αE-catenin inhibits a Src–YAP1 oncogenic module that couples tyrosine kinases and the effector of hippo signaling pathway

Genes and Development

Volumn 30, Issue 7, 2016, Pages 798-811

  Li, Peng ^a   Silvis, Mark R ^a   Honaker, Yuchi ^a   Lien, Wen Hui ^a,c   Arron, Sarah T ^b   Vasioukhin, Valeri ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DE DUVE INSTITUTE   (Belgium)

Author keywords

Keratinocytes; SCC; Skin; SRC; YAP1; E catenin

Indexed keywords

ALPHA CATENIN; ALPHA E CATENIN; BETA4 INTEGRIN; ONCOPROTEIN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE SRC; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG; PHOSPHOPROTEIN; PROTEIN KINASE P60; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; YAP PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA; TRANSCRIPTION INITIATION; ANIMAL; CELL CULTURE; CELL NUCLEUS; CELL PROLIFERATION; CELL TRANSFORMATION; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; KERATINOCYTE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALPHA CATENIN; ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL NUCLEUS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KERATINOCYTES; MICE; ONCOGENE PROTEIN PP60(V-SRC); PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

EID: 84962467132     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.274951.115     Document Type: Article

References (58)

1. Barry ER, Camargo FD. 2013. The Hippo superhighway: signaling crossroads converging on the Hippo/Yap pathway in stem cells and development. Curr Opin Cell Biol 25: 247–253.
2. Basu S, Totty NF, Irwin MS, Sudol M, Downward J. 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.
3. Benham-Pyle BW, Pruitt BL, Nelson WJ. 2015. Cell adhesion. Mechanical strain induces E-cadherin-dependent Yap1 and β-catenin activation to drive cell cycle entry. Science 348: 1024–1027.
4. Benjamin JM, Nelson WJ. 2008. Bench to bedside and back again: molecular mechanisms of α-catenin function and roles in tumorigenesis. Semin Cancer Biol 18: 53–64.
5. Bertotti A, Comoglio PM, Trusolino L. 2006. β4 integrin activates a Shp2–Src signaling pathway that sustains HGF-induced anchorage- independent growth. J Cell Biol 175: 993–1003.
6. Buckley CD, Tan J, Anderson KL, Hanein D, Volkmann N, Weis WI, Nelson WJ, Dunn AR. 2014. Cell adhesion. The minimal cadherin-catenin complex binds to actin filaments under force. Science 346: 1254211.
7. Bullions LC, Notterman DA, Chung LS, Levine AJ. 1997. Expression of wild-type α-catenin protein in cells with a mutant α- catenin gene restores both growth regulation and tumor suppressor activities. Mol Cell Biol 17: 4501–4508.
8. Collett MS, Purchio AF, Erikson RL. 1980. Avian sarcoma virustransforming protein, pp60src shows protein kinase activity specific for tyrosine. Nature 285: 167–169.
9. Collins C, Nelson WJ. 2015. Running with neighbors: coordinating cell migration and cell–cell adhesion. Curr Opin Cell Biol 36: 62–70.
10. Enderle L, McNeill H. 2013. Hippo gains weight: added insights and complexity to pathway control. Sci Signal 6: re7.
11. Enomoto M, Igaki T. 2013. Src controls tumorigenesis via JNKdependent regulation of the Hippo pathway in Drosophila. EMBO Rep 14: 65–72.
12. Ewing CM, Ru N, Morton RA, Robinson JC, Wheelock MJ, Johnson KR, Barrett JC, Isaacs WB. 1995. Chromosome 5 suppresses tumorigenicity of PC3 prostate cancer cells: correlation with re-expression of α-catenin and restoration of E-cadherin function. Cancer Res 55: 4813–4817.
13. Gottardi CJ, Gumbiner BM. 2004. Distinct molecular forms of β- catenin are targeted to adhesive or transcriptional complexes. J Cell Biol 167: 339–349.
