H-Ras activation promotes cytoplasmic accumulation and phosphoinositide 3-OH kinase association of β-catenin in epidermal keratinocytes

Journal of Cell Biology

Volumn 146, Issue 5, 1999, Pages 967-980

  Espada, Jesús ^a   Perez Moreno, Mirna ^a   Braga, Vania M M ^b   Rodriguez Viciana, Pablo ^c   Cano, Amparo ^a,d  

^a CSIC   (Spain)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

Adenomatous polyposis coli; E cadherin; H Ras; Phosphoinositide 3 OH kinase; catenin

Indexed keywords

BETA CATENIN; PHOSPHATIDYLINOSITOL 3 KINASE; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL TRANSFORMATION; COLON CARCINOGENESIS; COLON CARCINOMA; COLON POLYPOSIS; CONTROLLED STUDY; EPIDERMIS CELL; KERATINOCYTE; MOUSE; NONHUMAN; ONCOGENE H RAS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SKIN CARCINOGENESIS; SKIN CARCINOMA;

ANIMALIA;

EID: 0032847443     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.146.5.967     Document Type: Article

References (73)

1. Aberle. H., H. Schwartz, and R. Kemler. 1996. Cadherin-catenin complexes: protein interactions and their implications for cadherin function. J. Cell. Biochem. 61:514-523.
2. Aberle, H., A. Bauer, J. Stappert, A. Kispert, and R. Kemler. 1997. β-catenin is a target for the ubiquitin-proteasome pathway. EMBO (Ear. Mol. Biol. Organ.) J. 6:3797-3804.
3. Barbacid, M. 1987. ras genes. Annu. Rev. Biochem. 56:779-827.
4. Behrens. J., M.M. Mareel, P.M. Van Roy, and W. Birchmeier. 1989. Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion. J. Cell Biol. 108:2435-2447.
5. Behrens, J., L. Vakaet, R. Früs, E. Winterhager, F. Van Roy, and W. Birchmeier. 1993. Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/β-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J. Cell Biol. 120: 757-766.
6. Behrens. J., J.P. Vonkries, M. Kuhl, L. Bruhn, D. Wedlich, R. Grosschedl, and W. Birchmeier. 1996. Functional interaction of β-catenin with the transcription factor Lef-1. Nature. 382:638-642.
7. Bianchi, A.B., C.M. Aldaz, and C.J. Conti. 1990. Nonrandom duplication of the chromosome bearing a mutated Ha-ras-1 allele in mouse skin tumors. Proc. Natl. Acad. Sci. USA. 87:6902-6906.
8. Birchmeier, W., and J. Behrens. 1994. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim. Biophys. Acta. 1198:11-26.
9. Boyle, W.J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two dimensional separation on thin layer cellulose plates. Methods Enzymol. 201:110-148.
10. Braga, V.M.M., K.J. Hodivala, and F.M. Watt. 1995. Calcium-induced changes in distribution and solubility of cadherins and their associated cytoplasmic proteins in human keratinocytes. Cell Adhes. Commun. 3:201-215.
11. Braga, V.M.M., L.M. Machesky, A. Hall, and N.A. Hotchin. 1997. The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J. Cell Biol. 137:1421-1431.
12. Braga, V.M.M., A. Del Maschio, L. Machesky, and E. Dejana. 1999. Regulation of cadherin function by Rho and Rac: modulation by junction modulation and cellular context. Mol. Biol. Cell. 10:9-22.
13. Bremner, R., and A. Balmain. 1990. Genetic changes in skin tumor progression: correlation between presence of a mutant ras gene and loss of heterozygosity on mouse chromosome 7. Cell. 61:407-417.
14. Brown, K., M. Ouintanilla, M. Ramsden, I.B. Kerr, S. Young, and A. Balmain. 1986. v-ras genes from Harvey and BALB murine sarcoma virus can act as initiators of two-stage mouse skin carcinogenesis. Cell. 46:447-456.
