Dynamic and Static Interactions between p120 Catenin and E-Cadherin Regulate the Stability of Cell-Cell Adhesion

Cell

Volumn 141, Issue 1, 2010, Pages 117-128

  Ishiyama, Noboru ^a   Lee, Seung Hye ^c   Liu, Shuang ^a   Li, Guang Yao ^a   Smith, Matthew J ^a   Reichardt, Louis F ^c   Ikura, Mitsuhiko ^a,b  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cellbio; Molneuro

Indexed keywords

ARMADILLO DOMAIN PROTEIN; CADHERIN; JUXTAMEMBRANE DOMAIN PROTEIN; MEMBRANE PROTEIN; NERVE CELL ADHESION MOLECULE; P120 CATENIN; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; BINDING SITE; BRAIN DEVELOPMENT; CELL ADHESION; CELL INTERACTION; CRYSTAL STRUCTURE; DENDRITIC SPINE; GENE MUTATION; HYDROPHOBICITY; IN VITRO STUDY; MOLECULAR DYNAMICS; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STATIC ELECTRICITY; SYNAPSE;

ARMADILLO;

EID: 77950932981     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.01.017     Document Type: Article

References (48)

1. Al-Amoudi A., Díez D.C., Betts M.J., Frangakis A.S. The molecular architecture of cadherins in native epidermal desmosomes. Nature 2007, 450:832-837.
2. Anastasiadis P.Z., Reynolds A.B. The p120 catenin family: complex roles in adhesion, signaling and cancer. J. Cell Sci. 2000, 113:1319-1334.
3. Arikkath J., Reichardt L.F. Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity. Trends Neurosci. 2008, 31:487-494.
4. Bauer A., Lickert H., Kemler R., Stappert J. Modification of the E-cadherin-catenin complex in mitotic Madin-Darby canine kidney epithelial cells. J. Biol. Chem. 1998, 273:28314-28321.
5. Boggon T.J., Murray J., Chappuis-Flament S., Wong E., Gumbiner B.M., Shapiro L. C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 2002, 296:1308-1313.
6. Castaño J., Solanas G., Casagolda D., Raurell I., Villagrasa P., Bustelo X.R., García de Herreros A., Duñach M. Specific phosphorylation of p120-catenin regulatory domain differently modulates its binding to RhoA. Mol. Cell. Biol. 2007, 27:1745-1757.
7. Chen H., Paradies N.E., Fedor-Chaiken M., Brackenbury R. E-cadherin mediates adhesion and suppresses cell motility via distinct mechanisms. J. Cell Sci. 1997, 110:345-356.
8. Choi H.J., Weis W.I. Structure of the armadillo repeat domain of plakophilin 1. J. Mol. Biol. 2005, 346:367-376.
9. Daniel J.M., Reynolds A.B. The tyrosine kinase substrate p120cas binds directly to E-cadherin but not to the adenomatous polyposis coli protein or α-catenin. Mol. Cell. Biol. 1995, 15:4819-4824.
10. Daniel J.M., Reynolds A.B. The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol. Cell. Biol. 1999, 19:3614-3623.
11. Davis M.A., Ireton R.C., Reynolds A.B. A core function for p120-catenin in cadherin turnover. J. Cell Biol. 2003, 163:525-534.
12. Elia L.P., Yamamoto M., Zang K., Reichardt L.F. p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 2006, 51:43-56.
13. Fujita Y., Krause G., Scheffner M., Zechner D., Leddy H.E., Behrens J., Sommer T., Birchmeier W. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 2002, 4:222-231.
14. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
15. Huber A.H., Weis W.I. The structure of the β-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by β-catenin. Cell 2001, 105:391-402.
16. Huber A.H., Stewart D.B., Laurents D.V., Nelson W.J., Weis W.I. The cadherin cytoplasmic domain is unstructured in the absence of β-catenin. A possible mechanism for regulating cadherin turnover. J. Biol. Chem. 2001, 276:12301-12309.
17. Ireton R.C., Davis M.A., van Hengel J., Mariner D.J., Barnes K., Thoreson M.A., Anastasiadis P.Z., Matrisian L., Bundy L.M., Sealy L., et al. A novel role for p120 catenin in E-cadherin function. J. Cell Biol. 2002, 159:465-476.
18. Kaurah P., MacMillan A., Boyd N., Senz J., De Luca A., Chun N., Suriano G., Zaor S., Van Manen L., Gilpin C., et al. Founder and recurrent CDH1 mutations in families with hereditary diffuse gastric cancer. JAMA 2007, 297:2360-2372.
19. Kelly B.T., McCoy A.J., Späte K., Miller S.E., Evans P.R., Höning S., Owen D.J. A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 2008, 456:976-979.
20. Lampugnani M.G., Corada M., Andriopoulou P., Esser S., Risau W., Dejana E. Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells. J. Cell Sci. 1997, 110:2065-2077.
21. Lee S.-H., Peng I.-F., Ng Y.G., Yanagisawa M., Bamji S.X., Elia L.P., Balsamo J., Lilien J., Anastasiadis P.Z., Ullian E.M., Reichardt L.F. Synapses are regulated by the cytoplasmic tyrosine kinase Fer in a pathway mediated by p120catenin, Fer, SHP-2, and β-catenin. J. Cell Biol. 2008, 183:893-908.