14. Kassenbrock CK, Anderson SM. 2004. Regulation of ubiquitin protein ligase activity in c-Cbl by phosphorylation-induced conformational change and constitutive activation by tyrosine to glutamate point mutations. J Biol Chem 279: 28017–28027.
15. Kim NG, Gumbiner BM. 2015. Adhesion to fibronectin regulates Hippo signaling via the FAK–Src–PI3K pathway. J Cell Biol 210: 503–515.
16. Kim NG, Koh E, Chen X, Gumbiner BM. 2011. E-cadherin mediates contact inhibition of proliferation through Hippo signaling- pathway components. Proc Natl Acad Sci 108: 11930–11935.
17. Klezovitch O, Vasioukhin V. 2015. Cadherin signaling: keeping cells in touch. F1000Res 4: 550.
18. Kobielak A, Fuchs E. 2006. Links between α-catenin, NF-κB, and squamous cell carcinoma in skin. Proc Natl Acad Sci 103: 2322–2327.
19. Komuro A, Nagai M, Navin NE, Sudol M. 2003.WWdomain-containing protein YAP associates with ErbB-4 and acts as a cotranscriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J Biol Chem 278: 33334–33341.
20. Kwon HJ, Waghmare I, Verghese S, Singh A, Singh A, Kango- Singh M. 2015. Drosophila C-terminal Src kinase regulates growth via the Hippo signaling pathway. Dev Biol 397: 67–76.
21. Lee JH, Pyon JK, Kim DW, Lee SH, Nam HS, Kim CH, Kang SG, Lee YJ, Park MY, Jeong DJ, et al. 2010. Elevated c-Src and c-Yes expression in malignant skin cancers. J Exp Clin Cancer Res 29: 116.
22. Levy D, Adamovich Y, Reuven N, Shaul Y. 2008. Yap1 phosphorylation by c-Abl is a critical step in selective activation of proapoptotic genes in response to DNA damage. Mol Cell 29: 350–361.
23. Li Z, Zhao B, Wang P, Chen F, Dong Z, Yang H, Guan KL, Xu Y. 2010. Structural insights into the YAP and TEAD complex. Genes Dev 24: 235–240.
24. Lien WH, Gelfand VI, Vasioukhin V. 2008a. αE-catenin binds to dynamitin and regulates dynactin-mediated intracellular traffic. J Cell Biol 183: 989–997.
25. Lien WH, Klezovitch O, Null M, Vasioukhin V. 2008b. αE-catenin is not a significant regulator of β-catenin signaling in the developing mammalian brain. J Cell Sci 121: 1357–1362.
26. Livshits G, Kobielak A, Fuchs E. 2012. Governing epidermal homeostasis by coupling cell–cell adhesion to integrin and growth factor signaling, proliferation, and apoptosis. Proc Natl Acad Sci 109: 4886–4891.
27. Matsumoto T, Jiang J, Kiguchi K, Ruffino L, Carbajal S, Beltran L, Bol DK, Rosenberg MP, DiGiovanni J. 2003. Targeted expression of c-Src in epidermal basal cells leads to enhanced skin tumor promotion, malignant progression, and metastasis. Cancer Res 63: 4819–4828.
28. McClatchey AI, Yap AS. 2012. Contact inhibition (of proliferation) redux. Curr Opin Cell Biol 24: 685–694.
29. Muthuswamy SK. 2011. Trastuzumab resistance: all roads lead to SRC. Nat Med 17: 416–418.
30. Nemade RV, Bierie B, Nozawa M, Bry C, Smith GH, Vasioukhin V, Fuchs E, Hennighausen L. 2004. Biogenesis and function of mouse mammary epithelium depends on the presence of functional α-catenin. Mech Dev 121: 91–99.
31. Pan D. 2010. The hippo signaling pathway in development and cancer. Dev Cell 19: 491–505.
32. Piao HL, Yuan Y, Wang M, Sun Y, Liang H, Ma L. 2014. α-Catenin acts as a tumour suppressor in E-cadherin-negative basal-like breast cancer by inhibiting NF-κB signalling. Nat Cell Biol 16: 245–254.
33. Pijuan-Galito S, Tamm C, Anneren C. 2014. Serum inter-α-inhibitor activates the Yes tyrosine kinase and YAP/TEAD transcriptional complex in mouse embryonic stem cells. J Biol Chem 289: 33492–33502.
34. Piwnica-Worms H, Saunders KB, Roberts TM, Smith AE, Cheng SH. 1987. Tyrosine phosphorylation regulates the biochemical and biological properties of pp60c-src. Cell 49: 75–82.
35. Qian X, Karpova T, Sheppard AM, McNally J, Lowy DR. 2004. Ecadherin- mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J 23: 1739–1748.