15. Calautti, E., S. Cabodi, P.L. Stein, M. Hatzfeld, N. Kedersha, and G.P. Dotto. 1998. Tyrosine phosphorylation and Src family kinases control keratinocyte cell-cell adhesion. J. Cell Biol. 141:1449-1465.
16. 4 integrin is altered in pre-malignant skin tumors of p53-deficient mice. Int. J. Cancer. 65:254-262.
17. Cook, D., M.J. Fry, K. Hughes, R. Sumathipala, J.R. Woodgett, and T.C. Dale. 1996. Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C. EMBO (Eur. Mol. Biol. Organ.) J. 15:4526-4536.
18. Daniel, J.M., and A.B. Reynolds. 1995. The tyrosine kinase substrate p120cas binds directly to E-cadherin but not to adenomatous polyposis coli protein or α-catenin. Mol. Cell. Biol. 15:4819-4824.
19. Delcommenne, M., C. Tan, V. Gray, L. Rue, J. Woodgett, and S. Dedhar. 1998. Phosphoinositide-3-OH kinase-dependent regulation of glycogen kinase 3 and protein kinase B/AKT by the integrin-linked kinase. Proc. Acad. Sci. USA. 95:11211-11216.
20. Duclos. B., S. Marcandier, and A.J. Cozzone. 1991. Chemical properties and separation of phosphoamino acids by thin-layer Chromatography and/or electrophoresis. Methods Enzymol. 201:10-21.
21. Fagotto, F., U. Glück, and B.M. Gumbiner. 1998. Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of β-catenin. Curr. Biol. 8:181-190.
22. Gumbiner, B.M. 1995. Signal lransduction by β-catenin. Curr. Opin. Cell Biol. 7:634-640.
23. Gumbiner, B.M. 1996. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 84:345-357.
24. Hinck, L., I.S. Näthke, J. Papkoff, and W.J. Nelson. 1994. Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly. J. Cell Biol. 125:1327-1340.
25. Huber, O., R. Korn, J. McLaughlin, M. Ohsugi, E.G. Herrmann, and R. Kemler. 1996. Nuclear localization of β-catenin by interaction with transcription factor LEF-1. Mech. Dev. 59:3-10.
26. Ikeda, S., S. Kishida, H. Yamamoto, H. Murai, S. Koyama, and A. Kikuchi. 1998. Axin, a negative regulator of the Wnt signalling pathway, forms a complex with GSK-3β and β-catenin and promotes GSK-3β-dependent phosphorylation of β-catenin. EMBO (Ear. Mol. Biol. Organ.) J. 17:1371-1384.
27. Jou, T., D.B. Stewart, J. Stappert, W.J. Nelson, and J.A. Marrs. 1995. Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex. Proc. Natl. Acad. Sci. USA. 92:5067-5071.
28. Kemler, R. 1993. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 9:317-321.
29. Kinch, M.S., G.J. Clark, C.J. Der, and K. Burridge. 1995. Tyrosine phosphorylation regulates the adhesion of Ras-transformed breast epithelia. J. Cell Biol. 130:461-471.
30. Knudsen, K.A., A. Peralta Soler, K.R. Johnson, and M.J. Wheelock. 1995. Interaction of α-actinin with the E-cadherin/catenin cell-cell adhesion complex via α-catenin. J. Cell Biol. 130:67-77.
31. -/- colon carcinoma. Science. 275:1784-1787.
32. Lozano, E., and A. Cano. 1998. Cadherin/catenin complexes in murine epidermal keratinocytes: E-cadherin complexes containing either β-catenin or plakoglobin contribute to stable cell-cell contacts. Cell Adh. Commun. 6:51-67.
33. Miller, J.R., and R.T. Moon. 1996. Signal transduction through β-catenin and specification of cell fate during embryogenesis. Genes Dev. 10:2527-2539.
34. Missero, C., S. Ramón y Cajal, and G.P. Dotto. 1991. Escape from transforming growth factor β control and oncogene cooperation in skin tumor development. Proc. Natl. Acad. Sci. USA. 88:9613-9617.
