Abstract
Cadherins are glycoproteins that are responsible for homophilic, Ca2+-dependent cell-cell adhesion and play crucial roles in many cellular adhesion processes ranging from embryogenesis to the formation of neuronal circuits in the central nervous system. Many different experimental approaches have been used to unravel the molecular basis for cadherin-mediated adhesion. In particular, several high-resolution structures have provided models for cadherin-cadherin interactions that are illuminative in many respects yet contradictory in others. This review gives an overview of the structural studies of cadherins over the past decade while focusing on recent developments that reconcile some of the earlier findings.
Key words: Cell adhesion, cadherin, desmosome, cis- and trans-interactions, X-ray crystallography, nuclear magnetic resonance (NMR) spectroscopy, electron microscopy (EM), electron tomography (ET)
References
- 1.Takeichi M. Cadherins: a molecular family important in selective cell-cell adhesion. Annu. Rev. Biochem. 1990;59:237–252. doi: 10.1146/annurev.bi.59.070190.001321. [DOI] [PubMed] [Google Scholar]
- 2.Gumbiner B. M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell. 1996;84:345–357. doi: 10.1016/S0092-8674(00)81279-9. [DOI] [PubMed] [Google Scholar]
- 3.Takeichi M. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 1995;7:619–627. doi: 10.1016/0955-0674(95)80102-2. [DOI] [PubMed] [Google Scholar]
- 4.Tepass U., Truong K., Godt D., Ikura M., Peifer M. Cadherins in embryonic and neural morphogenesis. Nat. Rev. Mol. Cell. Biol. 2000;1:91–100. doi: 10.1038/35040042. [DOI] [PubMed] [Google Scholar]
- 5.Ranscht B. Cadherins: molecular codes for axon guidance and synapse formation. Int. J. Dev. Neurosci. 2000;18:643–651. doi: 10.1016/S0736-5748(00)00030-7. [DOI] [PubMed] [Google Scholar]
- 6.Redies C. Cadherins in the central nervous system. Prog. Neurobiol. 2000;61:611–648. doi: 10.1016/S0301-0082(99)00070-2. [DOI] [PubMed] [Google Scholar]
- 7.Christofori G. Changing neighbours, changing behaviour: cell adhesion molecule-mediated signalling during tumour progression. EMBO. 2003;122:2318–2323. doi: 10.1093/emboj/cdg228. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Van Aken E., De Wever O., Correia da Rocha A. S., Mareel M. Defective E-cadherin/catenin complexes in human cancer. Virchows Arch. 2001;439:725–751. doi: 10.1007/s004280100516. [DOI] [PubMed] [Google Scholar]
- 9.Behrens J. Cadherins and catenins: role in signal transduction and tumor progression. Cancer Metastasis Rev. 1999;18:15–30. doi: 10.1023/A:1006200102166. [DOI] [PubMed] [Google Scholar]
- 10.Christofori G., Semb H. The role of the cell-adhesion molecule E-cadherin as a tumour-suppressor gene. Trends Biochem. Sci. 1999;24:73–76. doi: 10.1016/S0968-0004(98)01343-7. [DOI] [PubMed] [Google Scholar]
- 11.Perl A. K., Wilgenbus P., Dahl U., Semb H., Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature. 1998;392:190–193. doi: 10.1038/32433. [DOI] [PubMed] [Google Scholar]
- 12.Nose A., Tsuji K., Takeichi M. Localization of specificity determining sites in cadherin cell adhesion molecules. Cell. 1990;61:147–155. doi: 10.1016/0092-8674(90)90222-Z. [DOI] [PubMed] [Google Scholar]
- 13.Kemler R. Classical cadherins. Semin. Cell Biol. 1992;3:149–155. doi: 10.1016/S1043-4682(10)80011-X. [DOI] [PubMed] [Google Scholar]
- 14.Takeichi M., Hatta K., Nose A., Nagafuchi A., Matsunaga M. Cadherin-mediated specific cell adhesion and animal morphogenesis. Ciba Found. Symp. 1989;144:243–249. doi: 10.1002/9780470513798.ch14. [DOI] [PubMed] [Google Scholar]
- 15.Yap A. S., Brieher W. M., Gumbiner B. M. Molecular and functional analysis of cadherin-based adherens junctions. Annu. Rev. Cell. Dev. Biol. 1997;13:119–146. doi: 10.1146/annurev.cellbio.13.1.119. [DOI] [PubMed] [Google Scholar]
