Cited by 97Cellular Mechanics and InteractionsCell Adhesion Molecules ResearchForce Microscopy Techniques and Applications

E-cadherin-mediated force transduction signals regulate global cell mechanics

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Muhamed, Ismaeel, Wu, Jun, Sehgal, Poonam, Kong, Xinyu, Tajik, Arash, Wang, Ning, Leckband, Deborah E.·2016·Journal of Cell Science

Abstract

This report elucidates an E-cadherin-based force-transduction pathway that triggers changes in cell mechanics through a mechanism requiring epidermal growth factor receptor (EGFR), phosphoinositide 3-kinase (PI3K), and the downstream formation of new integrin adhesions. This mechanism operates in addition to local cytoskeletal remodeling triggered by conformational changes in the E-cadherin-associated protein α-catenin, at sites of mechanical perturbation. Studies using magnetic twisting cytometry (MTC), together with traction force microscopy (TFM) and confocal imaging identified force-activated E-cadherin-specific signals that integrate cadherin force transduction, integrin activation and cell contractility. EGFR is required for the downstream activation of PI3K and myosin-II-dependent cell stiffening. Our findings also demonstrated that α-catenin-dependent cytoskeletal remodeling at perturbed E-cadherin adhesions does not require cell stiffening. These results broaden the repertoire of E-cadherin-based force transduction mechanisms, and define the force-sensitive signaling network underlying the mechano-chemical integration of spatially segregated adhesion receptors.

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  1. Al-Kilani A., de Freitas O., Dufour S. and Gallet F. (2011). Negative feedback from integrins to cadherins: a micromechanical study. Biophys. J. 101, 336-344. 10.1016/j.bpj.2011.06.009 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  2. Barry A. K., Wang N. and Leckband D. E. (2015). Local VE-cadherin mechanotransduction triggers long-ranged remodeling of endothelial monolayers. J. Cell Sci. 128, 1341-1351. 10.1242/jcs.159954 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  3. Batra N., Burra S., Siller-Jackson A. J., Gu S., Xia X., Weber G. F., DeSimone D., Bonewald L. F., Lafer E. M., Sprague E. et al. (2012). Mechanical stress-activated integrin alpha5beta1 induces opening of connexin 43 hemichannels. Proc. Natl. Acad. Sci. USA 109, 3359-3364. 10.1073/pnas.1115967109 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  4. Brehmer D., Greff Z., Godl K., Blencke S., Kurtenbach A., Weber M., Muller S., Klebl B., Cotten M., Keri G. et al. (2005). Cellular targets of gefitinib. Cancer Res. 65, 379-382. [PubMed] [Google Scholar]
  5. Buckley C. D., Tan J., Anderson K. L., Hanein D., Volkmann N., Weis W. I., Nelson W. J. and Dunn A. R. (2014). The minimal cadherin-catenin complex binds to actin filaments under force. Science 346, 1254211 10.1126/science.1254211 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  6. Butler J. P., Tolic-Norrelykke I. M., Fabry B. and Fredberg J. J. (2002). Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Cell Physiol. 282, C595-C605. 10.1152/ajpcell.00270.2001 [DOI] [PubMed] [Google Scholar] · DOI
  7. Cavey M., Rauzi M., Lenne P.-F. and Lecuit T. (2008). A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453, 751-756. 10.1038/nature06953 [DOI] [PubMed] [Google Scholar] · DOI