35. Miyoshi, Y., K. Iwao, Y. Nagasawa, T. Aihara, Y. Sasaki, S. Imaoka, M. Murata, T. Shimano, and Y. Nakamura. 1998. Activation of the β-catenin gene in primary hepatocellular carcinomas by somatic alterations involving exon 3. Cancer Res. 58:2524-2527.
36. Molenaar, M., M. van de Wetering, M. Oosterwegel, J. Paterson-Maduro, S. Godsave, V. Korinek, J. Roose, O. Destrée, and H. Clevers. 1996. XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell. 86:391-399.
37. Morin, P.J., A.B. Sparks, V. Korinek, N. Barker, H. Clevers, B. Vogelstein, and K.W. Kinzler. 1997. Activation of β-catenin-Tcf signalling in colon cancer by mutations in β-catenin or APC. Science. 275:1787-1790.
38. Munemitsu, S., I. Albert, A. Souza, B. Rubinfeld, and P. Polakis. 1995. Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. USA. 92:3046-3050.
39. Nagafuchi, A., S. Ishihara, and S. Tsukita. 1994. The roles of catenins in the cadherin-mediated cell adhesion: functional analysis of E-cadherin-α-catenin fusion molecules. J. Cell Biol. 127:235-245.
40. Navarro, P., M. Gómez, A. Pizarro, C. Gamallo, M. Quintanilla, and A. Cano. 1991. A role for the E-cadherin cell-cell adhesion molecule in tumor progression of mouse epidermal carcinogenesis. J. Cell Biol. 115:517-533.
41. Novak, A., S. Hsu, C. Leung-Hagesteijn, G. Radeva, J. Papkoff, R. Montesano, C. Roskelley, R. Grosschedl, and S. Dedhar. 1998. Cell adhesion and the integrin-linked kinase regulate the LEF-1 and β-catenin signalling pathways. Proc. Natl. Acad. Sci. USA. 95:4374-4379.
42. Orford, K., C. Crockett, J.P. Jensen, A.M. Weissman, and S.W. Byers. 1997. Serine phosphorylation-regulated ubiquitination and degradation of β-catenin. J. Biol. Chem. 272:24735-24738.
43. Orsulic, S., and M. Peifer. 1996. An in vivo structure-function study of armadillo, the β-catenin homologue, reveals both separate and overlapping regions of the protein required for cell adhesion and for Wingless signalling. J. Cell Biol. 134:1283-1300.
44. Palacios, J., and C. Gamallo. 1998. Mutations in the β-catenin gene (CTNNB1) in endometrioid ovarian carcinomas. Cancer Res. 58:1344-1347.
45. Papkoff, J., B. Rubinfeld, B. Schryver, and P. Polakis. 1996. Wnt-1 regulates free pools of catenins and stabilizes APC-catenin complexes. Mol. Cell. Biol. 16:2128-2134.
46. Peifer, M., P. McCrea, K.J. Green, E. Wieschaus, and B.M. Gumbiner. 1992. The vertebrate adhesive junction proteins β-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J. Cell Biol. 118:681-691.
47. Peifer, M., S. Berg, and A.B. Reynolds. 1994. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell. 76:789-791.
48. Peifer, M. 1997. β-catenin as oncogene: the smoking gun. Science. 275:1752-1753.
49. Pennisi, E. 1998. How a growth control path takes a wrong turn to cancer. Science. 281:1438-1441.
50. Pérez-Moreno, M., A. Avila, S. Islas, S. Sánchez, and L. González-Mariscal. 1998. Vinculin but not α-actinin is a target of PKC phosphorylation during junctional assembly induced by calcium. J. Cell Sci. 111:3563-3571.
51. Perl, A.K., P. Wilgenbus, U. Dahl, H. Semb, and G. Christofori. 1998. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature. 392:190-193.
52. Potempa, S., and A.J. Ridley. 1998. Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/ scatter factor-induced adherens junction disassembly. Mol. Biol. Cell. 9:2185-2200.
53. Prieve, M.G., and M.L. Waterman. 1999. Nuclear localization and formation of β-catenin-Lymphoid Enhancer Factor 1 complexes are not sufficient for activation of gene expression. Mol. Cell. Biol. 19:4503-4515.