- 16.Koch A. W., Bozic D., Pertz O., Engel J. Homophilic adhesion by cadherins. Curr. Opin. Struct. Biol. 1999;9:275–281. doi: 10.1016/S0959-440X(99)80038-4. [DOI] [PubMed] [Google Scholar]
- 17.Aberle H., Schwartz H., Kemler R. Cadherincatenin complex: protein interactions and their implications for cadherin function. J. Cell. Biochem. 1996;61:514–523. doi: 10.1002/(SICI)1097-4644(19960616)61:4<514::AID-JCB4>3.0.CO;2-R. [DOI] [PubMed] [Google Scholar]
- 18.Angst B. D., Marcozzi C., Magee A. I. The cadherin superfamily: diversity in form and function. J. Cell Sci. 2001;114:629–641. doi: 10.1242/jcs.114.4.629. [DOI] [PubMed] [Google Scholar]
- 19.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. doi: 10.1006/jmbi.2000.3777. [DOI] [PubMed] [Google Scholar]
- 20.Gumbiner B. M. Regulation of cadherin adhesive activity. J. Cell Biol. 2000;148:399–404. doi: 10.1083/jcb.148.3.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Lilien J., Balsamo J., Arregui C., Xu G. Turn-off, drop-out: functional state switching of cadherins. Dev. Dyn. 2002;224:18–29. doi: 10.1002/dvdy.10087. [DOI] [PubMed] [Google Scholar]
- 22.Steinberg M. S., McNutt P. M. Cadherins and their connections: adhesion junctions have broader functions. Curr. Opin. Cell Biol. 1999;11:554–560. doi: 10.1016/S0955-0674(99)00027-7. [DOI] [PubMed] [Google Scholar]
- 23.Yap A. S., Kovacs E. M. Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell Biol. 2003;160:11–16. doi: 10.1083/jcb.200208156. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Pokutta S., Drees F., Takai Y., Nelson W. J., Weis W. I. Biochemical and structural definition of the 1-afadin- and actinbinding sites of alpha-catenin. J. Biol. Chem. 2002;277:18868–18874. doi: 10.1074/jbc.M201463200. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Huber A. H., Weis W. I. The structure of the betacatenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell. 2001;105:391–402. doi: 10.1016/S0092-8674(01)00330-0. [DOI] [PubMed] [Google Scholar]
- 26.Pokutta S., Weis W. I. Structure of the dimerization and beta-catenin-binding region of alpha-catenin. Mol. Cell. 2000;5:533–543. doi: 10.1016/S1097-2765(00)80447-5. [DOI] [PubMed] [Google Scholar]
- 27.Huber O. Structure and function of desmosomal proteins and their role in development and disease. Cell. Mol. Life Sci. 2003;60:1872–1890. doi: 10.1007/s00018-003-3050-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Frank M., Kemler R. Protocadherins. Curr. Opin. Cell Biol. 2002;14:557–562. doi: 10.1016/S0955-0674(02)00365-4. [DOI] [PubMed] [Google Scholar]
- 29.Mareel M., Leroy A. Clinical, cellular and molecular aspects of cancer invasion. Physiol. Rev. 2003;83:337–376. doi: 10.1152/physrev.00024.2002. [DOI] [PubMed] [Google Scholar]
- 30.Dustin M. L., Colman D. R. Neural and immunological synaptic relations. Science. 2002;298:785–789. doi: 10.1126/science.1076386. [DOI] [PubMed] [Google Scholar]
- 31.Goda Y. Cadherins communicate structural plasticity of presynaptic and postsynaptic terminals. Neuron. 2002;35:1–3. doi: 10.1016/S0896-6273(02)00765-1. [DOI] [PubMed] [Google Scholar]
- 32.Guthrie S. Neuronal development: sorting out motor neurons. Curr. Biol. 2002;12:R488–R490. doi: 10.1016/S0960-9822(02)00965-X. [DOI] [PubMed] [Google Scholar]
- 33.Huntley G. W., Gil O., Bozdagi O. The cadherin family of cell adhesion molecules: multiple roles in synaptic plasticity. Neuroscientist. 2002;8:221–233. doi: 10.1177/1073858402008003008. [DOI] [PubMed] [Google Scholar]
- 34.Yagi T. Diversity of the cadherin-related neuronal receptor/protocadherin family and possible DNA rearrangement in the brain. Genes Cells. 2003;8:1–8. doi: 10.1046/j.1365-2443.2003.00614.x. [DOI] [PubMed] [Google Scholar]
- 35.Blaschuk O. W., Sullivan R., David S., Pouliot Y. Identification of a cadherin cell adhesion recognition sequence. Dev. Biol. 1990;139:227–229. doi: 10.1016/0012-1606(90)90290-Y. [DOI] [PubMed] [Google Scholar]
