p120-catenin binding masks an endocytic signal conserved in classical cadherins

Journal of Cell Biology

Volumn 199, Issue 2, 2012, Pages 365-380

  Nanes, Benjamin A ^a   Chiasson MacKenzie, Christine ^a   Lowery, Anthony M ^b   Ishiyama, Noboru ^c   Faundez, Victor ^a   Ikura, Mitsuhiko ^c   Vincent, Peter A ^b   Kowalczyk, Andrew P ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CATENIN; PROTEIN P120; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CELL JUNCTION; CELL MIGRATION; ENDOCYTOSIS; ENDOSOME; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INFLAMMATION; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN STABILITY;

ADHERENS JUNCTIONS; ANIMALS; ANTIGENS, CD; BINDING SITES; CADHERINS; CATENINS; CELL ADHESION; CELL COMMUNICATION; CELL LINE, TUMOR; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOCYTOSIS; ENDOTHELIAL CELLS; HELA CELLS; HUMANS; INFLAMMATION; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN BINDING; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 84869116723     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201205029     Document Type: Article

References (51)

1. Adam, A.P., A.L. Sharenko, K. Pumiglia, and P.A. Vincent. 2010. Src-induced tyrosine phosphorylation of VE-cadherin is not sufficient to decrease barrier function of endothelial monolayers. J. Biol. Chem. 285:7045-7055. http://dx.doi.org/10.1074/jbc.M109.079277
2. Canel, M., A. Serrels, K.I. Anderson, M.C. Frame, and V.G. Brunton. 2010. Use of photoactivation and photobleaching to monitor the dynamic regulation of E-cadherin at the plasma membrane. Cell Adh. Migr. 4:491-501. http://dx.doi.org/10.4161/cam.4.4.12661
3. Chacon-Heszele, M.F., D. Ren, A.B. Reynolds, F. Chi, and P. Chen. 2012. Regulation of cochlear convergent extension by the vertebrate planar cell polarity pathway is dependent on p120-catenin. Development. 139: 968-978. http://dx.doi.org/10.1242/dev.065326
4. Chiasson, C.M., K.B. Wittich, P.A. Vincent, V. Faundez, and A.P. Kowalczyk. 2009. p120-catenin inhibits VE-cadherin internalization through a Rhoindependent mechanism. Mol. Biol. Cell. 20:1970-1980. http://dx.doi.org/10.1091/mbc.E08-07-0735
5. Davis, M.A., and A.B. Reynolds. 2006. Blocked acinar development, E-cadherin reduction, and intraepithelial neoplasia upon ablation of p120-catenin in the mouse salivary gland. Dev. Cell. 10:21-31. http://dx.doi.org/10.1016/j.devcel.2005.12.004
6. Davis, M.A., R.C. Ireton, and A.B. Reynolds. 2003. A core function for p120-catenin in cadherin turnover. J. Cell Biol. 163:525-534. http://dx.doi.org/10.1083/jcb.200307111
7. de Beco, S., C. Gueudry, F. Amblard, and S. Coscoy. 2009. Endocytosis is required for E-cadherin redistribution at mature adherens junctions. Proc. Natl. Acad. Sci. USA. 106:7010-7015. http://dx.doi.org/10.1073/pnas.0811253106.
8. Dejana, E., F. Orsenigo, and M.G. Lampugnani. 2008. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J. Cell Sci. 121:2115-2122. http://dx.doi.org/10.1242/jcs.017897
9. Dejana, E., E. Tournier-Lasserve, and B.M. Weinstein. 2009. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev. Cell. 16:209-221. http://dx.doi.org/10.1016/j.devcel.2009.01.004
10. Drees, F., S. Pokutta, S. Yamada, W.J. Nelson, and W.I. Weis. 2005. Alphacatenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell. 123:903-915. http://dx.doi.org/10.1016/j.cell.2005.09.021
11. Elia, L.P., M. Yamamoto, K. Zang, and L.F. Reichardt. 2006. p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron. 51:43-56. http://dx.doi.org/10.1016/j.neuron.2006.05.018
12. Ferreri, D.M., F.L. Minnear, T. Yin, A.P. Kowalczyk, and P.A. Vincent. 2008. N-cadherin levels in endothelial cells are regulated by monolayer maturity and p120 availability. Cell Commun. Adhes. 15:333-349. http://dx.doi.org/10.1080/15419060802440377
13. Fujita, Y., G. Krause, M. Scheffner, D. Zechner, H.E. Leddy, J. Behrens, T. Sommer, and W. Birchmeier. 2002. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4:222-231. http://dx.doi.org/10.1038/ncb758
14. Gavard, J., and J.S. Gutkind. 2006. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat. Cell Biol. 8:1223-1234. http://dx.doi.org/10.1038/ncb1486