54. Quintanilla, M., K. Brown, M. Ramsden, and A. Balmain 1986. Carcinogen-specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature. 322:78-80.
55. Reynolds, A.B., J. Daniel, P.D. McCrea, M.J. Wheelock, J. Wu, and Z. Zhang. 1994. Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol. Cell. Biol. 14:8333-8342.
56. Ridley, A.J., H.F. Paterson, C.L. Johnston, D. Dickman, and A. Hall. 1992. The small GTP-binding protein Rac regulates growth factor-induced membrane ruffling. Cell. 70:401-410.
57. Rimm, D.L., E.R. Koslov, P. Kebriaei, C.D. Cianci, and J.S. Morrow. 1995. γ1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc. Natl. Acad. Sci. USA. 92:8813-8817.
58. Rodríguez-Viciana, P., P.H. Warne, A. Khwaja, B.M. Marte, D. Pappin, P. Das, M.D. Waterfield, A. Ridley, and J. Downward. 1997. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell. 89:457-467.
59. Rubinfeld, B., I. Albert, E. Porfiri, C. Fiol, S. Munemitsu, and P. Polakis. 1996. Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science. 272:1023-1026.
60. Rubinfeld, B., P. Robbins, M. El-Gamil, I. Albert, E. Porfiri, and P. Polakis. 1997. Stabilization of β-catenin by genetic defects in melanoma cell lines. Science. 275:1790-1792.
61. Ryves, W.J., L. Fryer, T. Dale, and A.J. Harwood. 1998. An assay for glycogen synthase kinase 3 (GSK-3) for use in crude cell extracts. Anal. Biochem. 264: 124-127.
62. Sakanaka, C., J.B. Weiss, and L.T. Williams. 1998. Bridging of β-catenin and glycogen synthase kinase-3β by axin and inhibition of β-catenin-mediated transcription. Proc. Natl. Acad. Sci. USA. 95:3020-3023.
63. Sánchez-Prieto, R., J.A. Vargas, A. Carnero, E. Marchetti, J. Romero, A. Durantez, J.L. Lacal, and S. Ramón y Cajal. 1995. Modulation of cellular chemoresistance in keratinocytes by activation of different oncogenes. Int. J. Cancer. 60:235-243.
64. Sander, E.E., S. van Delft, J.P. ten Klooster, T. Reid, R.A. van der Kammen, F. Michiels, and J.G. Collard. 1998. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 143:1385-1398.
65. Seeling, J.M., J.R. Miller, R. Gil, R.T. Moon, R. White, and D.M. Virshup. 1999. Regulation of β-catenin signaling by the B56 subunit of protein phosphatase 2A. Science. 283:2089-2091.
66. Takeichi, M. 1991. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 251:1451-1455.
67. Takeichi, M. 1993. Cadherins in cancer: implications for invasion and metastasis. Curr. Opin. Cell Biol. 5:806-811.
68. Vleminckx, K., L. Vakaet, Jr., M.M. Mareel, W. Fiers, and F. Van Roy. 1991. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell. 66:107-119.
69. Voeller, H.J., C.I. Truica, and E.P. Gelmann. 1998. β-catenin mutations in human prostate cancer. Cancer Res. 58:2520-2523.
70. Willert, K., and R. Nusse. 1998. β-catenin: a key mediator of Wnt signalling. Curr. Opin. Gen. Dev. 8:95-102.
71. Yost, C., M. Torres, J.R. Miller, E. Huang, D. Kimelman, and R.T. Moon. 1996. The axis-inducing activity, stability and subcellular distribution of β-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev. 10:1443-1454.
72. Yuspa, S.H., P. Hanley-Relson, B. Koehler, and J.P. Stanley. 1980. A survey of differentiation markers in differentiation cell lines in culture. Cancer Res. 40: 4694-4703.
73. Zhong, C., M.S. Kinch, and K. Burridge. 1997. Rho-stimulated contractility contributes to the fibroblastic phenotype of Ras-transformed epithelial cells. Mol. Biol. Cell. 8:2329-2344.