Matrix stiffening sensitizes epithelial cells to EGF and enables the loss of contact inhibition of proliferation

Journal of Cell Science

Volumn 124, Issue 8, 2011, Pages 1280-1287

  Kim, Jin Hong ^a   Asthagiri, Anand R ^b,c  

^a California Institute of Technology   (United States)

^b California Institute of Technology   (United States)

^c NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Cancer; Contact inhibition; Matrix stiffness; Mechanotransduction; Proliferation

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN KINASE B; PROTEIN ZO1; UVOMORULIN;

ANIMAL CELL; ARTICLE; CANCER GROWTH; CELL ADHESION; CELL ANCHORAGE; CELL CONTACT; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; EPITHELIUM CELL; EXTRACELLULAR MATRIX; LIGAND BINDING; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; TISSUE GROWTH;

ANIMALS; BIOMECHANICS; CADHERINS; CELL LINE; CELL PROLIFERATION; CONTACT INHIBITION; DOGS; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; KINETICS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 79953144263     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.078394     Document Type: Article

References (34)

1. Assoian, R. K. (1997). Anchorage-dependent cell cycle progression. J. Cell Biol. 136, 1-4.
2. Balda, M. S., Garrett, M. D. and Matter, K. (2003). The ZO-1-associated Y-box factor ZONAB regulates epithelial cell proliferation and cell density. J. Cell Biol. 160, 423-432.
3. Balkovetz, D. F., Pollack, A. L. and Mostov, K. E. (1997). Hepatocyte growth factor alters the polarity of Madin-Darby canine kidney cell monolayers. J. Biol. Chem. 272, 3471-3477.
4. Behrens, J., von Kries, J. P., Kuhl, M., Bruhn, L., Wedlich, D., Grosschedl, R. and Birchmeier, W. (1996). Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382, 638-642.
5. Butcher, D. T., Alliston, T. and Weaver, V. M. (2009). A tense situation: forcing tumour progression. Nat. Rev. Cancer 9, 108-122.
6. Chen, R. H., Sarnecki, C. and Blenis, J. (1992). Nuclear localization and regulation of erk- and rsk-encoded protein kinases. Mol. Cell. Biol. 12, 915-927.
7. Curto, M., Cole, B. K., Lallemand, D., Liu, C.-H. and McClatchey, A. I. (2007). Contact-dependent inhibition of EGFR signaling by Nf2/Merlin. J. Cell Biol. 177, 893-903.
8. Dahmane, A., Gil, S., Brehier, A., Davy, J. and Feger, J. (1996). Kinetic analysis of epidermal growth factor endocytosis in rat hepatocytes. Effects of diabetes. Eur. J. Cell Biol. 69, 335-342.
9. de Rooij, J., Kerstens, A., Danuser, G., Schwartz, M. A. and Waterman-Storer, C. M. (2005). Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J. Cell Biol. 171, 153-164.
10. den Elzen, N., Buttery, C. V., Maddugoda, M. P., Ren, G. and Yap, A. S. (2009). Cadherin adhesion receptors orient the mitotic spindle during symmetric cell division in mammalian epithelia. Mol. Biol. Cell 20, 3740-3750.
11. Discher, D. E., Janmey, P. and Wang, Y. L. (2005). Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143.
12. Engler, A. J., Sen, S., Sweeney, H. L. and Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689.
13. Fogg, V. C., Liu, C. J. and Margolis, B. (2005). Multiple regions of Crumbs3 are required for tight junction formation in MCF10A cells. J. Cell Sci. 118, 2859-2869.
14. Franck, C., Hong, S., Maskarinec, S. A., Tirrell, D. A. and Ravichandran, G. (2007). Three-dimensional full-field measurements of large deformations in soft materials using confocal microscopy and digital volume correlation. Exp. Mech. 47, 427-438.
15. French, A. R., Tadaki, D. K., Niyogi, S. K. and Lauffenburger, D. A. (1995). Intracellular trafficking of epidermal growth factor family ligands is directly influenced by the pH sensitivity of the receptor/ligand interaction. J. Biol. Chem. 270, 4334-4340.