- 36.Brieher W. M., Yap A. S., Gumbiner B. M. Lateral dimerization is required for the homophilic binding activity of C-cadherin. J. Cell Biol. 1996;135:487–496. doi: 10.1083/jcb.135.2.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Shan W. S., Koch A., Murray J., Colman D. R., Shapiro L. The adhesive binding site of cadherins revisited. Biophys. Chem. 1999;82:157–163. doi: 10.1016/S0301-4622(99)00115-5. [DOI] [PubMed] [Google Scholar]
- 38.Takeda H., Shimoyama Y., Nagafuchi A., Hirohashi S. E-cadherin functions as a cis-dimer at the cell-cell adhesive interface in vivo. Nat. Struct. Bio.l. 1999;6:310–312. doi: 10.1038/7542. [DOI] [PubMed] [Google Scholar]
- 39.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. doi: 10.1016/S0960-9822(06)00154-0. [DOI] [PubMed] [Google Scholar]
- 40.Chappuis-Flament S., Wong E., Hicks L. D., Kay C. M., Gumbiner B. M. Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J. Cell Biol. 2001;154:231–243. doi: 10.1083/jcb.200103143. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Kitagawa M., Natori M., Murase S., Hirano S., Taketani S., Suzuki S. T. Mutation analysis of cadherin-4 reveals amino acid residues of EC1 important for the structure and function. Biochem. Biophys. Res. Commun. 2000;271:358–363. doi: 10.1006/bbrc.2000.2636. [DOI] [PubMed] [Google Scholar]
- 42.Shan W. S., Tanaka H., Phillips G. R., Arndt K., Yoshida M., Colman D. R., et al. Functional cis-heterodimers of N- and R-cadherins. J. Cell Biol. 2000;148:579–590. doi: 10.1083/jcb.148.3.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Shimoyama Y., Tsujimoto G., Kitajima M., Natori M. Identification of three human type-II classic cadherins and frequent heterophilic interactions between different subclasses of type-II classic cadherins. Biochem. J. 2000;349:159–167. doi: 10.1042/bj3490159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Tamura K., Shan W. S., Hendrickson W. A., Colman D. R., Shapiro L. Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron. 1998;20:1153–1163. doi: 10.1016/S0896-6273(00)80496-1. [DOI] [PubMed] [Google Scholar]
- 45.Ozawa M. Lateral dimerization of the E-cadherin extracellular domain is necessary but not sufficient for adhesive activity. J. Biol. Chem. 2002;277:19600–19608. doi: 10.1074/jbc.M202029200. [DOI] [PubMed] [Google Scholar]
- 46.Troyanovsky R. B., Klingelhofer J., Troyanovsky S. Removal of calcium ions triggers a novel type of intercadherin interaction. J. Cell Sci. 1999;112:4379–4387. doi: 10.1242/jcs.112.23.4379. [DOI] [PubMed] [Google Scholar]
- 47.Chitaev N. A., Troyanovsky S. M. Adhesive but not lateral E-cadherin complexes require calcium and catenins for their formation. J. Cell Biol. 1998;142:837–846. doi: 10.1083/jcb.142.3.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48.Klingelhofer J., Laur O. Y., Troyanovsky R. B., Troyanovsky S. M. Dynamic interplay between adhesive and lateral E-cadherin dimers. Mol. Cell. Biol. 2002;22:7449–7458. doi: 10.1128/MCB.22.21.7449-7458.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Troyanovsky R. B., Sokolov E., Troyanovsky S. M. Adhesive and lateral E-cadherin dimers are mediated by the same interface. Mol. Cell. Biol. 2003;23:7965–7972. doi: 10.1128/MCB.23.22.7965-7972.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Pokutta S., Herrenknecht K., Kemler R., Engel J. Conformational changes of the recombinant extracellular domain of E- cadherin upon calcium binding. Eur. J. Biochem. 1994;223:1019–1026. doi: 10.1111/j.1432-1033.1994.tb19080.x. [DOI] [PubMed] [Google Scholar]
