Adhesion to fibronectin regulates Hippo signaling via the FAK-Src-PI3K pathway

Journal of Cell Biology

Volumn 210, Issue 3, 2015, Pages 503-515

  Kim, Nam Gyun ^a   Gumbiner, Barry M ^a,b  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; FOCAL ADHESION KINASE 1; LAMININ; PHOSPHATIDYLINOSITOL 3 KINASE; POLYLYSINE; STEROID RECEPTOR COACTIVATOR 1; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN; HIPPO PROTEIN, HUMAN; LATS1 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 4,5-BIPHOSPHATE KINASE; PHOSPHOPROTEIN; PHOSPHOTRANSFERASE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; PTK2 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

ARTICLE; CELL ADHESION; CELL DENSITY; CELL SPREADING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HIPPO PATHWAY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CELL LINE; CELL PROLIFERATION; CONTACT INHIBITION; GENETICS; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE; CELL PROLIFERATION; CONTACT INHIBITION; FIBRONECTINS; FOCAL ADHESION KINASE 1; HUMANS; LAMININ; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEINS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); POLYLYSINE; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84953394763     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201501025     Document Type: Article

References (63)

1. Aragona, M., T. Panciera, A. Manfrin, S. Giulitti, F. Michielin, N. Elvassore, S. Dupont, and S. Piccolo. 2013. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell. 154:1047-1059. http://dx.doi.org/10.1016/j.cell.2013.07.042.
2. Basu, S., N.F. Totty, M.S. Irwin, M. Sudol, and J. Downward. 2003. Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis. Mol. Cell. 11:11-23. http://dx.doi.org/10.1016/S1097-2765(02)00776-1.
3. Cabodi, S., M. del Pilar Camacho-Leal, P. Di Stefano, and P. Defilippi. 2010. Integrin signalling adaptors: not only figurants in the cancer story. Nat. Rev. Cancer. 10:858-870. http://dx.doi.org/10.1038/nrc2967.
4. Calvo, F., N. Ege, A. Grande-Garcia, S. Hooper, R.P. Jenkins, S.I. Chaudhry, K. Harrington, P. Williamson, E. Moeendarbary, G. Charras, and E. Sahai. 2013. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat. Cell Biol. 15:637-646. http://dx.doi.org/10.1038/ncb2756.
5. Debnath, J., S.K. Muthuswamy, and J.S. Brugge. 2003. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods. 30:256-268. http://dx.doi.org/10.1016/S1046-2023(03)00032-X.
6. Di Paolo, G., and P. De Camilli. 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature. 443:651-657. http://dx.doi.org/10.1038/nature05185.
7. Dupont, S., L. Morsut, M. Aragona, E. Enzo, S. Giulitti, M. Cordenonsi, F. Zanconato, J. Le Digabel, M. Forcato, S. Bicciato, et al. 2011. Role of YAP/TAZ in mechanotransduction. Nature. 474:179-183. http://dx.doi.org/10.1038/nature10137.
8. Enomoto, M., and T. Igaki. 2013. Src controls tumorigenesis via JNK-dependent regulation of the Hippo pathway in Drosophila. EMBO Rep. 14:65-72. http://dx.doi.org/10.1038/embor.2012.185.
9. Fan, R., N.G. Kim, and B.M. Gumbiner. 2013. Regulation of Hippo pathway by mitogenic growth factors via phosphoinositide 3-kinase and phosphoinositide-dependent kinase-1. Proc. Natl. Acad. Sci. USA. 110:2569-2574. http://dx.doi.org/10.1073/pnas.1216462110.
10. Govindarajan, G., D.M. Eble, P.A. Lucchesi, and A.M. Samarel. 2000. Focal adhesion kinase is involved in angiotensin II-mediated protein synthesis in cultured vascular smooth muscle cells. Circ. Res. 87:710-716. http://dx.doi.org/10.1161/01.RES.87.8.710.
11. Gu, J., Y. Sumida, N. Sanzen, and K. Sekiguchi. 2001. Laminin-10/11 and fibronectin differentially regulate integrin-dependent Rho and Rac activation via p130Cas-CrkII-DOCK180 pathway. J. Biol. Chem. 276:27090-27097. http://dx.doi.org/10.1074/jbc. M102284200.
12. Gumbiner, B.M., and N.G. Kim. 2014. The Hippo-YAP signaling pathway and contact inhibition of growth. J. Cell Sci. 127:709-717. http://dx.doi.org/10.1242/jcs.140103.
13. Halder, G., S. Dupont, and S. Piccolo. 2012. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 13:591-600. http://dx.doi.org/10.1038/nrm3416.
14. Hynes, R.O. 2009. The extracellular matrix: not just pretty fibrils. Science. 326:1216-1219. http://dx.doi.org/10.1126/science.1176009.
