p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions

Journal of Cell Biology

Volumn 163, Issue 3, 2003, Pages 547-557

  Chen, Xinyu ^a   Kojima, Shin Ichiro ^a   Borisy, Gary G ^a   Green, Kathleen J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Adherens junction; Armadillo; Microtubule; N cadherin; Trafficking

Indexed keywords

CADHERIN; CALCIUM; CATENIN; GUANOSINE TRIPHOSPHATASE; KINESIN; NERVE CELL ADHESION MOLECULE; PROTEIN P120; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL ADHESION; CELL JUNCTION; CELL VACUOLE; COMPLEX FORMATION; ENZYME ACTIVITY; GENE DELETION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MEMBRANE TRANSPORT; MICROTUBULE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

ADHERENS JUNCTIONS; CADHERINS; CALCIUM SIGNALING; CELL ADHESION; CELL ADHESION MOLECULES; CELL LINE; HUMANS; KINESIN; MACROMOLECULAR SUBSTANCES; MICROTUBULES; MUTATION; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; TRANSPORT VESICLES;

ARMADILLO;

EID: 0242456020     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200305137     Document Type: Article

References (49)

1. Aberle, H., S. Butz, J. Stappert, H. Weissig, R. Kemler, and H. Hoschuetzky. 1994. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J. Cell Sci. 107:3655-3663.
2. Anastasiadis, P.Z., and A.B. Reynolds. 2000. The p120 catenin family: complex roles in adhesion, signaling and cancer. J. Cell Sci. 113:1319-1334.
3. Anastasiadis, P.Z., S.Y. Moon, M.A. Thoreson, D.J. Mariner, H.C. Crawford, Y. Zheng, and A.B. Reynolds. 2000. Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2:637-644.
4. Aono, S., S. Nakagawa, A.B. Reynolds, and M. Takeichi. 1999. p120(ctn) acts as an inhibitory regulator of cadherin function in colon carcinoma cells. J. Cell Biol. 145:551-562.
5. Brieher, W.M., and B.M. Gumbiner. 1994. Regulation of C-cadherin function during activin induced morphogenesis of Xenopus animal caps. J. Cell Biol. 126:519-527.
6. Bronner-Fraser, M. 1993. Mechanisms of neural crest cell migration. Bioessays. 15:221-230.
7. Chen, X., S. Bonne, M. Hatzfeld, F. van Roy, and K.J. Green. 2002. Protein binding and functional characterization of plakophilin 2. Evidence for its diverse roles in desmosomes and β-catenin signaling. J. Biol. Chem. 277:10512-10522.
8. 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 α-catenin. Mol. Cell. Biol. 15:4819-4824.
9. Daniel, J.M., and A.B. Reynolds. 1997. Tyrosine phosphorylation and cadherin/catenin function. Bioessays. 19:883-891.
10. Diefenbach, R.J., J.P. Mackay, P.J. Armati, and A.L. Cunningham. 1998. The C-terminal region of the stalk domain of ubiquitous human kinesin heavy chain contains the binding site for kinesin light chain. Biochemistry. 37:16663-16670.
11. Downing, J.R., and A.B. Reynolds. 1991. PDGF, CSF-1, and EGF induce tyrosine phosphorylation of p120, a pp60src transformation-associated substrate. Oncogene. 6:607-613.
12. Grosheva, I., M. Shtutman, M. Elbaum, and A.D. Bershadsky. 2001. p120 catenin affects cell motility via modulation of activity of Rho-family GTPases: a link between cell-cell contact formation and regulation of cell locomotion. J. Cell Sci. 114:695-707.
13. Gumbiner, B.M. 1996. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 84:345-357.
14. Gumbiner, B.M. 2000. Regulation of cadherin adhesive activity. J. Cell Biol. 148:399-404.
15. Hinck, L., I.S. Nathke, 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.
16. Hulsken, J., W. Birchmeier, and J. Behrens. 1994. E-cadherin and APC compete for the interaction with β-catenin and the cytoskeleton. J. Cell Biol. 127:2061-2069.
17. Ireton, R.C., M.A. Davis, J. van Hengel, D.J. Mariner, K. Barnes, M.A. Thoreson, P.Z. Anastasiadis, L.M. Bundy, L. Sealy, et al. 2002. A novel role for p120 catenin in E-cadherin function. J. Cell Biol. 159:465-476.
18. Jou, T.S., 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.
19. Kanner, S.B., A.B. Reynolds, and J.T. Parsons. 1991. Tyrosine phosphorylation of a 120-kilodalton pp60src substrate upon epidermal growth factor and platelet-derived growth factor receptor stimulation and in polyomavirus middle-T-antigen-transformed cells. Mol. Cell. Biol. 11:713-720.
20. Karcher, R.L., S.W. Deacon, and V.I. Gelfand. 2002. Motor-cargo interactions: the key to transport specificity. Trends Cell Biol. 12:21-27.
21. Kartenbeck, J., E. Schmid, W.W. Franke, and B. Geiger. 1982. Different modes of internalization of proteins associated with adhaerens junctions and desmosomes: experimental separation of lateral contacts induces endocytosis of desmosomal plaque material. EMBO J. 1:725-732.