  8. Cluzel C., Saltel F., Lussi J., Paulhe F., Imhof B. A. and Wehrle-Haller B. (2005). The mechanisms and dynamics of (alpha)v(beta)3 integrin clustering in living cells. J. Cell Biol. 171, 383-392. 10.1083/jcb.200503017 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  9. Collins C., Guilluy C., Welch C., O'Brien E. T., Hahn K., Superfine R., Burridge K. and Tzima E. (2012). Localized tensional forces on PECAM-1 elicit a global mechanotransduction response via the integrin-RhoA pathway. Curr. Biol. 22, 2087-2094. 10.1016/j.cub.2012.08.051 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  10. Coon B. G., Baeyens N., Han J., Budatha M., Ross T. D., Fang J. S., Yun S., Thomas J.-L. and Schwartz M. A. (2015). Intramembrane binding of VE-cadherin to VEGFR2 and VEGFR3 assembles the endothelial mechanosensory complex. J. Cell Biol. 208, 975-986. 10.1083/jcb.201408103 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  11. Cully M., You H., Levine A. J. and Mak T. W. (2006). Beyond PTEN mutations: the PI3K pathway as an integrator of multiple inputs during tumorigenesis. Nat. Rev. Cancer 6, 184-192. 10.1038/nrc1819 [DOI] [PubMed] [Google Scholar] · DOI
  12. 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. 10.1083/jcb.200703010 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  13. Desai R., Sarpal R., Ishiyama N., Pellikka M., Ikura M. and Tepass U. (2013). Monomeric alpha-catenin links cadherin to the actin cytoskeleton. Nat. Cell Biol. 15, 261-273. 10.1038/ncb2685 [DOI] [PubMed] [Google Scholar] · DOI
  14. Fedor-Chaikin M., Hein P. W., Stewart J. C., Brackenbury R. and Kinch M. S. (2003). E-cadherin binding modulates EGF receptor activation. Cell Commun. Adhes. 10, 105-118. 10.1080/cac.10.2.105.118 [DOI] [PubMed] [Google Scholar] · DOI
  15. Fruman D. A., Meyers R. E. and Cantley L. C. (1998). Phosphoinositide kinases. Annu. Rev. Biochem. 67, 481-507. 10.1146/annurev.biochem.67.1.481 [DOI] [PubMed] [Google Scholar] · DOI
  16. Geiger B. and Yamada K. M. (2011). Molecular architecture and function of matrix adhesions. Cold Spring Harb. Perspect. Biol. 3, a005033 10.1101/cshperspect.a005033 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  17. Gonon E. M., Skalski M., Kean M. and Coppolino M. G. (2005). SNARE-mediated membrane traffic modulates RhoA-regulated focal adhesion formation. FEBS Lett. 579, 6169-6178. 10.1016/j.febslet.2005.09.090 [DOI] [PubMed] [Google Scholar] · DOI
  18. Guilluy C., Swaminathan V., Garcia-Mata R., O'Brien E. T., Superfine R. and Burridge K. (2011). The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat. Cell Biol. 13, 722-727. 10.1038/ncb2254 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  19. Hahn C. and Schwartz M. A. (2009). Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10, 53-62. 10.1038/nrm2596 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  20. Hall D. E., Reichardt L. F., Crowley E., Holley B., Moezzi H., Sonnenberg A. and Damsky C. H. (1990). The alpha 1/beta 1 and alpha 6/beta 1 integrin heterodimers mediate cell attachment to distinct sites on laminin. J. Cell Biol. 110, 2175-2184. 10.1083/jcb.110.6.2175 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  21. Hazan R. B. and Norton L. (1998). The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton. J. Biol. Chem. 273, 9078-9084. 10.1074/jbc.273.15.9078 [DOI] [PubMed] [Google Scholar] · DOI
  22. Higashida C., Kiuchi T., Akiba Y., Mizuno H., Maruoka M., Narumiya S., Mizuno K. and Watanabe N. (2013). F- and G-actin homeostasis regulates mechanosensitive actin nucleation by formins. Nat. Cell Biol. 15, 395-405. 10.1038/ncb2693 [DOI] [PubMed] [Google Scholar] · DOI