15. Johnson, R., and G. Halder. 2014. The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat. Rev. Drug Discov. 13:63-79. http://dx.doi.org/10.1038/nrd4161.
16. Kaneko, K., M. Ito, Y. Naoe, A. Lacy-Hulbert, and K. Ikeda. 2014. Integrin av in the mechanical response of osteoblast lineage cells. Biochem. Biophys. Res. Commun. 447:352-357. http://dx.doi.org/10.1016/j.bbrc.2014.04.006.
17. Kim, J.H., and A.R. Asthagiri. 2011. Matrix stiffening sensitizes epithelial cells to EGF and enables the loss of contact inhibition of proliferation. J. Cell Sci. 124:1280-1287. http://dx.doi.org/10.1242/jcs.078394.
18. Kim, J.H., K. Kushiro, N.A. Graham, and A.R. Asthagiri. 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. http://dx.doi.org/10.1073/pnas.0812651106.
19. Kim, N.G., E. Koh, X. Chen, and B.M. Gumbiner. 2011. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc. Natl. Acad. Sci. USA. 108:11930-11935. http://dx.doi.org/10.1073/pnas.1103345108.
20. Kim, M., M. Kim, S. Lee, S. Kuninaka, H. Saya, H. Lee, S. Lee, and D.S. Lim. 2013. cAMP/PKA signalling reinforces the LATS-YAP pathway to fully suppress YAP in response to actin cytoskeletal changes. EMBO J. 32:1543-1555. http://dx.doi.org/10.1038/emboj.2013.102.
21. Kinoshita, E., E. Kinoshita-Kikuta, K. Takiyama, and T. Koike. 2006. Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics. 5:749-757. http://dx.doi.org/10.1074/mcp. T500024-MCP200.
22. Komuro, A., M. Nagai, N.E. Navin, and M. Sudol. 2003. WW domain-containing protein YAP associates with ErbB-4 and acts as a co-transcriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J. Biol. Chem. 278:33334-33341. http://dx.doi.org/10.1074/jbc. M305597200.
23. Korinek, V., N. Barker, P.J. Morin, D. van Wichen, R. de Weger, K.W. Kinzler, B. Vogelstein, and H. Clevers. 1997. Constitutive transcriptional activation by a ß-catenin-Tcf complex in APC-/-colon carcinoma. Science. 275:1784-1787. http://dx.doi.org/10.1126/science.275.5307.1784.
24. Lamesch, P., N. Li, S. Milstein, C. Fan, T. Hao, G. Szabo, Z. Hu, K. Venkatesan, G. Bethel, P. Martin, et al. 2007. hORFeome v3.1: a resource of human open reading frames representing over 10, 000 human genes. Genomics. 89:307-315. http://dx.doi.org/10.1016/j.ygeno.2006.11.012.
25. Li, L., M. Okura, and A. Imamoto. 2002. Focal adhesions require catalytic activity of Src family kinases to mediate integrin-matrix adhesion. Mol. Cell. Biol. 22:1203-1217. http://dx.doi.org/10.1128/MCB.22.4.1203-1217.2002.
26. Low, B.C., C.Q. Pan, G.V. Shivashankar, A. Bershadsky, M. Sudol, and M. Sheetz. 2014. YAP/TAZ as mechanosensors and mechanotransducers in regulating organ size and tumor growth. FEBS Lett. 588:2663-2670. http://dx.doi.org/10.1016/j.febslet.2014.04.012.
27. Lu, Y., Q. Yu, J.H. Liu, J. Zhang, H. Wang, D. Koul, J.S. McMurray, X. Fang, W.K. Yung, K.A. Siminovitch, and G.B. Mills. 2003. Src family protein-tyrosine kinases alter the function of PTEN to regulate phosphatidylinositol 3-kinase/AKT cascades. J. Biol. Chem. 278:40057-40066. http://dx.doi.org/10.1074/jbc. M303621200.
28. McClatchey, A.I., and A.S. Yap. 2012. Contact inhibition (of proliferation) redux. Curr. Opin. Cell Biol. 24:685-694. http://dx.doi.org/10.1016/j.ceb.2012.06.009.
29. Miller, E., J. Yang, M. DeRan, C. Wu, A.I. Su, G.M. Bonamy, J. Liu, E.C. Peters, and X. Wu. 2012. Identification of serum-derived sphingosine-1-phosphate as a small molecule regulator of YAP. Chem. Biol. 19:955-962. http://dx.doi.org/10.1016/j.chembiol.2012.07.005.
30. Mo, J.S., F.X. Yu, R. Gong, J.H. Brown, and K.L. Guan. 2012. Regulation of the Hippo-YAP pathway by protease-activated receptors (PARs). Genes Dev. 26:2138-2143. http://dx.doi.org/10.1101/gad.197582.112.