22. 2+ ion medium. J. Cell Biol. 113:881-892.
23. Le, T.L., A.S. Yap, and J.L. Stow. 1999. Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146:219-232.
24. Ligon, L.A., S. Karki, M. Tokito, and E.L. Holzbaur. 2001. Dynein binds to β-catenin and may tether microtubules at adherens junctions. Nat. Cell Biol. 3:913-917.
25. Mariner, D.J., 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. Mary, S., S. Charrasse, M. Meriane, F. Comunale, P. Travo, A. Blangy, and C. Gauthier-Rouviere. 2002. Biogenesis of N-cadherin-dependent cell-cell contacts in living fibroblasts is a microtubule-dependent kinesin-driven mechanism. Mol. Biol. Cell. 13:285-301.
27. Monier-Gavelle, F., and J.L. Duband. 1995. Control of N-cadherin-mediated intercellular adhesion in migrating neural crest cells in vitro. J. Cell Sci. 108:3839-3853.
28. Monier-Gavelle, F., and J.L. Duband. 1997. Cross talk between adhesion molecules: control of N-cadherin activity by intracellular signals elicited by β1 and β3 integrins in migrating neural crest cells. J. Cell Biol. 137:1663-1681.
29. Myster, S.H., R. Cavallo, C.T. Anderson, D.T. Fox, and M. Peifer. 2003. Drosophila p120catenin plays a supporting role in cell adhesion but is not an essential adherens junction component. J. Cell Biol. 160:433-449.
30. Nollet, F., G. Berx, and F. van Roy. 1999. The role of the E-cadherin/catenin adhesion complex in the development and progression of cancer. Mol. Cell Biol. Res. Commun. 2:77-85.
31. Noren, N.K., B.P. Liu, K. Burridge, and B. Kreft. 2000. p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J. Cell Biol. 150:567-580.
32. Pacquelet, A., L. Lin, and P. Rorth. 2003. Binding site for p120/δ-catenin is not required for Drosophila E-cadherin function in vivo. J. Cell Biol. 160:313-319.
33. Palacios, F., J.K. Schweitzer, R.L. Boshans, and C. D'Souza-Schorey. 2002. ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat. Cell Biol. 4:929-936.
34. Palka, H.L., and K.J. Green. 1997. Roles of plakoglobin end domains in desmosome assembly. J. Cell Sci. 110:2359-2371.
35. 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.
36. Pettitt, J., E.A. Cox, I.D. Broadbent, A. Flett, and J. Hardin. 2003. The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis. J. Cell Biol. 162:15-22.
37. Reynolds, A.B., L. Herbert, J.L. Cleveland, S.T. Berg, and J.R. Gaut. 1992. p 120, a novel substrate of protein tyrosine kinase receptors and of p60v-src, is related to cadherin-binding factors β-catenin, plakoglobin and armadillo. Oncogene. 7:2439-2445.
38. Reynolds, A.B., J.M. Daniel, Y.Y. Mo, J. Wu, and Z. Zhang. 1996. The novel catenin p120cas binds classical cadherins and induces an unusual morphological phenotype in NIH3T3 fibroblasts. Exp. Cell Res. 225:328-337.
39. Stappenbeck, T.S., and K.J. Green. 1992. The desmoplakin carboxyl terminus coaligns with and specifically disrupts intermediate filament networks when expressed in cultured cells. J. Cell Biol. 116:1197-1209.
40. Takeichi, M. 1995. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7:619-627.
41. Thoreson, M.A., and A.B. Reynolds. 2002. Altered expression of the catenin p 120 in human cancer: implications for tumor progression. Differentiation. 70:583-589.
42. 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.
43. Vale, R.D., and R.J. Fletterick. 1997. The design plan of kinesin motors. Annu. Rev. Cell Dev. Biol. 13:745-777.
44. Verhey, K.J., D.L. Lizotte, T. Abramson, L. Barenboim, B.J. Schnapp, and T.A. Rapoport. 1998. Light chain-dependent regulation of kinesin's interaction with microtubules. J. Cell Biol. 143:1053-1066.
45. Verhey, K.J., D. Meyer, R. Deehan, J. Blenis, B.J. Schnapp, T.A. Rapoport, and B. Margolis. 2001. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 152:959-970.
46. Wahl, J.K., III, Y.J. Kim, J.M. Cullen, K.R. Johnson, and M.J. Wheelock. 2003. N-cadherin-catenin complexes form prior to cleavage of the proregion and transport to the plasma membrane. J. Biol. Chem. 278:17269-17276.
47. Wilson, A.J., and P.R. Gibson. 1997. Epithelial migration in the colon: filling in the gaps. Clin. Sci. (Lond.). 93:97-108.
48. Yap, A.S. 1998. The morphogenetic role of cadherin cell adhesion molecules in human cancer: a thematic review. Cancer Invest. 16:252-261.
49. Yap, A.S., C.M. Niessen, and B.M. Gumbinet. 1998. The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120ctn. J. Cell Biol. 141:779-789.