  23. Hirata H., Tatsumi H. and Sokabe M. (2008). Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J. Cell Sci. 121, 2795-2804. 10.1242/jcs.030320 [DOI] [PubMed] [Google Scholar] · DOI
  24. Hu S., Chen J., Fabry B., Numaguchi Y., Gouldstone A., Ingber D. E., Fredberg J. J., Butler J. P. and Wang N. (2003). Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells. Am. J. Physiol. Cell Physiol. 285, C1082-C1090. 10.1152/ajpcell.00159.2003 [DOI] [PubMed] [Google Scholar] · DOI
  25. Jasaitis A., Estevez M., Heysch J., Ladoux B. and Dufour S. (2012). E-cadherin-dependent stimulation of traction force at focal adhesions via the Src and PI3K signaling pathways. Biophys. J. 103, 175-184. 10.1016/j.bpj.2012.06.009 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  26. Katsumi A., Naoe T., Matsushita T., Kaibuchi K. and Schwartz M. A. (2005). Integrin activation and matrix binding mediate cellular responses to mechanical stretch. J. Biol. Chem. 280, 16546-16549. 10.1074/jbc.C400455200 [DOI] [PubMed] [Google Scholar] · DOI
  27. Kim J.-H. and Asthagiri A. R. (2011). Matrix stiffening sensitizes epithelial cells to EGF and enables the loss of contact inhibition of proliferation. J. Cell Sci. 124, 1280-1287. 10.1242/jcs.078394 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  28. 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. 10.1073/pnas.0812651106 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  29. Kim T.-J., Zheng S., Sun J., Muhamed I., Wu J., Lei L., Kong X., Leckband D. E. and Wang Y. (2015). Dynamic visualization of alpha-catenin reveals rapid, reversible conformation switching between tension states. Curr. Biol. 25, 218-224. 10.1016/j.cub.2014.11.017 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  30. Kovacs E. M., Ali R. G., McCormack A. J. and Yap A. S. (2002). E-cadherin homophilic ligation directly signals through Rac and Phosphatidylinositol 3-kinase to regulate adhesive contacts. J. Biol. Chem. 277, 6708-6718. 10.1074/jbc.M109640200 [DOI] [PubMed] [Google Scholar] · DOI
  31. Ladoux B., Anon E., Lambert M., Rabodzey A., Hersen P., Buguin A., Silberzan P. and Mege R.-M. (2010). Strength dependence of cadherin-mediated adhesions. Biophys. J. 98, 534-542. 10.1016/j.bpj.2009.10.044 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  32. le Duc Q., Shi Q., Blonk I., Sonnenberg A., Wang N., Leckband D. and de Rooij J. (2010). Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a MyosinII dependent manner. J. Cell Biol. 189, 1107-1115. 10.1083/jcb.201001149 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  33. Leckband D. E. and de Rooij J. (2014). Cadherin adhesion and mechanotransduction. Annu. Rev. Cell Dev. Biol. 30, 291-315. 10.1146/annurev-cellbio-100913-013212 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  34. Leckband D. E., le Duc Q., Wang N. and de Rooij J. (2011). Mechanotransduction at cadherin-mediated adhesions. Curr. Opin. Cell Biol. 23, 523-530. 10.1016/j.ceb.2011.08.003 [DOI] [PubMed] [Google Scholar] · DOI
  35. Leerberg J. M., Gomez G. A., Verma S., Moussa E. J., Wu S. K., Priya R., Hoffman B. D., Grashoff C., Schwartz M. A. and Yap A. S. (2014). Tension-sensitive actin assembly supports contractility at the epithelial zonula adherens. Curr. Biol. 24, 1689-1699. 10.1016/j.cub.2014.06.028 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  36. Liu Z., Tan J. L., Cohen D. M., Yang M. T., Sniadecki N. J., Ruiz S. A., Nelson C. M. and Chen C. S. (2010). Mechanical tugging force regulates the size of cell-cell junctions. Proc. Natl. Acad. Sci. USA 107, 9944-9949. 10.1073/pnas.0914547107 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  37. Lorch J. H., Klessner J., Park J. K., Getsios S., Wu Y. L., Stack M. S. and Green K. J. (2004). Epidermal growth factor receptor inhibition promotes desmosome assembly and strengthens intercellular adhesion in squamous cell carcinoma cells. J. Biol. Chem. 279, 37191-37200. 10.1074/jbc.M405123200 [DOI] [PubMed] [Google Scholar] · DOI
