p120 catenin-associated Fer and Fyn tyrosine kinases regulate β-catenin Tyr-142 phosphorylation and β-catenin-α-catenin interaction

Molecular and Cellular Biology

Volumn 23, Issue 7, 2003, Pages 2287-2297

  Piedra, Jose ^a,b   Miravet, Susana ^a   Castaño, Julio ^a   Pálmer, Héctor G ^c   Heisterkamp, Nora ^d   De Herreros, Antonio García ^b,e   Duñach, Mireia ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e INST MUNIC D INVESTIGACIO MEDICA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CATENIN; BETA CATENIN; DOCKING PROTEIN; FER PROTEIN TYROSINE KINASE; PROTEIN KINASE FYN; PROTEIN P120; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; CELL JUNCTION; ENZYME ACTIVATION; EPITHELIUM CELL; INTESTINE EPITHELIUM CELL; MOLECULAR CLONING; NONHUMAN; ONCOGENE K RAS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ALPHA CATENIN; ANIMALS; BETA CATENIN; CELL ADHESION MOLECULES; CELL LINE; CLONE CELLS; CYTOSKELETAL PROTEINS; EPITHELIAL CELLS; GENES, RAS; HUMANS; PHOSPHOPROTEINS; PHOSPHORYLATION; PRECIPITIN TESTS; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FYN; PROTO-ONCOGENE PROTEINS C-YES; RATS; SRC-FAMILY KINASES; TRANS-ACTIVATORS; TRANSFECTION;

EID: 0037378505     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.7.2287-2297.2003     Document Type: Article

References (48)

