Delay of cell cycle progression and induction of death of cancer cells on type I collagen fibrils

REFERENCES

• Sabeh, F., Ota, I., Holmbeck, K., Birkedal-Hansen, H., Soloway, P., Balbin, M., Lopez-Otin, C., Shapiro, S., Inada, M., Krane, S., Allen, E., Chung, D., and Weiss, S.J. (2004). Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J. Cell Biol. 167:769–781.
   PubMed Web of Science ®Google Scholar
• Suzuki, Y., Someki, I., Adachi, E., Irie, S., and Hattori, S. (1999). Interaction of collagen molecules from the aspect of fibril formation: Acid-soluble, alkali-treated, and MMP1-digested fragments of type I collagen. J. Biochem. 126:54–67.
   PubMed Web of Science ®Google Scholar
• Elsdale, T., and Bard, J. (1972). Collagen substrata for studies on cell behavior. J. Cell Biol. 54:626–637.
   PubMed Web of Science ®Google Scholar
• Friedl, P., and Brocker, E.B. (2000). The biology of cell locomotion within three-dimensional extracellular matrix. Cell. Mol. Life Sci. 57:41–64.
   PubMed Web of Science ®Google Scholar
• Grinnell, F. (2000). Fibroblast-collagen-matrix contraction: Growth-factor signalling and mechanical loading. Trends Cell Biol. 10:362–365.
   PubMed Web of Science ®Google Scholar
• Nishiyama, T., Tsunenaga, M., Nakayama, Y., Adachi, E., and Hayashi, T. (1989). Growth rate of human fibroblasts is repressed by the culture within reconstituted collagen matrix but not by the culture on the matrix. Matrix 9:193–199.
   PubMedGoogle Scholar
• Koyama, H., Raines, E.W., Bornfeldt, K.E., Roberts, J.M., and Ross, R. (1996). Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of Cdk2 inhibitors. Cell 87:1069–1078.
   PubMed Web of Science ®Google Scholar
• Fujisaki, H., and Hattori, S. (2002). Keratinocyte apoptosis on type I collagen gel caused by lack of laminin 5/10/11 deposition and Akt signaling. Exp. Cell Res. 280:255–269.
   PubMed Web of Science ®Google Scholar
• Franke, T.F., Hornik, C.P., Segev, L., Shostak, G.A., and Sugimoto, C. (2003). PI3K/Akt and apoptosis: Size matters. Oncogene 22:8983–8998.
   PubMed Web of Science ®Google Scholar
• Tian, B., Lessan, K., Kahm, J., Kleidon, J., and Henke, C. (2002). Beta 1 integrin regulates fibroblast viability during collagen matrix contraction through a phosphatidylinositol 3‐kinase/Akt/protein kinase B signaling pathway. J. Biol. Chem. 277:24667–24675.
   PubMed Web of Science ®Google Scholar
• Graff, J.R., Konicek, B.W., McNulty, A.M., Wang, Z., Houck, K., Allen, S., Paul, J.D., Hbaiu, A., Goode, R.G., Sandusky, G.E., Vessella, R.L., and Neubauer, B.L. (2000). Increased AKT activity contributes to prostate cancer progression by dramatically accelerating prostate tumor growth and diminishing p27Kip1 expression. J. Biol. Chem. 275:24500–24505.
   PubMed Web of Science ®Google Scholar
• Grille, S.J., Bellacosa, A., Upson, J., Klein-Szanto, A.J., van Roy, F., Lee-Kwon, W., Donowitz, M., Tsichlis, P.N., and Larue, L. (2003). The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res. 63:2172–2178.
   PubMed Web of Science ®Google Scholar
• Vivanco, I., and Sawyers, C.L. (2002). The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat. Rev. Cancer 2:489–501.
   PubMed Web of Science ®Google Scholar
• Brognard, J., Clark, A.S., Ni, Y., and Dennis, P.A. (2001). Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res. 61:3986–3997.
   PubMed Web of Science ®Google Scholar
• Nakatani, K., Thompson, D.A., Barthel, A., Sakaue, H., Liu, W., Weigel, R.J., and Roth, R.A. (1999). Up-regulation of Akt3 in estrogen receptor-deficient breast cancers and androgen-independent prostate cancer lines. J. Biol. Chem. 274: 21528–21532.
   PubMed Web of Science ®Google Scholar
• Sato, K., Ebihara, T., Adachi, E., Kawashima, S., Hattori, S., and Irie, S. (2000). Possible involvement of aminotelopeptide in self-assembly and thermal stability of collagen I as revealed by its removal with proteases. J. Biol. Chem. 275 25870–25875.
   PubMed Web of Science ®Google Scholar
• Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76:4350–4354.
   PubMed Web of Science ®Google Scholar
• Knight, C.G., Morton, L.F., Onley, D.J., Peachey, A.R., Messent, A.J., Smethurst, P.A., Tuckwell, D.S., Farndale, R.W., and Barnes, M.J. (1998). Identification in collagen type I of an integrin alpha2 beta1-binding site containing an essential GER sequence. J. Biol. Chem. 273:33287–33294.