  38. Mariner D. J., Davis M. A. and Reynolds A. B. (2004). EGFR signaling to p120-catenin through phosphorylation at Y228. J. Cell Sci. 117, 1339-1350. 10.1242/jcs.01001 [DOI] [PubMed] [Google Scholar] · DOI
  39. McClatchey A. I. and Yap A. S. (2012). Contact inhibition (of proliferation) redux. Curr. Opin. Cell Biol. 24, 685-694. 10.1016/j.ceb.2012.06.009 [DOI] [PubMed] [Google Scholar] · DOI
  40. McLachlan R. W. and Yap A. S. (2007). Not so simple: the complexity of phosphotyrosine signaling at cadherin adhesive contacts. J. Mol. Med. 85, 545-554. 10.1007/s00109-007-0198-x [DOI] [PubMed] [Google Scholar] · DOI
  41. McLachlan R. W. and Yap A. S. (2011). Protein tyrosine phosphatase activity is necessary for E-cadherin-activated Src signaling. Cytoskeleton 68, 32-43. 10.1002/cm.20492 [DOI] [PubMed] [Google Scholar] · DOI
  42. McLachlan R. W., Kraemer A., Helwani F. M., Kovacs E. M. and Yap A. S. (2007). E-cadherin adhesion activates c-Src signaling at cell-cell contacts. Mol. Biol. Cell 18, 3214-3223. 10.1091/mbc.E06-12-1154 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  43. Mould A. P. (2002). Analyzing integrin-dependent adhesion. Curr. Protoc. Cell Biol. Chapter 9, Unit 9 4 10.1002/0471143030.cb0904s15 [DOI] [PubMed] [Google Scholar] · DOI
  44. Nagafuchi A., Takeichi M. and Tsukita S. (1991). The 102 kd cadherin-associated protein: similarity to vinculin and posttranscriptional regulation of expression. Cell 65, 849-857. 10.1016/0092-8674(91)90392-C [DOI] [PubMed] [Google Scholar] · DOI
  45. Nagai T., Yamakawa N., Aota S., Yamada S. S., Akiyama S. K., Olden K. and Yamada K. M. (1991). Monoclonal antibody characterization of two distant sites required for function of the central cell-binding domain of fibronectin in cell adhesion, cell migration, and matrix assembly. J. Cell Biol. 114, 1295-1305. 10.1083/jcb.114.6.1295 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  46. Noren N. K., Arthur W. T. and Burridge K. (2003). Cadherin engagement inhibits RhoA via p190RhoGAP. J. Biol. Chem. 278, 13615-13618. 10.1074/jbc.C200657200 [DOI] [PubMed] [Google Scholar] · DOI
  47. Oldenburg J., van der Krogt G., Twiss F., Bongaarts A., Habani Y., Slotman J. A., Houtsmuller A., Huveneers S. and de Rooij J. (2015). VASP, zyxin and TES are tension-dependent members of Focal Adherens Junctions independent of the alpha-catenin-vinculin module. Sci. Rep. 5, 17225 10.1038/srep17225 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  48. Orr A. W., Ginsberg M. H., Shattil S. J., Deckmyn H. and Schwartz M. A. (2006). Matrix-specific suppression of integrin activation in shear stress signaling. Mol. Biol. Cell 17, 4686-4697. 10.1091/mbc.E06-04-0289 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  49. Ozawa M., Hoschutzky H., Herrenknecht K. and Kemler R. (1990). A possible new adhesive site in the cell-adhesion molecule uvomorulin. Mech. Dev. 33, 49-56. 10.1016/0925-4773(90)90134-8 [DOI] [PubMed] [Google Scholar] · DOI