36. Rheinwald JG, Green H. 1975. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6: 331–343.
37. Rosenbluh J, Nijhawan D, Cox AG, Li X, Neal JT, Schafer EJ, Zack TI, Wang X, Tsherniak A, Schinzel AC, et al. 2012. β-Catenindriven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell 151: 1457–1473.
38. Roura S, Miravet S, Piedra J, Garcia de Herreros A, Dunach M. 1999. Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J Biol Chem 274: 36734–36740.
39. Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, et al. 2011. Yap1 acts downstream of α-catenin to control epidermal proliferation. Cell 144: 782–795.
40. Shanzer M, Ricardo-Lax I, Keshet R, Reuven N, Shaul Y. 2015. The polyomavirus middle T-antigen oncogene activates the Hippo pathway tumor suppressor Lats in a Src-dependent manner. Oncogene 34: 4190–4198.
41. Silvis MR, Kreger BT, Lien WH, Klezovitch O, Rudakova GM, Camargo FD, Lantz DM, Seykora JT, Vasioukhin V. 2011. α- Catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci Signal 4: ra33.
42. Stepniak E, Radice GL, Vasioukhin V. 2009. Adhesive and signaling functions of cadherins and catenins in vertebrate development. Cold Spring Harb Perspect Biol 1: a002949.
43. 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.
44. Sudol M. 2011. From Rous sarcoma virus to plasminogen activator, src oncogene and cancer management. Oncogene 30: 3003–3010.
45. Sudol M, Bork P, Einbond A, Kastury K, Druck T, Negrini M, Huebner K, Lehman D. 1995. Characterization of the mammalian YAP (Yes-associated protein) gene and its role in defining a novel protein module, theWWdomain. J Biol Chem 270: 14733–14741.
46. Tamm C, Bower N, Anneren C. 2011. Regulation of mouse embryonic stem cell self-renewal by a Yes–YAP–TEAD2 signaling pathway downstream of LIF. J Cell Sci 124: 1136–1144.
47. Taniguchi K, Wu LW, Grivennikov SI, de Jong PR, Lian I, Yu FX, Wang K, Ho SB, Boland BS, Chang JT, et al. 2015.Agp130–Src–YAP module links inflammation to epithelial regeneration. Nature 519: 57–62.
48. Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, Larsen BG, Rossant J, Wrana JL. 2010. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-β–SMAD pathway. Dev Cell 19: 831–844.
49. Vasioukhin V. 2012. Adherens junctions and cancer. Subcell Biochem 60: 379–414.
50. Vasioukhin V, Bauer C, Degenstein L, Wise B, Fuchs E. 2001. Hyperproliferation and defects in epithelial polarity upon conditional ablation of α-catenin in skin. Cell 104: 605–617.
51. Vermeer PD, Einwalter LA, Moninger TO, Rokhlina T, Kern JA, Zabner J, Welsh MJ. 2003. Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 422: 322–326.
52. Wang X, Zinkel S, Polonsky K, Fuchs E. 1997. Transgenic studies with a keratin promoter-driven growth hormone transgene: prospects for gene therapy. Proc Natl Acad Sci 94: 219–226.
53. Wu S, Liu Y, Zheng Y, Dong J, Pan D. 2008. The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev Cell 14: 388–398.
54. Yagi R, Chen LF, Shigesada K, Murakami Y, Ito Y. 1999. A WW domain-containing yes-associated protein (YAP) is a novel transcriptional co-activator. EMBO J 18: 2551–2562.
55. Yu FX, Guan KL. 2013. The Hippo pathway: regulators and regulations. Genes Dev 27: 355–371.
56. Zaidi SK, Sullivan AJ, Medina R, Ito Y, van Wijnen AJ, Stein JL, Lian JB, Stein GS. 2004. Tyrosine phosphorylation controls Runx2-mediated subnuclear targeting of YAP to repress transcription. EMBO J 23: 790–799.
57. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, 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.
58. Zhao B, Ye X, Yu J, Li L, Li W, Li S, Yu J, Lin JD, Wang CY, Chinnaiyan AM, et al. 2008. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 22: 1962–1971.