16. Gottardi, C. J., Arpin, M., Fanning, A. S. and Louvard, D. (1996). The junctionassociated protein, zonula occludens-1, localizes to the nucleus before the maturation and during the remodeling of cell-cell contacts. Proc. Natl. Acad. Sci. USA 93, 10779-10784.
17. Guo, W. H., Frey, M. T., Burnham, N. A. and Wang, Y. L. (2006). Substrate rigidity regulates the formation and maintenance of tissues. Biophys. J. 90, 2213-2220.
18. Hamaratoglu, F., Willecke, M., Kango-Singh, M., Nolo, R., Hyun, E., Tao, C., Jafar-Nejad, H. and Halder, G. (2006). The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat. Cell Biol. 8, 27-36.
19. Hanahan, D. and Weinberg, R. A. (2000). The hallmarks of cancer. Cell 100, 57-70.
20. Kim, J. H., Kushiro, K., Graham, N. A. and Asthagiri, A. R. (2009). Tunable interplay between epidermal growth factor and cell-cell contact governs the spatial dynamics of epithelial growth. Proc. Natl. Acad. Sci. USA 106, 11149-11153.
21. Klein, E. A., Yin, L., Kothapalli, D., Castagnino, P., Byfield, F. J., Xu, T., Levental, I., Hawthorne, E., Janmey, P. A. and Assoian, R. K. (2009). Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr. Biol. 19, 1511-1518.
22. Lampugnani, M., Zanetti, A., Corada, M., Takahashi, T., Balconi, G., Breviario, F., Orsenigo, F., Cattelino, A., Kemler, R., Daniel, T. O. et al. (2003). Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148. J. Cell Biol. 161, 793-804.
23. Lampugnani, M. G., Orsenigo, F., Gagliani, M. C., Tacchetti, C. and Dejana, E. (2006). Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J. Cell Biol. 174, 593-604.
24. Lee, J. W. and Juliano, R. (2004). Mitogenic signal transduction by integrin- and growth factor receptor-mediated pathways. Mol. Cells 17, 188-202.
25. Lee, S. B., Xuan Nguyen, T. L., Choi, J. W., Lee, K. H., Cho, S. W., Liu, Z., Ye, K., Bae, S. S. and Ahn, J. Y. (2008). Nuclear Akt interacts with B23/NPM and protects it from proteolytic cleavage, enhancing cell survival. Proc. Natl. Acad. Sci. USA 105, 16584-16589.
26. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F., Csiszar, K., Giaccia, A., Weninger, W. et al. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906.
27. Meier, R., Alessi, D. R., Cron, P., Andjelkovic, M. and Hemmings, B. A. (1997). Mitogenic activation, phosphorylation, and nuclear translocation of protein kinase Bbeta. J. Biol. Chem. 272, 30491-30497.
28. Molenaar, M., van de Wetering, M., Oosterwegel, M., Peterson-Maduro, J., Godsave, S., Korinek, V., Roose, J., Destree, O. and Clevers, H. (1996). XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86, 391-399.
29. Nelson, C. M., Jean, R. P., Tan, J. L., Liu, W. F., Sniadecki, N. J., Spector, A. A. and Chen, C. S. (2005). Emergent patterns of growth controlled by multicellular form and mechanics. Proc. Natl. Acad. Sci. USA 102, 11594-11599.
30. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D. et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254.
31. Pelham, R. J., Jr and Wang, Y. (1997). Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 94, 13661-13665.
32. Tsapara, A., Matter, K. and Balda, M. S. (2006). The heat-shock protein Apg-2 binds to the tight junction protein ZO-1 and regulates transcriptional activity of ZONAB. Mol. Biol. Cell 17, 1322-1330.
33. Wiseman, B. S. and Werb, Z. (2002). Stromal effects on mammary gland development and breast cancer. Science 296, 1046-1049.
34. Yin, F. and Pan, D. (2007). Fat flies expanded the hippo pathway: a matter of size control. Sci. STKE 2007, pe12.