  50. Paez J. G., Janne P. A., Lee J. C., Tracy S., Greulich H., Gabriel S., Herman P., Kaye F. J., Lindeman N., Boggon T. J. et al. (2004). EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304, 1497-1500. 10.1126/science.1099314 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  51. Pece S. and Gutkind J. S. (2000). Signaling from E-cadherins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation. J. Biol. Chem. 275, 41227-41233. 10.1074/jbc.M006578200 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  52. Perez T. D., Tamada M., Sheetz M. P. and Nelson W. J. (2008). Immediate-early signaling induced by E-cadherin engagement and adhesion. J. Biol. Chem. 283, 5014-5022. 10.1074/jbc.M705209200 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  53. Perrais M., Chen X., Perez-Moreno M. and Gumbiner B. M. (2007). E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. Mol. Biol. Cell 18, 2013-2025. 10.1091/mbc.E06-04-0348 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  54. Petrova Y. I., Spano M. M. and Gumbiner B. M. (2012). Conformational epitopes at cadherin calcium-binding sites and p120-catenin phosphorylation regulate cell adhesion. Mol. Biol. Cell 23, 2092-2108. 10.1091/mbc.E11-12-1060 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  55. Prakasam A. K., Maruthamuthu V. and Leckband D. E. (2006). Similarities between heterophilic and homophilic cadherin adhesion. Proc. Natl. Acad. Sci. USA 103, 15434-15439. 10.1073/pnas.0606701103 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  56. Qian X., Karpova T., Sheppard A. M., McNally J. and Lowy D. R. (2004). E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J. 23, 1739-1784. 10.1038/sj.emboj.7600136 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  57. Ratheesh A., Priya R. and Yap A. S. (2013). Coordinating Rho and Rac: the regulation of Rho GTPase signaling and cadherin junctions. Prog. Mol. Biol. Transl. Sci. 116, 49-68. 10.1016/B978-0-12-394311-8.00003-0 [DOI] [PubMed] [Google Scholar] · DOI
  58. Riveline D., Zamir E., Balaban N. Q., Schwarz U. S., Ishizaki T., Narumiya S., Kam Z., Geiger B. and Bershadsky A. D. (2001). Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153, 1175-1186. 10.1083/jcb.153.6.1175 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  59. Sakaguchi M., Sonegawa H., Murata H., Kitazoe M., Futami J.-I., Kataoka K., Yamada H. and Huh N.-H. (2008). S100A11, an dual mediator for growth regulation of human keratinocytes. Mol. Biol. Cell 19, 78-85. 10.1091/mbc.E07-07-0682 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  60. Schluck T., Nienhaus U., Aegerter-Wilmsen T. and Aegerter C. M. (2013). Mechanical control of organ size in the development of the Drosophila wing disc. PLoS ONE 8, e76171 10.1371/journal.pone.0076171 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  61. Schwartz M. A. and DeSimone D. W. (2008). Cell adhesion receptors in mechanotransduction. Curr. Opin. Cell Biol. 20, 551-556. 10.1016/j.ceb.2008.05.005 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  62. Seong J., Tajik A., Sun J., Guan J.-L., Humphries M. J., Craig S. E., Shekaran A., Garcia A. J., Lu S., Lin M. Z. et al. (2013). Distinct biophysical mechanisms of focal adhesion kinase mechanoactivation by different extracellular matrix proteins. Proc. Natl. Acad. Sci. USA 110, 19372-19377. 10.1073/pnas.1307405110 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  63. Shashikanth N., Petrova Y. I., Park S., Chekan J., Maiden S., Spano M., Ha T., Gumbiner B. M. and Leckband D. E. (2015). Allosteric regulation of E-cadherin adhesion. J. Biol. Chem. 290, 21749-21761. 