31. Morin-Kensicki, E.M., B.N. Boone, M. Howell, J.R. Stonebraker, J. Teed, J.G. Alb, T.R. Magnuson, W. O'Neal, and S.L. Milgram. 2006. Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol. Cell. Biol. 26:77-87. http://dx.doi.org/10.1128/MCB.26.1.77-87.2006.
32. Nakajima, K., and Y. Yaoita. 1997. Construction of multiple-epitope tag sequence by PCR for sensitive Western blot analysis. Nucleic Acids Res. 25:2231-2232. http://dx.doi.org/10.1093/nar/25.11.2231.
33. Okada, M. 2012. Regulation of the SRC family kinases by Csk. Int. J. Biol. Sci. 8:1385-1397. http://dx.doi.org/10.7150/ijbs.5141.
34. Pleiman, C.M., W.M. Hertz, and J.C. Cambier. 1994. Activation of phosphatidylinositol-3' kinase by Src-family kinase SH3 binding to the p85 subunit. Science. 263:1609-1612. http://dx.doi.org/10.1126/science.8128248.
35. Provenzano, P.P., and P.J. Keely. 2011. Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J. Cell Sci. 124:1195-1205. http://dx.doi.org/10.1242/jcs.067009.
36. Richardson, A., R.K. Malik, J.D. Hildebrand, and J.T. Parsons. 1997. Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation. Mol. Cell. Biol. 17:6906-6914.
37. Roberts, W.G., E. Ung, P. Whalen, B. Cooper, C. Hulford, C. Autry, D. Richter, E. Emerson, J. Lin, J. Kath, et al. 2008. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562, 271. Cancer Res. 68:1935-1944. http://dx.doi.org/10.1158/0008-5472.CAN-07-5155.
38. Rosenbluh, J., D. Nijhawan, A.G. Cox, X. Li, J.T. Neal, E.J. Schafer, T.I. Zack, X. Wang, A. Tsherniak, A.C. Schinzel, et al. 2012. ß-Catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell. 151:1457-1473. http://dx.doi.org/10.1016/j.cell.2012.11.026.
39. Sandilands, E., C. Cans, V.J. Fincham, V.G. Brunton, H. Mellor, G.C. Prendergast, J.C. Norman, G. Superti-Furga, and M.C. Frame. 2004. RhoB and actin polymerization coordinate Src activation with endosome-mediated delivery to the membrane. Dev. Cell. 7:855-869. http://dx.doi.org/10.1016/j.devcel.2004.09.019.
40. Sansores-Garcia, L., W. Bossuyt, K. Wada, S. Yonemura, C. Tao, H. Sasaki, and G. Halder. 2011. Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J. 30:2325-2335. http://dx.doi.org/10.1038/emboj.2011.157.
41. Schwartz, M.A. 2010. Integrins and extracellular matrix in mechanotransduction. Cold Spring Harb. Perspect. Biol. 2:a005066. http://dx.doi.org/10.1101/cshperspect.a005066.
42. Shao, D.D., W. Xue, E.B. Krall, A. Bhutkar, F. Piccioni, X. Wang, A.C. Schinzel, S. Sood, J. Rosenbluh, J.W. Kim, et al. 2014. KRAS and YAP1 converge to regulate EMT and tumor survival. Cell. 158:171-184. http://dx.doi.org/10.1016/j.cell.2014.06.004.
43. Sieg, D.J., C.R. Hauck, and D.D. Schlaepfer. 1999. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci. 112:2677-2691.
44. Slack-Davis, J.K., K.H. Martin, R.W. Tilghman, M. Iwanicki, E.J. Ung, C. Autry, M.J. Luzzio, B. Cooper, J.C. Kath, W.G. Roberts, and J.T. Parsons. 2007. Cellular characterization of a novel focal adhesion kinase inhibitor. J. Biol. Chem. 282:14845-14852. http://dx.doi.org/10.1074/jbc. M606695200.
45. Straßburger, K., M. Tiebe, F. Pinna, K. Breuhahn, and A.A. Teleman. 2012. Insulin/IGF signaling drives cell proliferation in part via Yorkie/YAP. Dev. Biol. 367:187-196. http://dx.doi.org/10.1016/j.ydbio.2012.05.008.
46. Sudol, M. 1994. Yes-associated protein (YAP65) is a proline-rich phosphoprotein that binds to the SH3 domain of the Yes proto-oncogene product. Oncogene. 9:2145-2152.
47. Takeichi, M. 2014. Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling. Nat. Rev. Mol. Cell Biol. 15:397-410. http://dx.doi.org/10.1038/nrm3802.