22. Marambaud P., Shioi J., Serban G., Georgakopoulos A., Sarner S., Nagy V., Baki L., Wen P., Efthimiopoulos S., Shao Z., et al. A presenilin-1/γ-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J. 2002, 21:1948-1956.
23. Meng W., Mushika Y., Ichii T., Takeichi M. Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 2008, 135:948-959.
24. Miyashita Y., Ozawa M. A dileucine motif in its cytoplasmic domain directs β-catenin-uncoupled E-cadherin to the lysosome. J. Cell Sci. 2007, 120:4395-4406.
25. Miyashita Y., Ozawa M. Increased internalization of p120-uncoupled E-cadherin and a requirement for a dileucine motif in the cytoplasmic domain for endocytosis of the protein. J. Biol. Chem. 2007, 282:11540-11548.
26. Mosesson Y., Mills G.B., Yarden Y. Derailed endocytosis: an emerging feature of cancer. Nat. Rev. Cancer 2008, 8:835-850.
27. Myster S.H., Cavallo R., Anderson C.T., Fox D.T., Peifer M. Drosophila p120catenin plays a supporting role in cell adhesion but is not an essential adherens junction component. J. Cell Biol. 2003, 160:433-449.
28. Nishimura T., Takeichi M. Remodeling of the adherens junctions during morphogenesis. Curr. Top. Dev. Biol. 2009, 89:33-54.
29. Nollet F., Kools P., van Roy F. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J. Mol. Biol. 2000, 299:551-572.
30. Notredame C., Higgins D.G., Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 2000, 302:205-217.
31. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
32. Peifer M., Yap A.S. Traffic control: p120-catenin acts as a gatekeeper to control the fate of classical cadherins in mammalian cells. J. Cell Biol. 2003, 163:437-440.
33. Perez-Moreno M., Davis M.A., Wong E., Pasolli H.A., Reynolds A.B., Fuchs E. p120-catenin mediates inflammatory responses in the skin. Cell 2006, 124:631-644.
34. Pokutta S., Weis W.I. Structure of the dimerization and β-catenin-binding region of α-catenin. Mol. Cell 2000, 5:533-543.
35. v-src, is related to cadherin-binding factors β-catenin, plakoglobin and armadillo. Oncogene 1992, 7:2439-2445.
36. Reynolds A.B., Daniel J., McCrea P.D., Wheelock M.J., Wu J., Zhang Z. Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol. Cell. Biol. 1994, 14:8333-8342.
37. Riehl R., Johnson K., Bradley R., Grunwald G.B., Cornel E., Lilienbaum A., Holt C.E. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 1996, 17:837-848.
38. Shapiro L., Weis W.I. Structure and biochemistry of cadherins and catenins. Cold Spring Harb Perspect Biol 2009, 1:a003053.
39. Thoreson M.A., Reynolds A.B. Altered expression of the catenin p120 in human cancer: implications for tumor progression. Differentiation 2002, 70:583-589.
40. Thoreson M.A., Anastasiadis P.Z., Daniel J.M., Ireton R.C., Wheelock M.J., Johnson K.R., Hummingbird D.K., Reynolds A.B. Selective uncoupling of p120(ctn) from E-cadherin disrupts strong adhesion. J. Cell Biol. 2000, 148:189-202.
41. Xiao K., Allison D.F., Buckley K.M., Kottke M.D., Vincent P.A., Faundez V., Kowalczyk A.P. Cellular levels of p120 catenin function as a set point for cadherin expression levels in microvascular endothelial cells. J. Cell Biol. 2003, 163:535-545.
42. Xu G., Craig A.W., Greer P., Miller M., Anastasiadis P.Z., Lilien J., Balsamo J. Continuous association of cadherin with β-catenin requires the non-receptor tyrosine-kinase Fer. J. Cell Sci. 2004, 117:3207-3219.
43. Yamada S., Nelson W.J. Synapses: sites of cell recognition, adhesion, and functional specification. Annu. Rev. Biochem. 2007, 76:267-294.
44. Yamada S., Pokutta S., Drees F., Weis W.I., Nelson W.J. Deconstructing the cadherin-catenin-actin complex. Cell 2005, 123:889-901.
45. Yanagisawa M., Huveldt D., Kreinest P., Lohse C.M., Cheville J.C., Parker A.S., Copland J.A., Anastasiadis P.Z. A p120 catenin isoform switch affects Rho activity, induces tumor cell invasion, and predicts metastatic disease. J. Biol. Chem. 2008, 283:18344-18354.
46. Yang J., Dokurno P., Tonks N.K., Barford D. Crystal structure of the M-fragment of α-catenin: implications for modulation of cell adhesion. EMBO J. 2001, 20:3645-3656.
47. Yap A.S., Brieher W.M., Pruschy M., Gumbiner B.M. Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function. Curr. Biol. 1997, 7:308-315.
48. Yap A.S., Niessen C.M., Gumbiner B.M. The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120ctn. J. Cell Biol. 1998, 141:779-789.