1. Aberle, H., S. Butz, J. Stappert, H. Weisseig, R. Kemler, and H. Hoschuetzky. 1994. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J. Cell Sci. 107:3655-3663.
2. Aberle, H., H. Schwartz, H. Hoschuetzky, and R. Kemler. 1996. Single amino acid substitutions in proteins of the armadillo gene family abolish their binding to α-catenin. J. Biol. Chem. 271:1520-1526.
3. Adams, C., and J. W. Nelson. 1998. Cytomechanics of cadherin-mediated cell-cell adhesion. Curr. Opin. Cell Biol. 10:572-577.
4. Anastasiadis, P. Z., and A. B. Reynolds. 2000. The p120 catenin family: complex roles in adhesion, signalling and cancer. J. Cell Sci. 113:1319-1334.
5. Aono, S., S. Nagakawa, A. B. Reynolds, and M. Takeichi. 1999. p120ctn acts as an inhibitory regulator of cadherin function in colon carcinoma cells. J. Cell Biol. 145:551-562.
6. Behrens, J., L. Vakaet, R. Friis, E. Winterhager, F. Van Roy, M. Mareel, 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.
7. Bonvini, P., W. G. An, A. Rosolen, P. Nguyen, J. Trepel, A. García de Herreros, M. Duñach, and L. M. Neckers. 2001. Geldanamycin abrogates erbB2 association with proteasome-resistant β-catenin in melanoma cells, increases β-catenin-E-cadherin association, and decreases β-catenin-sensitive transcription. Cancer Res. 61:1671-1677.
8. Calautti, E., S. Cabodi, P. Stein, M. Hatzfeld, N. Kedersha, and P. Dotto. 1998. Tyrosine phosphorylation and Src family kinases control keratinocyte cell-cell adhesion. J. Cell Biol. 141:1449-1465.
9. Calautti, E., M. Grossi, C. Mammucari, Y. Aoyama, M. Pirro, Y. Ono, J. Li, and P. Dotto. 2002. Fyn tyrosine kinase is a downstream mediator of Rho/ PRK2 function in keratinocyte cell-cell adhesion. J. Cell Biol. 156:137-148.
10. Craig, A., R. Zirngibl, K. Williams, L. Cole, and P. Greer. 2001. Mice devoid of Fer protein-tyrosine kinase activity are viable and fertile but display reduced cortactin phosphorylation. Mol. Cell. Biol. 21:603-613.
11. Daniel, J. M., and A. B. Reynolds. 1995. The tyrosine kinase substrate p120cas binds directly to E-cadherin but not to the adenomatous polyposis coli protein or alpha-catenin. Mol. Cell. Biol. 110:345-356.
12. Daniel, J. M., and A. B. Reynolds. 1997. Tyrosine phosphorylation and cadherin/catenin function. Bioessays 19:883-891.
13. Giannini, A., M. M. Vivanco, and R. M. Kypta. 2000. α-catenin inhibits β-catenin signaling by preventing formation of a β-catenin-T-cell factor DNA complex. J. Biol. Chem. 275:21883-21888.
14. Gumbiner, B. M. 2000. Regulation of cadherin adhesive activity. J. Cell Biol. 148:399-404.
15. 2+ during intestinal epithelial cell migration. Am. J. Physiol. Cell Physiol. 283:C722-C734.
16. Hazan, R. B., and L. Norton. 1998. The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton. J. Biol. Chem. 273:9078-9084.
17. Hoschuetzky, H., H. Aberle, and R. Kemler. 1994. β-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127:1375-1380.
18. Hu, P., E. J. O'Keefe, and D. S. Rubinstein. 2001. Tyrosine phosphorylation of human keratinocyte β-catenin and plakoglobin reversibly regulates their binding to E-cadherin and α-catenin. J. Invest. Dermatol. 117:1059-1067.
19. Huber, A., and W. Weis. 2001. The structure of β-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by β-catenin. Cell 105:391-402.
20. Kapus, A., C. Di Ciano, J. Sun, X. Zhan, L. Kim, T. W. Wong, and O. D. Rotstein. 2000. Cell volume-dependent phosphorylation of proteins of the cortical cytoskeleton and cell-cell contact sites. J. Biol. Chem. 275:32289-32298.
21. Kim, L., and T. W. Wong. 1995. The cytoplasmic tyrosine kinase FER is associated with the catenin-like substrate pp120 and is activated by growth factors. Mol. Cell. Biol. 15:4553-4561.
22. Kinch, M. S., G. J. Clark, J. D. Channing, and K. Burridge. 1995. Tyrosine phosphorylation regulates the adhesions of ras-transformed breast epithelia. J. Cell Biol. 130:461-471.
23. Lilien, J., J. Balsamo, C. Arregui, and G. Xu. 2002. Turn-off, drop-out. Functional state switching of cadherins. Dev. Dyn. 224:8-29.
24. Magie, C. R., D. Pinto-Santini, and S. M. Parkhurst. 2002. Rho1 interacts with p120ctn and a-catenin, and regulates cadherin-based adherens junction components in Drosophila. Development 129:3771-3782.
25. Mariner, D., P. Anastasiadis, H. Keilhack, F. D. Bohmer, J. Wang, and A. B. Reynolds. 2001. Identification of Src phosphorylation sites in the catenin p120ctn. J. Biol. Chem. 276:28006-28013.