10.1074/jbc.M115.657098 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  64. Shewan A. M., Maddugoda M., Kraemer A., Stehbens S. J., Verma S., Kovacs E. M. and Yap A. S. (2005). Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 16, 4531-4542. 10.1091/mbc.E05-04-0330 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  65. Tabdili H., Barry A. K., Langer M. D., Chien Y.-H., Shi Q., Lee K. J. and Leckband D. E. (2012a). Cadherin point mutations alter cell sorting and modulate GTPase signaling. J. Cell Sci. 125, 3299-3309. 10.1242/jcs.087395 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  66. Tabdili H., Langer M., Shi Q., Poh Y.-C., Wang N. and Leckband D. (2012b). Cadherin-dependent mechanotransduction depends on ligand identity but not affinity. J. Cell Sci. 125, 4362-4371. 10.1242/jcs.105775 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  67. Takeichi M. and Nakagawa S. (2001). Cadherin-dependent cell-cell adhesion. Curr. Protoc. Cell Biol. Chapter 9, Unit 9 3 10.1002/0471143030.cb0903s00 [DOI] [PubMed] [Google Scholar] · DOI
  68. Tepass U., Godt D. and Winklbauer R. (2002). Cell sorting in animal development: signalling and adhesive mechanisms in the formation of tissue boundaries. Curr. Opin. Genet. Dev. 12, 572-582. 10.1016/S0959-437X(02)00342-8 [DOI] [PubMed] [Google Scholar] · DOI
  69. Thomas W. A., Boscher C., Chu Y.-S., Cuvelier D., Martinez-Rico C., Seddiki R., Heysch J., Ladoux B., Thiery J. P., Mege R.-M. et al. (2013). alpha-catenin and vinculin cooperate to promote high E-cadherin-based adhesion strength. J. Biol. Chem. 288, 4957-4969. 10.1074/jbc.M112.403774 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  70. Tse J. R. and Engler A. J. (2010). Preparation of hydrogel substrates with tunable mechanical properties. Curr. Protoc. Cell Biol. Chapter 10, Unit 10 16 10.1002/0471143030.cb1016s47 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  71. Twiss F., Le Duc Q., Van Der Horst S., Tabdili H., Van Der Krogt G., Wang N., Rehmann H., Huveneers S., Leckband D. E. and De Rooij J. (2012). Vinculin-dependent Cadherin mechanosensing regulates efficient epithelial barrier formation. Biol. Open 1, 1128-1140. 10.1242/bio.20122428 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  72. Tzima E., del Pozo M. A., Shattil S. J., Chien S. and Schwartz M. A. (2001). Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J. 20, 4639-4647. 10.1093/emboj/20.17.4639 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  73. Tzima E., Irani-Tehrani M., Kiosses W. B., Dejana E., Schultz D. A., Engelhardt B., Cao G., DeLisser H. and Schwartz M. A. (2005). A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426-431. 10.1038/nature03952 [DOI] [PubMed] [Google Scholar] · DOI
  74. Vasudevan K. M., Barbie D. A., Davies M. A., Rabinovsky R., McNear C. J., Kim J. J., Hennessy B. T., Tseng H., Pochanard P., Kim S. Y. et al. (2009). AKT-independent signaling downstream of oncogenic PIK3CA mutations in human cancer. Cancer Cell 16, 21-32. 10.1016/j.ccr.2009.04.012 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  75. Vlahos C. J., Matter W. F., Hui K. Y. and Brown R. F. (1994). A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248. [PubMed] [Google Scholar]
  76. Wang N., Butler J. P. and Ingber D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127. 10.1126/science.7684161 [DOI] [PubMed] [Google Scholar] · DOI
  77. Wang Y., Boltvinick E. L., Zhao Y., Berns M. W., Usami S., Tsien R. Y. and Chien S. (2005). Visualizing the mechanical activation of Src. Nature 434, 1040-1045. 10.1038/nature03469 [DOI] [PubMed] [Google Scholar] · DOI
