Cell Migration Induced by Native Type IV Collagen Requires PI3K/Akt2 and EGFR Activity in MDA-MB-231 Breast Cancer Cells
Basement membrane (BM) is a specialized extracellular matrix (ECM) that separates epithelial cells from surrounding stroma and regulates various biological processes including morphology, growth, differentiation, adhesion and motility. Type IV collagen is the major component of BM, provides structural framework of all BMs and interacts with cell surface receptors including integrins and discoidin domain receptors (DDRs). The DDRs are receptor tyrosine kinases that get activated by collagens in their native triple-helical form and present sustained and slow activation kinetics. Particularly, DDR1 signaling mediates differentiation, immune response, migration and wound healing. However, the signal transduction pathways involved in cell migration induced by native IV collagen in breast cancer cells has been poorly studied. Here we demonstrate that native type IV collagen induces Akt2 and FAK activation through a DDR1, PI3K and epidermal growth factor receptor (EGFR)-dependent pathway in MDA-MB-231 breast cancer cells. In addition, cell migration induced by native type IV collagen requires PI3K, Akt2 and EGFR activity, whereas collagen IV also induces NFκB-DNA binding activity through a DDR1, PI3K, Akt2 and EGFR-dependent pathway. In summary, we demonstrate that migration induced by native type IV collagen requires PI3K/Akt2 and EGFR activity in MDA-MB-231 breast cancer cells.
Eduardo Perez Salazar,
Cell Migration Induced by Native Type IV Collagen Requires PI3K/Akt2 and EGFR Activity in MDA-MB-231 Breast Cancer Cells, Cancer Research Journal.
Vol. 3, No. 3,
2015, pp. 52-62.
Aumailley, M. & Gayraud, B. Structure and biological activity of the extracellular matrix. J Mol Med (Berl) 76, 253-65, 1998.
Nagase, H. & Woessner, J.F., Jr. Matrix metalloproteinases. J Biol Chem 274, 21491-4, 1999.
Stetler-Stevenson, W.G., Liotta, L.A. & Kleiner, D.E., Jr. Extracellular matrix 6: role of matrix metalloproteinases in tumor invasion and metastasis. FASEB J 7, 1434-41, 1993.
Weaver, V.M. et al. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2, 205-16, 2002.
Oskarsson, T. Extracellular matrix components in breast cancer progression and metastasis. Breast 22 Suppl 2, S66-72 ,2013.
Vogel, W.F., Abdulhussein, R. & Ford, C.E. Sensing extracellular matrix: an update on discoidin domain receptor function. Cell Signal 18, 1108-16, 2006.
Borza, C.M. & Pozzi, A. Discoidin domain receptors in disease. Matrix Biol, 2013.
Hou, G., Vogel, W. & Bendeck, M.P. The discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J Clin Invest 107, 727-35, 2001.
Kamohara, H., Yamashiro, S., Galligan, C. & Yoshimura, T. Discoidin domain receptor 1 isoform-a (DDR1alpha) promotes migration of leukocytes in three-dimensional collagen lattices. FASEB J 15, 2724-6, 2001.
Valiathan, R.R., Marco, M., Leitinger, B., Kleer, C.G. & Fridman, R. Discoidin domain receptor tyrosine kinases: new players in cancer progression. Cancer Metastasis Rev 31, 295-321, 2012.
Dillon, R.L., White, D.E. & Muller, W.J. The phosphatidyl inositol 3-kinase signaling network: implications for human breast cancer. Oncogene 26, 1338-45, 2007.
Fresno Vara, J.A. et al. PI3K/Akt signalling pathway and cancer. Cancer Treat Rev 30, 193-204, 2004.
Liu, P., Cheng, H., Roberts, T.M. & Zhao, J.J. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat Rev Drug Discov 8, 627-44, 2009.
Vanhaesebroeck, B., Guillermet-Guibert, J., Graupera, M. & Bilanges, B. The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol 11, 329-41, 2010.
Engelman, J.A. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 9, 550-62, 2009.
Matheny, R.W., Jr. & Adamo, M.L. Current perspectives on Akt Akt-ivation and Akt-ions. Exp Biol Med (Maywood) 234, 1264-70, 2009.
Robledo, T., Arriaga-Pizano, L., Lopez-Perez, M. & Salazar, E.P. Type IV collagen induces STAT5 activation in MCF7 human breast cancer cells. Matrix Biol 24, 469-77, 2005.
Santoro, S.A. & Cunningham, L.W. Platelet-collagen adhesion. Methods Enzymol 82 Pt A, 509-13, 1982.
Castro-Sanchez, L., Soto-Guzman, A., Guaderrama-Diaz, M., Cortes-Reynosa, P. & Salazar, E.P. Role of DDR1 in the gelatinases secretion induced by native type IV collagen in MDA-MB-231 breast cancer cells. Clin Exp Metastasis 28, 463-77, 2011.
Hodgson, L., Henderson, A.J. & Dong, C. Melanoma cell migration to type IV collagen requires activation of NF-kappaB. Oncogene 22, 98-108, 2003.
Buchdunger, E. et al. Abl protein-tyrosine kinase inhibitor STI571 inhibits in vitro signal transduction mediated by c-kit and platelet-derived growth factor receptors. J Pharmacol Exp Ther 295, 139-45, 2000.
Bantscheff, M. et al. Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat Biotechnol 25, 1035-44, 2007.