15. Gavard, J., V. Patel, and J.S. Gutkind. 2008. Angiopoietin-1 prevents VEGFinduced endothelial permeability by sequestering Src through mDia. Dev. Cell. 14:25-36. http://dx.doi.org/10.1016/j.devcel.2007.10.019
16. Harris, T.J., and U. Tepass. 2010. Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11:502-514. http://dx.doi.org/10.1038/nrm2927
17. Hashimoto, A., S. Hashimoto, R. Ando, K. Noda, E. Ogawa, H. Kotani, M. Hirose, T. Menju, M. Morishige, T. Manabe, et al. 2011. GEP100-Arf6-AMAP1-cortactin pathway frequently used in cancer invasion is activated by VEGFR2 to promote angiogenesis. PLoS ONE. 6:e23359. http://dx.doi.org/10.1371/journal.pone.0023359
18. Hatzfeld, M. 2005. The p120 family of cell adhesion molecules. Eur. J. Cell Biol. 84:205-214. http://dx.doi.org/10.1016/j.ejcb.2004.12.016
19. Ireton, R.C., M.A. Davis, J. van Hengel, D.J. Mariner, K. Barnes, M.A. Thoreson, P.Z. Anastasiadis, L. Matrisian, L.M. Bundy, L. Sealy, et al. 2002. A novel role for p120 catenin in E-cadherin function. J. Cell Biol. 159:465-476. http://dx.doi.org/10.1083/jcb.200205115
20. Ishiyama, N., S.H. Lee, S. Liu, G.Y. Li, M.J. Smith, L.F. Reichardt, and M. Ikura. 2010. Dynamic and static interactions between p120 catenin and E-cadherin regulate the stability of cell-cell adhesion. Cell. 141:117-128. http://dx.doi.org/10.1016/j.cell.2010.01.017
21. Jarrett, O., J.L. Stow, A.S. Yap, and B. Key. 2002. Dynamin-dependent endocytosis is necessary for convergent-extension movements in Xenopus animal cap explants. Int. J. Dev. Biol. 46:467-473.
22. Kawauchi, T., K. Sekine, M. Shikanai, K. Chihama, K. Tomita, K. Kubo, K. Nakajima, Y. Nabeshima, and M. Hoshino. 2010. Rab GTPasesdependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron. 67:588-602. http://dx.doi.org/10.1016/j.neuron.2010.07.007
23. Kidoya, H., H. Naito, and N. Takakura. 2010. Apelin induces enlarged and nonleaky blood vessels for functional recovery from ischemia. Blood. 115:3166-3174. http://dx.doi.org/10.1182/blood-2009-07-232306
24. Kurley, S.J., B. Bierie, R.H. Carnahan, N.A. Lobdell, M.A. Davis, I. Hofmann, H.L. Moses, W.J. Muller, and A.B. Reynolds. 2012. p120-catenin is essential for terminal end bud function and mammary morphogenesis. Development. 139:1754-1764. http://dx.doi.org/10.1242/dev.072769
25. LaFlamme, S.E., L.A. Thomas, S.S. Yamada, and K.M. Yamada. 1994. Single subunit chimeric integrins as mimics and inhibitors of endogenous integrin functions in receptor localization, cell spreading and migration, and matrix assembly. J. Cell Biol. 126:1287-1298. http://dx.doi.org/10.1083/jcb.126.5.1287
26. 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. http://dx.doi.org/10.1083/jcb.146.1.219
27. Levayer, R., A. Pelissier-Monier, and T. Lecuit. 2011. Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat. Cell Biol. 13:529-540. http://dx.doi.org/10.1038/ncb2224
28. Lewis, J.E., J.K. Wahl III, K.M. Sass, P.J. Jensen, K.R. Johnson, and M.J. Wheelock. 1997. Cross-talk between adherens junctions and desmosomes depends on plakoglobin. J. Cell Biol. 136:919-934. http://dx.doi.org/10.1083/jcb.136.4.919
29. Marciano, D.K., P.R. Brakeman, C.Z. Lee, N. Spivak, D.J. Eastburn, D.M. Bryant, G.M. Beaudoin III, I. Hofmann, K.E. Mostov, and L.F. Reichardt. 2011. p120 catenin is required for normal renal tubulogenesis and glomerulogenesis. Development. 138:2099-2109. http://dx.doi.org/10.1242/dev.056564
30. Miyashita, Y., and M. Ozawa. 2007. 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. 282:11540-11548. http://dx.doi.org/10.1074/jbc.M608351200
31. 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. http://dx.doi.org/10.1083/jcb.200211083
32. Nanes, B.A., and A.P. Kowalczyk. 2012. Adherens junction turnover: Regulating adhesion through cadherin endocytosis, degradation, and recycling. In Adherens Junctions: From Molecular Mechanisms to Tissue Development and Disease. T. Harris, editor. Springer Science + Business Media, Heidelberg, Germany/New York. 197-222. http://dx.doi.org/10.1007/978-94-007-4186-7_9