  78. Watanabe T., Sato K. and Kaibuchi K. (2009). Cadherin-mediated intercellular adhesion and signaling cascades involving small GTPases. Cold Spring Harb. Perspect. Biol. 1, a003020 10.1101/cshperspect.a003020 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  79. Weber G. F., Bjerke M. A. and DeSimone D. W. (2011). Integrins and cadherins join forces to form adhesive networks. J. Cell Sci. 124, 1183-1193. 10.1242/jcs.064618 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  80. Weber G. F., Bjerke M. A. and DeSimone D. W. (2012). A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev. Cell 22, 104-115. 10.1016/j.devcel.2011.10.013 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  81. Wheelock M. J. and Johnson K. R. (2003). Cadherins as modulators of cellular phenotype. Annu. Rev. Cell Dev. Biol. 19, 207-235. 10.1146/annurev.cellbio.19.011102.111135 [DOI] [PubMed] [Google Scholar] · DOI
  82. Yao M., Qiu W., Liu R., Efremov A. K., Cong P., Seddiki R., Payre M., Lim C. T., Ladoux B., Mege R.-M. et al. (2014). Force-dependent conformational switch of alpha-catenin controls vinculin binding. Nat. Commun. 5, 4525 10.1038/ncomms5525 [DOI] [PubMed] [Google Scholar] · DOI
  83. Yen H.-Y., Liu Y.-C., Chen N.-Y., Tsai C.-F., Wang Y.-T., Chen Y.-J., Hsu T.-L., Yang P.-C. and Wong C.-H. (2015). Effect of sialylation on EGFR phosphorylation and resistance to tyrosine kinase inhibition. Proc. Natl. Acad. Sci. USA 112, 6955-6960. 10.1073/pnas.1507329112 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  84. Yonemura S., Wada Y., Watanabe T., Nagafuchi A. and Shibata M. (2010). alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12, 533-542. 10.1038/ncb2055 [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  85. Zaidel-Bar R. and Geiger B. (2010). The switchable integrin adhesome. J. Cell Sci. 123, 1385-1388. 10.1242/jcs.066183 [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  86. Zamir E., Katz B. Z., Aota S., Yamada K. M., Geiger B. and Kam Z. (1999). Molecular diversity of cell-matrix adhesions. J. Cell Sci. 112, 1655-1669. [DOI] [PubMed] [Google Scholar]

Cited by

Sorted by citations

Authors
Muhamed, I., Wu, J., Sehgal, P., Kong, X., Tajik, A., Wang, N., & Leckband, D. E.
Affiliations
University of Illinois Urbana-Champaign (US)
Venue
Journal of Cell Science
Published
2016-05-01
Volume
129
Issue
9
Pages
1843-1854
ISSN
  • 0021-9533 (ISSN-L)
  • 1477-9137
OpenAlex
W2296441026
Cited by
97
References
3
Citations by year
2026: 6 · 2025: 13 · 2024: 5 · 2023: 9 · 2022: 9 · 2021: 9 · 2020: 8 · 2019: 7 · 2018: 12 · 2017: 15 · 2016: 4
FWCI
8.72
Type
journal article
Language
en
Open access
Locations
  • Journal of Cell Science (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HighWire Press Open Archive (submittedVersion)
Funders
  • National Institutes of Health (R01 GM097443)
  • National Science Foundation (1029871, 1462739)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
  • Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Force Microscopy Techniques and Applications
Keywords
E-cadherin, force transduction, cell mechanics, epidermal growth factor receptor, phosphatidylinositol 3-kinase, integrin-mediated adhesion, alpha-catenin, cytoskeletal remodeling, myosin II, cell contractility, mechanotransduction, magnetic twisting cytometry, traction force microscopy
MeSH terms
Animals, Cytoskeleton, Dogs, Humans, Cadherins, Mechanotransduction, Cellular, alpha Catenin, Madin Darby Canine Kidney Cells, MCF-7 Cells, ErbB Receptors

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