- 51.Pertz O., Bozic D., Koch A. W., Fauser C., Brancaccio A., Engel J. A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 1999;18:1738–1747. doi: 10.1093/emboj/18.7.1738. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Ahrens T., Pertz O., Haussinger D., Fauser C., Schulthess T., Engel J. Analysis of heterophilic and homophilic interactions of cadherins using the c-Jun/c-Fos dimerization domains. J. Biol. Chem. 2002;277:19455–19460. doi: 10.1074/jbc.M200606200. [DOI] [PubMed] [Google Scholar]
- 53.Ahrens T., Lambert M., Pertz O., Sasaki T., Schulthess T., Mege R. M., et al. Homoassociation of VE-cadherin follows a mechanism common to ‘classical’ cadherins. J. Mol. Biol. 2003;325:733–742. doi: 10.1016/S0022-2836(02)01286-X. [DOI] [PubMed] [Google Scholar]
- 54.Tomschy A., Fauser C., Landwehr R., Engel J. Homophilic adhesion of E-cadherin occurs by a co-operative two-step interaction of N-terminal domains. EMBO J. 1996;15:3507–3514. [PMC free article] [PubMed] [Google Scholar]
- 55.Sivasankar S., Gumbiner B., Leckband D. Direct measurements of multiple adhesive alignments and unbinding trajectories between cadherin extracellular domains. Biophys. J. 2001;80:1758–1768. doi: 10.1016/S0006-3495(01)76146-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Zhu B., Chappuis-Flament S., Wong E., Jensen I. E., Gumbiner B. M., Leckband D. Functional analysis of the structural basis of homophilic cadherin adhesion. Biophys. J. 2003;84:4033–4042. doi: 10.1016/S0006-3495(03)75129-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Sivasankar S., Brieher W., Lavrik N., Gumbiner B., Leckband D. Direct molecular force measurements of multiple adhesive interactions between cadherin ectodomains. Proc. Natl. Acad. Sci. USA. 1999;96:11820–11824. doi: 10.1073/pnas.96.21.11820. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Nagar B., Overduin M., Ikura M., Rini J. M. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature. 1996;380:360–364. doi: 10.1038/380360a0. [DOI] [PubMed] [Google Scholar]
- 59.Overduin M., Harvey T. S., Bagby S., Tong K. I., Yau P., Takeichi M., et al. Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science. 1995;267:386–389. doi: 10.1126/science.7824937. [DOI] [PubMed] [Google Scholar]
- 60.Overduin M., Tong K. I., Kay C. M., Ikura M. 1H, 15N and 13C resonance assignments and monomeric structure of the amino-terminal extracellular domain of epithelial cadherin. J. Biomol. NMR. 1996;7:173–189. doi: 10.1007/BF00202035. [DOI] [PubMed] [Google Scholar]
- 61.Shapiro L., Fannon A. M., Kwong P. D., Thompson A., Lehmann M. S., Grubel G., et al. Structural basis of cellcell adhesion by cadherins. Nature. 1995;374:327–337. doi: 10.1038/374327a0. [DOI] [PubMed] [Google Scholar]
- 62.Shapiro L., Kwong P. D., Fannon A. M., Colman D. R., Hendrickson W. A. Considerations on the folding topology and evolutionary origin of cadherin domains. Proc. Natl. Acad. Sci. USA. 1995;92:6793–6797. doi: 10.1073/pnas.92.15.6793. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63.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. doi: 10.1126/science.1071559. [DOI] [PubMed] [Google Scholar]
- 64.Haussinger D., Ahrens T., Sass H. J., Pertz O., Engel J., Grzesiek S. Calcium-dependent homoassociation of Ecadherin by NMR spectroscopy: changes in mobility, conformation and mapping of contact regions. J. Mol. Biol. 2002;324:823–839. doi: 10.1016/S0022-2836(02)01137-3. [DOI] [PubMed] [Google Scholar]
- 65.He W., Cowin P., Stokes D. L. Untangling desmosomal knots with electron tomography. Science. 2003;302:109–113. doi: 10.1126/science.1086957. [DOI] [PubMed] [Google Scholar]
- 66.Hyafil F., Babinet C., Jacob F. Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell. 1981;26:447–454. doi: 10.1016/0092-8674(81)90214-2. [DOI] [PubMed] [Google Scholar]
- 67.Ozawa M., Engel J., Kemler R. Single amino acid substitutions in one Ca2+ binding site of uvomorulin abolish the adhesive function. Cell. 1990;63:1033–1038. doi: 10.1016/0092-8674(90)90506-A. [DOI] [PubMed] [Google Scholar]
