (2010) Discovery of 3-(2-aminoethyl)-5-(3-phenyl-propylidene)-thiazolidine-2,4-dione as a dual inhibitor of the Raf/MEK/ERK and the PI3K/Akt signaling pathways. Bioorg Med Chem Lett, 20, 4526-4530.
[29]	Demers, M.J., Thibodeau, S., Noel, D., Fujita, N., Tsuruo, T., Gauthier, R., Arguin, M., Vachon, P.H. (2009) Intestinal epithelial cancer cell anoikis resistance: EGFR-mediated sustained activaton of Src overrides Fak-deoendent signaling to MEK/Erk and/or PI3-K/Akt-1. J Cell Biochem, 107, 639-654.
[30]	Ahmed, N., Niu, J., Dorahy, D.J., Gu, X., Andrews, S., Meldrum, C.J., Scott, R.J., Baker, M.S., Macreadie, I.G., Agrez, M.V. (2002) Direct integrin ανβ6-ERK binding: implications for tumor growth. Oncogene, 21, 1370-1380.
[31]	Walker, J.L., Assoian, R.K. (2005) Integrin-dependent signal transduction regulating cyclinD1 expression and G1 phase cell cycle progression. Cancer Metastasis Rev, 24, 383-393.
[32]	Blaschuk, O.W., Devemy, E. (2009) Cadherins as novel targets for anti-cancer therapy. Eur J Pharmacol, 625, 195-198.
[33]	Gavert, N., Ben-Ze`ev, A. (2007) β-catenin signaling in biological control and cancer. J Cell Biochem, 102, 820-828.
[34]	Steinhusen, U., Badock, V., Bauer, A., Behrens, J., Wittman-Liebold, B., Dorken, B., Bommert, K. (2000) Apoptosis-induced cleavage of β-catenin by caspase -3 results in proteolytic fragments with reduced transactivation potential. J Biol Chem, 275, 16345-16353.
[35]	Yasuhara-Bell, J., Lu, Y. (2010) Marine compounds and their antiviral activities. Antiviral Res, 86, 231-240.
[36]	Yuan, Y.V., Walsh, N.A. (2006) Antioxidant and antiproliferative activities of extracts from a variety of edible seaweeds. Food Chem Toxicol, 44, 1144-1150.
[37]	Zhu, Z., Zhang, Q., Chen, L., Ren, S., Xu, P., Tang, Y., Luo, D. (2010) Higher specificity of the activity of low molecular weight fucoidan for thrombin-induced platelet aggregation. Thromb Res, 125, 419-426.
[38]	Cho, D.M., Kim, D.S., Lee, D.S., Kim, H.R., Pyeun, J.H. (1995) Trace components and functional saccharides in seaweed-1. Changes in proximate composition and trace elements according to the harvest season and places. Bulletin of the Korean Fisheries, 28, 49-59.
[39]	Walden, P.D., Globina, Y., Nieder, A. (2004) Induction of anoikis by doxazosin in prostate cancer cells is associated with activation of caspase-3 and a reduction of focal adhesion kinase. Urol Res, 32, 261-265.
[40]	Jiang, C., Wang, Z., Ganther, H., Lu, J. (2001) Caspases as key executors of methyl selenium-induced apoptosis (anoikis) of DU-145 prostate cancer cells. Cancer Res, 61, 3062-3070.
[41]	Akiyama, T., Choong, P.F., Dass, C.R. (2010) RANK-Fc inhibits malignancy via inhibiting ERK activation and evoking caspase-3-mediated anoikis in human osteosarcoma cells. Clin Exp Metastasis, 27, 207-215.
[42]	Cao, L.Q., Wang, Q., Chen, X.L., Zhen, M.C., Fu, X.H., Huang, X.H. (2007) 15-Deoxy-delta (12,14)-prostaglandin J (2) induces anoikis of hepatocellular carcinoma cells: an in vitro experiment. Zhonghua Yi Xue Za Zhi, 87, 3001-3005.
[43]	Kochtebane, N., Choqueux, C., Passefort, S., Nataf, P., Messika-Zeitoun, D., Bartagi, A., Michel, J.B., Angles-Cano, E., Jacob, M.P. (2010) Plasmin induces apoptosis of aortic valvular myofibroblasts. J Pathol, 221, 37-48.
[44]	Wu, W.B., Chang, S.C., Liau, M.Y., Huang, T.F. (2001) Purification, molecular cloning and mechanism of action of graminelysin I, a snake-venom-derived metalloproteinase that induces apoptosis of human endothelial cells. Biochem J, 357, 719-728.
[45]	Liu, X.W., Bernardo, M.M., Fridman, R., Kim, H.R. (2003) Tissue inhibitor of metalloproteinase-1 protects human breast epithelial cells against intrinsic apoptotic cell death via the focal adhesion kinase/phosphatidylinositol 3-kinase and MAPK signaling pathway. J Biol Chem, 278, 40364-40372.