Day, E. et al. Inhibition of collagen-induced discoidin domain receptor 1 and 2 activation by imatinib, nilotinib and dasatinib. Eur J Pharmacol 599, 44-53, 2008.
Li, J. et al. Wortmannin reduces metastasis and angiogenesis of human breast cancer cells via nuclear factor-kappaB-dependent matrix metalloproteinase-9 and interleukin-8 pathways. J Int Med Res 40, 867-76.
Castro-Sanchez, L., Soto-Guzman, A., Navarro-Tito, N., Martinez-Orozco, R. & Salazar, E.P. Native type IV collagen induces cell migration through a CD9 and DDR1-dependent pathway in MDA-MB-231 breast cancer cells. Eur J Cell Biol 89, 843-52, 2010.
Hu, C. et al. Opposite regulation by PI3K/Akt and MAPK/ERK pathways of tissue factor expression, cell-associated procoagulant activity and invasiveness in MDA-MB-231 cells. J Hematol Oncol 5, 16, 2012.
Romashkova, J.A. & Makarov, S.S. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401, 86-90 ,1999.
Bishop, P.C. et al. Differential sensitivity of cancer cells to inhibitors of the epidermal growth factor receptor family. Oncogene 21, 119-27, 2002.
Liotta, L.A. & Kohn, E.C. The microenvironment of the tumour-host interface. Nature 411, 375-9, 2001.
Vogel, W., Gish, G.D., Alves, F. & Pawson, T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1, 13-23, 1997.
L'Hote C, G., Thomas, P.H. & Ganesan, T.S. Functional analysis of discoidin domain receptor 1: effect of adhesion on DDR1 phosphorylation. FASEB J 16, 234-6, 2002.
DeMali, K.A., Wennerberg, K. & Burridge, K. Integrin signaling to the actin cytoskeleton. Curr Opin Cell Biol 15, 572-82, 2003.
Wozniak, M.A., Modzelewska, K., Kwong, L. & Keely, P.J. Focal adhesion regulation of cell behavior. Biochim Biophys Acta 1692, 103-19, 2004.
Danen, E.H. & Yamada, K.M. Fibronectin, integrins, and growth control. J Cell Physiol 189, 1-13, 2001.
Chen, H.C. & Guan, J.L. Association of focal adhesion kinase with its potential substrate phosphatidylinositol 3-kinase. Proc Natl Acad Sci U S A 91, 10148-52, 1994.
Reiske, H.R. et al. Requirement of phosphatidylinositol 3-kinase in focal adhesion kinase-promoted cell migration. J Biol Chem 274, 12361-6, 1999.
Manning, B.D. & Cantley, L.C. AKT/PKB signaling: navigating downstream. Cell 129, 1261-74, 2007.
Vivanco, I. & Sawyers, C.L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2, 489-501, 2002.
Dillon, R.L. et al. Akt1 and akt2 play distinct roles in the initiation and metastatic phases of mammary tumor progression. Cancer Res 69, 5057-64, 2009.
Hutchinson, J., Jin, J., Cardiff, R.D., Woodgett, J.R. & Muller, W.J. Activation of Akt (protein kinase B) in mammary epithelium provides a critical cell survival signal required for tumor progression. Mol Cell Biol 21, 2203-12, 2001.
Hutchinson, J.N., Jin, J., Cardiff, R.D., Woodgett, J.R. & Muller, W.J. Activation of Akt-1 (PKB-alpha) can accelerate ErbB-2-mediated mammary tumorigenesis but suppresses tumor invasion. Cancer Res 64, 3171-8, 2004.
Villegas-Comonfort, S., Castillo-Sanchez, R., Serna-Marquez, N., Cortes-Reynosa, P. & Salazar, E.P. Arachidonic acid promotes migration and invasion through a PI3K/Akt-dependent pathway in MDA-MB-231 breast cancer cells. Prostaglandins Leukot Essent Fatty Acids 90, 169-77, 2014.
Prasad, S., Ravindran, J. & Aggarwal, B.B. NF-kappaB and cancer: how intimate is this relationship. Mol Cell Biochem 336, 25-37, 2010.
Ling, J. & Kumar, R. Crosstalk between NFkB and glucocorticoid signaling: a potential target of breast cancer therapy. Cancer Lett 322, 119-26, 2012.
Foley, J. et al. EGFR signaling in breast cancer: bad to the bone. Semin Cell Dev Biol 21, 951-60, 2010.
Fischer, O.M., Hart, S., Gschwind, A. & Ullrich, A. EGFR signal transactivation in cancer cells. Biochem Soc Trans 31, 1203-8, 2003.
Prenzel, N. et al. EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884-8, 1999.
Pai, R. et al. Prostaglandin E2 transactivates EGF receptor: a novel mechanism for promoting colon cancer growth and gastrointestinal hypertrophy. Nat Med 8, 289-93, 2002.
Yamauchi, T. et al. Growth hormone-induced tyrosine phosphorylation of EGF receptor as an essential element leading to MAP kinase activation and gene expression. Endocr J 45 Suppl, S27-31, 1998.
Decker, S.J. & Harris, P. Effects of platelet-derived growth factor on phosphorylation of the epidermal growth factor receptor in human skin fibroblasts. J Biol Chem 264, 9204-9, 1989.
Saito, Y., Haendeler, J., Hojo, Y., Yamamoto, K. & Berk, B.C. Receptor heterodimerization: essential mechanism for platelet-derived growth factor-induced epidermal growth factor receptor transactivation. Mol Cell Biol 21, 6387-94, 2001.