26. Matsuyoshi, N., M. Hamaguchi, S. Taniguchi, A. Nagafuchi, S. Tsukita, and M. Takeichi. 1992. Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts. J. Cell Biol. 118:703-714.
27. Müller, T., A. Choidas, E. Reichmann, and A. Ullrich. 1999. Phosphorylation and free pool of β-catenin are regulated by tyrosine kinases and tyrosine phosphatases during epithelial cell migration. J. Biol. Chem. 274:10173-10183.
28. Nagafuchi, A. 2001. Molecular architecture of adherens junctions. Curr. Opin. Cell Biol. 13:600-603.
29. Ohkubo, T., and M. Ozawa. 1999. p120ctn binds to the membrane-proximal region of the E-cadherin cytoplasmic domain and is involved in modulation of adhesion activity. J. Biol. Chem. 274:21409-21415.
30. Orsulic, S., O. Huber, H. Aberle, S. Arnold, and R. Kemler. 1999. E-cadherin binding prevents β-catenin nuclear localization and β-catenin/LEF-1-mediated transactivation. J. Cell Sci. 112:1237-1245.
31. Owens, D. W., G. W. McLean, A. W. Wyke, C. Paraskeva, E. K. Parkinson, M. C. Frame, and V. G. Brunton. 2000. The catalytic activity of the Src family kinases is required to disrupt cadherin-dependent cell-cell contacts. Mol. Biol. Cell 11:1-64.
32. Ozawa, M., and R. Kemler. 1998a. Altered cell adhesion activity by pervanadate due to the dissociation of alpha-catenin from the E-cadherin-catenin complex. J. Biol. Chem. 273:6166-6170.
33. Ozawa, M., and R. Kemler. 1998b. The membrane-proximal region of the E-cadherin cytoplasmic domain prevents dimerization and negatively regulates adhesion activity. J. Cell Biol. 142:1605-1613.
34. Piedra, J., D. Martínez, J. Castaño, S. Miravet, M. Duñach, and A. García de Herreros. 2001. Regulation of β-catenin structure and activity by tyrosine phosphorylation. J. Biol. Chem. 276:20436-20443.
35. Pokutta, S., and W. Weis. 2000. Structure of the dimerization and β-catenin-binding region of α-catenin. Mol. Cell 5:533-543.
36. Provost, E., and D. L. Rimm. 1999. Controversies at the cytoplasmic face of the cadherin-based adhesion complex. Curr. Opin. Cell Biol. 11:567-572.
37. cas associates with cadherin complexes. Mol. Cell. Biol. 14:8333-8342.
38. Rosato, R., J. Veltmaat, J. Groffen, and N. Heisterkamp. 1998. Involvement of the tyrosine kinase Fer in cell adhesion. Mol. Cell. Biol. 18:5762-5770.
39. Roura, S., S. Miravet, J. Piedra, A. Garcia de Herreros, and M. Duñach. 1999. Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J. Biol. Chem. 274:36734-36740.
40. Sadot, E., I. Simcha, M. Shtuman, A. Ben-Ze'ev, and B. Geiger. 1998. Inhibition of β-catenin-mediated transactivation by E-cadherin derivatives. Proc. Natl. Acad. Sci. USA 95:15339-15344.
41. Shibamoto, S., M. Hayakawara, K. Takeuchi, T. Hori, N. Oku, K. Miyazawa, N. Kimamura, M. Takeichi, and F. Ito. 1994. Tyrosine phosphorylation of beta-catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells. Cell Adhes. Commun. 1:295-305.
42. Shibata, T., A. Ochiai, Y. Kanai, S. Akimoto, M. Gotoh, N. Yasui, R. Machinami, and S. Hirohashi. 1996. Dominant negative inhibition of the association between β-catenin and c-erbB2 by N-terminally deleted β-calenin suppresses the invasion and metastasis of cancer cells. Oncogene 13: 883-889.
43. Skoudy, A., M. M. Llosas, and A. Garcia de Herreros. 1996. Intestinal HT-29 cells with dysfunction of E-cadherin show increased pp60src activity and tyrosine phosphorylation of p120-catenin. Biochem. J. 317:279-284.
44. Stein, P. L., H. M. Lee, S. Rich, and P. Soriano. 1992. pp59fyn mutant mice display differential signaling in thymocytes and peripheral T cells. Cell 70: 741-750.
45. Taddei, M. L., P. Chiarugi, P. Cirri, F. Buricchi, T. Fiaschi, E. Giannoni, D. Talini, G. Cozzi, L. Formigli, G. Raugel, and G. Ramponi. 2002. β-catenin interacts with low-molecular-weight protein tyrosine phosphates leading to cadherin-mediated cell-cell adhesion. Cancer Res. 62:6489-6499.
46. Thomas, S. M., and J. S. Brugge. 1997. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 13:513-609.
47. Thoreson, M. A., P. Z. Anastasiadis, J. M. Daniel, R. C. Ireton, M. J. Wheelock, K. R. Johnson, D. K. Hummingbird, and A. B. Reynolds. 2000. Selective uncoupling of p120(ctn) from E-cadherin disrupts strong adhesion. J. Cell Biol. 148:189-202.
48. Yap, A. S., C. M. Niessen, and B. M. Gumbiner. 1998. The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120ctn. J. Cell Biol. 141:779-789.