48. Tang, Y., R.G. Rowe, E.L. Botvinick, A. Kurup, A.J. Putnam, M. Seiki, V.M. Weaver, E.T. Keller, S. Goldstein, J. Dai, et al. 2013. MT1-MMP-dependent control of skeletal stem cell commitment via a ß1-integrin/YAP/TAZ signaling axis. Dev. Cell. 25:402-416. http://dx.doi.org/10.1016/j.devcel.2013.04.011.
49. Taniguchi, K., L.W. Wu, S.I. Grivennikov, P.R. de Jong, I. Lian, F.X. Yu, K. Wang, S.B. Ho, B.S. Boland, J.T. Chang, et al. 2015. A gp130-Src-YAP module links inflammation to epithelial regeneration. Nature. 519:57-62. http://dx.doi.org/10.1038/nature14228.
50. Thomas, S.M., and J.S. Brugge. 1997. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 13:513-609. http://dx.doi.org/10.1146/annurev.cellbio.13.1.513.
51. Tilghman, R.W., and J.T. Parsons. 2008. Focal adhesion kinase as a regulator of cell tension in the progression of cancer. Semin. Cancer Biol. 18:45-52. http://dx.doi.org/10.1016/j.semcancer.2007.08.002.
52. Varelas, X., P. Samavarchi-Tehrani, M. Narimatsu, A. Weiss, K. Cockburn, B.G. Larsen, J. Rossant, and J.L. Wrana. 2010. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-ß-SMAD pathway. Dev. Cell. 19:831-844. http://dx.doi.org/10.1016/j.devcel.2010.11.012.
53. Wada, K., K. Itoga, T. Okano, S. Yonemura, and H. Sasaki. 2011. Hippo pathway regulation by cell morphology and stress fibers. Development. 138:3907-3914. http://dx.doi.org/10.1242/dev.070987.
54. Weber, G.F., M.A. Bjerke, and D.W. DeSimone. 2011. Integrins and cadherins join forces to form adhesive networks. J. Cell Sci. 124:1183-1193. http://dx.doi.org/10.1242/jcs.064618.
55. Weiger, M.C., C.C. Wang, M. Krajcovic, A.T. Melvin, J.J. Rhoden, and J.M. Haugh. 2009. Spontaneous phosphoinositide 3-kinase signaling dynamics drive spreading and random migration of fibroblasts. J. Cell Sci. 122:313-323. http://dx.doi.org/10.1242/jcs.037564.
56. Welch, H.C., W.J. Coadwell, L.R. Stephens, and P.T. Hawkins. 2003. Phosphoinositide 3-kinase-dependent activation of Rac. FEBS Lett. 546:93-97. http://dx.doi.org/10.1016/S0014-5793(03)00454-X.
57. Yin, F., J. Yu, Y. Zheng, Q. Chen, N. Zhang, and D. Pan. 2013. Spatial organization of Hippo signaling at the plasma membrane mediated by the tumor suppressor Merlin/NF2. Cell. 154:1342-1355. http://dx.doi.org/10.1016/j.cell.2013.08.025.
58. Yu, F.X., B. Zhao, N. Panupinthu, J.L. Jewell, I. Lian, L.H. Wang, J. Zhao, H. Yuan, K. Tumaneng, H. Li, et al. 2012. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell. 150:780-791. http://dx.doi.org/10.1016/j.cell.2012.06.037.
59. Zaidi, S.K., A.J. Sullivan, R. Medina, Y. Ito, A.J. van Wijnen, J.L. Stein, J.B. Lian, and G.S. Stein. 2004. Tyrosine phosphorylation controls Runx2-mediated subnuclear targeting of YAP to repress transcription. EMBO J. 23:790-799. http://dx.doi.org/10.1038/sj.emboj.7600073.
60. Zhang, J., J.Y. Ji, M. Yu, M. Overholtzer, G.A. Smolen, R. Wang, J.S. Brugge, N.J. Dyson, and D.A. Haber. 2009. YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway. Nat. Cell Biol. 11:1444-1450. http://dx.doi.org/10.1038/ncb1993.
61. Zhao, B., X. Wei, W. Li, R.S. Udan, Q. Yang, J. Kim, J. Xie, T. Ikenoue, J. Yu, L. Li, et al. 2007. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21:2747-2761. http://dx.doi.org/10.1101/gad.1602907.
62. Zhao, B., X. Ye, J. Yu, L. Li, W. Li, S. Li, J. Yu, J.D. Lin, C.Y. Wang, A.M. Chinnaiyan, et al. 2008. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22:1962-1971. http://dx.doi.org/10.1101/gad.1664408.
63. Zhao, B., L. Li, L. Wang, C.Y. Wang, J. Yu, and K.L. Guan. 2012. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 26:54-68. http://dx.doi.org/10.1101/gad.173435.111.