33. Navarro, P., L. Caveda, F. Breviario, I. Mândoteanu, M.G. Lampugnani, and E. Dejana. 1995. Catenin-dependent and -independent functions of vascular endothelial cadherin. J. Biol. Chem. 270:30965-30972. http://dx.doi.org/10.1074/jbc.270.52.30965
34. Oas, R.G., K. Xiao, S. Summers, K.B. Wittich, C.M. Chiasson, W.D. Martin, H.E. Grossniklaus, P.A. Vincent, A.B. Reynolds, and A.P. Kowalczyk. 2010. p120-Catenin is required for mouse vascular development. Circ. Res. 106:941-951. http://dx.doi.org/10.1161/CIRCRESAHA.109.207753
35. Palacios, F., J.S. Tushir, Y. Fujita, and C. D'Souza-Schorey. 2005. Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol. Cell. Biol. 25:389-402. http://dx.doi.org/10.1128/MCB.25.1.389-402.2005
36. Perez-Moreno, M., M.A. Davis, E. Wong, H.A. Pasolli, A.B. Reynolds, and E. Fuchs. 2006. p120-catenin mediates inflammatory responses in the skin. Cell. 124:631-644. http://dx.doi.org/10.1016/j.cell.2005.11.043
37. 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. http://dx.doi.org/10.1083/jcb.200212136
38. Saito, M., D.K. Tucker, D. Kohlhorst, C.M. Niessen, and A.P. Kowalczyk. 2012. Classical and desmosomal cadherins at a glance. J. Cell Sci. 125: 2547-2552. http://dx.doi.org/10.1242/jcs.066654
39. Smalley-Freed, W.G., A. Efimov, P.E. Burnett, S.P. Short, M.A. Davis, D.L. Gumucio, M.K. Washington, R.J. Coffey, and A.B. Reynolds. 2010. p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J. Clin. Invest. 120:1824-1835. http://dx.doi.org/10.1172/JCI41414
40. Sprague, B.L., R.L. Pego, D.A. Stavreva, and J.G. McNally. 2004. Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys. J. 86:3473-3495. http://dx.doi.org/10.1529/biophysj.103.026765
41. Stairs, D.B., L.J. Bayne, B. Rhoades, M.E. Vega, T.J. Waldron, J. Kalabis, A. Klein-Szanto, J.S. Lee, J.P. Katz, J.A. Diehl, et al. 2011. Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a tumor suppressor gene. Cancer Cell. 19:470-483. http://dx.doi.org/10.1016/j.ccr.2011.02.007
42. Taguchi, K., T. Ishiuchi, and M. Takeichi. 2011. Mechanosensitive EPLINdependent remodeling of adherens junctions regulates epithelial reshaping. J. Cell Biol. 194:643-656. http://dx.doi.org/10.1083/jcb.201104124
43. 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 p120ctn from E-cadherin disrupts strong adhesion. J. Cell Biol. 148:189-202. http://dx.doi.org/10.1083/jcb.148.1.189
44. Troyanovsky, R.B., E.P. Sokolov, and S.M. Troyanovsky. 2006. Endocytosis of cadherin from intracellular junctions is the driving force for cadherin adhesive dimer disassembly. Mol. Biol. Cell. 17:3484-3493. http://dx.doi.org/10.1091/mbc.E06-03-0190
45. Venkiteswaran, K., K. Xiao, S. Summers, C.C. Calkins, P.A. Vincent, K. Pumiglia, and A.P. Kowalczyk. 2002. Regulation of endothelial barrier function and growth by VE-cadherin, plakoglobin, and beta-catenin. Am. J. Physiol. Cell Physiol. 283:C811-C821.
46. Vincent, P.A., K. Xiao, K.M. Buckley, and A.P. Kowalczyk. 2004. VE-cadherin: adhesion at arm's length. Am. J. Physiol. Cell Physiol. 286:C987-C997. http://dx.doi.org/10.1152/ajpcell.00522.2003
47. Xiao, K., D.F. Allison, K.M. Buckley, M.D. Kottke, P.A. Vincent, V. Faundez, and A.P. Kowalczyk. 2003a. Cellular levels of p120 catenin function as a set point for cadherin expression levels in microvascular endothelial cells. J. Cell Biol. 163:535-545. http://dx.doi.org/10.1083/jcb.200306001
48. Xiao, K., D.F. Allison, M.D. Kottke, S. Summers, G.P. Sorescu, V. Faundez, and A.P. Kowalczyk. 2003b. Mechanisms of VE-cadherin processing and degradation in microvascular endothelial cells. J. Biol. Chem. 278:19199-19208. http://dx.doi.org/10.1074/jbc.M211746200
49. Xiao, K., J. Garner, K.M. Buckley, P.A. Vincent, C.M. Chiasson, E. Dejana, V. Faundez, and A.P. Kowalczyk. 2005. p120-Catenin regulates clathrindependent endocytosis of VE-cadherin. Mol. Biol. Cell. 16:5141-5151. http://dx.doi.org/10.1091/mbc.E05-05-0440
50. Xiao, K., R.G. Oas, C.M. Chiasson, and A.P. Kowalczyk. 2007. Role of p120-catenin in cadherin trafficking. Biochim. Biophys. Acta. 1773:8-16. http://dx.doi.org/10.1016/j.bbamcr.2006.07.005
51. Yamada, S., S. Pokutta, F. Drees, W.I. Weis, and W.J. Nelson. 2005. Deconstructing the cadherin-catenin-actin complex. Cell. 123:889-901. http://dx.doi.org/10.1016/j.cell.2005.09.020