[46]	Cierniewski, C.S., Papiewska-Pajak, I., Malinowsi, M., Sacewicz-Hofman, I., Wiktorska, M., Kryczka, J., Wysocki, T., Niewiarowska, J., Bednarek, R. (2010) Thymosin beta4 regulates migration of colon cancer cells by a pathway involving interaction with Ku80. Annals NY Acad Sci, 1194, 60-71.
[47]	Park, E.K., Park, M.J., Lee, S.H., Li, Y.C., Kim, J., Lee, J.S., Lee, J.W., Ye, S.K., Park, J.W., Kim, C.W., Park, B.K., Kim, Y.N. (2009) Cholesterol depletion induces anoiki-like apoiptosis via FAK down-regulation and caveolae internalization. J Pathol, 218, 337-349.
[48]	Owens, L.V., Xu, L., Dent, G.A., Yang, X., Sturge, G.C., Craven, R.J., Cance, W.G. (1996) Focal adhesion kinase as a marker of invasive potential in differentiated human thyroid cancer. Ann Surg Oncol, 3, 100-105.
[49]	Agochiya, M., Brunton, V.G., Owens, D.W., Parkinson, E.K., Paraskeva, C., Keith, W.N., Frame, M.C. (1999) Increased dosage and amplification of the focal adhesion kinase gene in human cancer cells. Oncogene, 18, 5646-5653.
[50]	Liao, C.H., Sang, S., Ho, C.T., Lin, J.K. (2005) Garcinol modulates tyrosine phosphorylation of FAK and subsequently induces apoptosis through down-regulation of Src, ERK, and Akt survival signaling in human colon cancer cells. J Cell Biochem, 96, 155-169.
[51]	Zheng, D.Q., Woodard, A.S., Tallini, G., Languino, L.R. (2000) Substrate specificity of alpha(v)beta(3) integrin-mediated cell migration and phosphatidylinositol 3-kinase/ AKT pathway activation. J Biol Chem, 275, 24565-24574.
[52]	Shan, J.Z., Xuan, Y.Y., Zheng, S., Dong, Q., Zhang, S.Z. (2009) Ursolic acid inhibits proliferation and induces apoptosis of HT-29 colon cancer cells by inhibiting the EGFR/MAPK pathway. J Zhejiang Univ Sci B, 10, 668-674.
[53]	Sullivan, R., Graham, C.H. (2007) Hypoxia-driven selection of the metastatic phenotype. Cancer Metastasis Rev, 26, 319-331.
[54]	Fouquet, S., Lugo-Martinez, V.H., Faussat, A.M., Renaud, F., Cardot, P., Chambaz, J., Pincon-Raymond, M., Thenet, S. (2004) Early loss of E- cadherin from cell-cell contacts is involved in the onset of anoikis in enterocytes. J Biol Chem, 279, 43061-43069.
[55]	Daugherty, R.L., Gottardi, C.J. (2007) Phopho-regulation of β-catenin adhesion and signaling functions. Physiology, 22, 303-309.
[56]	Orford, K., Orford, C.C., Byers, S.W. (1999) Exogenous expression of β-catenin regulates contact inhibition, anchorage-independent growth, anoikis, and radiation-induced cell cycle arrest. J Cell Biol, 146, 855-868.
[57]	Peluso, J.J., Pappalardo, A., Fernandez, G. (2001) E-cadherin-mediated cell contact prevents apoptosis of spontaneously immortalized granulose cells by regulating Akt kinase activity. Biol Reprod, 64, 1183-1190.
[58]	Bergin, E., Levine, J.S., Koh, J.S., Lieberthal, W. (2000) Mouse proximal tubular cell-cell adhesion inhibits apoptosis by a cadherin-dependent mechanism. Am J Physiol, 278, F758-F768.
[59]	von Schlippe, M., Marshall, J.F., Perry, P., Stone, M., Zhu, A.J., Hart, I.R. (2000) Functional interaction between E-cadherin and alphav-containing integrins in carcinoma cells. J Cell Sci, 113, 425-437.
[60]	Xu, W., Kimelman, D. (2007) Mechanistic insights from structural studies of β-catenin and its binding partners. J Cell Sci, 120, 3337-3344.
[61]	Vanamala, J., Reddivari, L., Radhakrishnan, S., Tarver, C. (2010) Resveratrol suppresses IGF-1 induced human colon cacner cell proliferation and elevates apoptosis via suppression of IGF-1R/Wnt and activation of p53 signaling pathways. BMC Cancer, 10, 238.
[62]	Yoo, J.H., Lee, H.J., Kang, K., Jho, E.H., Kim, C.Y., Baturen, D., Tunsag, J., Nho, C.W. Lignans inhibit cell growth via regulation of Wnt/beta-catenin signaling. Food Chem Toxicol, 48, 2247-2252.
[63]	Minke, K.S., Staib, M., Puetter, A., Gehrke, I., Gandhirajan, R.K., Schlosser, A., Schmitt, E.K., Hallek, M., Kreuzer, K.A. (2009) Small molecule inhibitors of WNT signaling effectively induce apoptosis in acute myeloid leukemia cells. Eur J Haematol, 82, 165-175.