   PubMed Web of Science ®Google Scholar
• Frisch, S.M., and Francis, H. (1994). Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124: 619–626.
   PubMed Web of Science ®Google Scholar
• Liotta, L.A., and Kohn, E. (2004). Anoikis: Cancer and the homeless cell. Nature 430:973–974.
   PubMed Web of Science ®Google Scholar
• Jones, S.A., Butler, R.N., Sanderson, I.R., and Wilson, J.W. (2004). The effect of specific caspase inhibitors on TNF-alpha and butyrate-induced apoptosis of intestinal epithelial cells. Exp. Cell Res. 292:29–39.
   PubMed Web of Science ®Google Scholar
• Nicholson, D.W., Ali, A., Thornberry, N.A., Vaillancourt, J.P., Ding, C.K., Gallant, M., Gareau, Y., Griffin, P.R., Labelle, M., Lazebnik, Y.A., Munday, N.A., Raju, S.M., Smulson, M.E., Yamin, T.-T., Yu, V.L., and Miller D.K. (1995). Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376:37–43.
   PubMed Web of Science ®Google Scholar
• Tewari, M., Quan, L.T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D.R., Poirier, G.G., Salvesen, G.S., and Dixit, V.M. (1995). Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:801–809.
   PubMed Web of Science ®Google Scholar
• Pacini, A., Quattrone, A., Denegri, M., Fiorillo, C., Nediani, C., Ramon y Cajal, S., and Nassi, P. (1999). Transcriptional down-regulation of poly(ADP-ribose) polymerase gene expression by E1A binding to pRb proteins protects murine keratinocytes from radiation-induced apoptosis. J. Biol. Chem. 274:35107–35112.
   PubMed Web of Science ®Google Scholar
• Huang, S., and Ingber, D.E. (2000). Shape-dependent control of cell growth, differentiation, and apoptosis: Switching between attractors in cell regulatory networks. Exp. Cell Res. 261:91–103.
   PubMed Web of Science ®Google Scholar
• Hynes, R.O. (1992). Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69:11–25.
   PubMed Web of Science ®Google Scholar
• Ben-Ze'ev, A. (1997). Cytoskeletal and adhesion proteins as tumor suppressors. Curr. Opin. Cell Biol. 9:99–108.
   PubMed Web of Science ®Google Scholar
• Varner, J.A., and Cheresh, D.A. (1996). Integrins and cancer. Curr. Opin. Cell Biol. 8:724–730.
   PubMed Web of Science ®Google Scholar
• Henriet, P., Zhong, Z.D., Brooks, P.C., Weinberg, K.I., and DeClerck, Y.A. (2000). Contact with fibrillar collagen inhibits melanoma cell proliferation by up-regulating p27KIP1. Proc. Natl. Acad. Sci. U.S.A. 97:10026–10031.
   PubMed Web of Science ®Google Scholar
• Fujisaki, H., Adachi, E., and Hattori, S. (2008). Keratinocyte differentiation and proliferation are regulated by adhesion to the three-dimensional meshwork structure of type IV collagen. Connect. Tissue Res. 49:426–436.
   PubMed Web of Science ®Google Scholar
• Fujisaki, H., Ebihara, T., Irie, S., Kobayashi, T., Adachi, E., Mochitate, K., and Hattori, S. (2007). Keratinocyte apoptosis on type I collagen fibrils is prevented by Erk1/2 activation under high calcium condition. Connect. Tissue Res. 48:159–169.
   PubMed Web of Science ®Google Scholar
• Gayer, C.P., Chaturvedi, L.S., Wang, S., Craig, D.H., Flanigan, T., and Basson, M.D. (2009). Strain-induced proliferation requires the phosphatidylinositol 3-kinase/AKT/glycogen synthase kinase pathway. J. Biol. Chem. 284:2001–2011.
   PubMed Web of Science ®Google Scholar
• Wang, Y.K., Wang, Y.H., Wang, C.Z., Sung, J.M., Chiu, W.T., Lin, S.H., Chang, Y.H., and Tang, M.J. (2003). Rigidity of collagen fibrils controls collagen gel-induced down-regulation of focal adhesion complex proteins mediated by alpha2beta1 integrin. J. Biol. Chem. 278:21886–21892.
   PubMed Web of Science ®Google Scholar
• Del Re, D.P., Miyamoto, S., and Brown, J.H. (2008). Focal adhesion kinase as a RhoA-activable signaling scaffold mediating Akt activation and cardiomyocyte protection. J. Biol. Chem. 283:35622–35629.
   PubMed Web of Science ®Google Scholar
• Gehlsen, K.R., Davis, G.E., and Sriramarao, P. (1992). Integrin expression in human melanoma cells with differing invasive and metastatic properties. Clin. Exp. Metastasis 10:111–120.
   PubMed Web of Science ®Google Scholar