- 68.Tong K. I., Yau P., Overduin M., Bagby S., Porumb T., Takeichi M., et al. Purification and spectroscopic characterization of a recombinant amino-terminal polypeptide fragment of mouse epithelial cadherin. FEBS Lett. 1994;352:318–322. doi: 10.1016/0014-5793(94)00982-1. [DOI] [PubMed] [Google Scholar]
- 69.Koch A. W., Pokutta S., Lustig A., Engel J. Calcium binding and homoassociation of E-cadherin domains. Biochemistry. 1997;36:7697–7705. doi: 10.1021/bi9705624. [DOI] [PubMed] [Google Scholar]
- 70.Katz B. Z., Levenberg S., Yamada K. M., Geiger B. Modulation of cell-cell adherens junctions by surface clustering of the N-cadherin cytoplasmic tail. Exp. Cell Res. 1998;243:415–424. doi: 10.1006/excr.1998.4194. [DOI] [PubMed] [Google Scholar]
- 71.Ozawa M., Kemler R. The membrane-proximal region of the E-cadherin cytoplasmic domain prevents dimerization and negatively regulates adhesion activity. J. Cell Biol. 1998;142:1605–1613. doi: 10.1083/jcb.142.6.1605. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 72.Tanaka H., Shan W., Phillips G. R., Arndt K., Bozdagi O., Shapiro L., et al. Molecular modification of N-cadherin in response to synaptic activity. Neuron. 2000;25:93–107. doi: 10.1016/S0896-6273(00)80874-0. [DOI] [PubMed] [Google Scholar]
- 73.Laur O. Y., Klingelhofer J., Troyanovsky R. B., Troyanovsky S. M. Both the dimerization and immunochemical properties of E-cadherin EC 1 domain depend on Trp(156) residue. Arch. Biochem. Biophys. 2002;400:141–147. doi: 10.1006/abbi.2002.2774. [DOI] [PubMed] [Google Scholar]
- 74.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 pl20ctn. J. Cell Biol. 1998;141:779–789. doi: 10.1083/jcb.141.3.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 75.Huber O., Kemler R., Langosch D. Mutations affecting transmembrane segment interactions impair adhesiveness of E-cadherin. J. Cell Sci. 1999;112:4415–4423. doi: 10.1242/jcs.112.23.4415. [DOI] [PubMed] [Google Scholar]
- 76.Lambert M., Padilla F., Mege R. M. Immobilized dimers of N-cadherin-Fc chimera mimic cadherin-mediated cell contact formation: contribution of both outside-in and inside-out signals. J. Cell Sci. 2000;113:2207–2219. doi: 10.1242/jcs.113.12.2207. [DOI] [PubMed] [Google Scholar]
- 77.Alattia J. R., Ames J. B., Porumb T., Tong K. I., Heng Y. M., Ottensmeyer P., et al. Lateral self-assembly of E-cadherin directed by cooperative calcium binding. FEBS Lett. 1997;417:405–408. doi: 10.1016/S0014-5793(97)01333-1. [DOI] [PubMed] [Google Scholar]
- 78.Baumgartner W., Hinterdorfer P., Ness W., Raab A., Vestweber D., Schindler H., et al. Cadherin interaction probed by atomic force microscopy. Proc. Natl. Acad. Sci. USA. 2000;97:4005–4010. doi: 10.1073/pnas.070052697. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 79.Wahl J. K. 3., Kim Y. J., Cullen J. M., Johnson K. R., Wheelock M. J. N-cadherin-catenin complexes form prior to cleavage of the proregion and transport to the plasma membrane. J. Biol. Chem. 2003;278:17269–17276. doi: 10.1074/jbc.M211452200. [DOI] [PubMed] [Google Scholar]
- 80.Niessen C. M., Gumbiner B. M. Cadherin-mediated cell sorting not determined by binding or adhesion specificity. J. Cell Biol. 2002;156:389–399. doi: 10.1083/jcb.200108040. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 81.Karecla P. I., Green S. J., Bowden S. J., Coadwell J., Kilshaw P. J. Identification of a binding site for integrin alphaEbeta7 in the N-terminal domain of E-cadherin. J. Biol. Chem. 1996;271:30909–30915. doi: 10.1074/jbc.271.48.30909. [DOI] [PubMed] [Google Scholar]
- 82.Whittard J. D., Craig S. E., Mould A. P., Koch A., Pertz O., Engel J., et al. E-cadherin is a ligand for integrin alpha2betal. Matrix Biol. 2002;21:525. doi: 10.1016/S0945-053X(02)00037-9. [DOI] [PubMed] [Google Scholar]
- 83.Ozawa M., Kemler R. Correct proteolytic cleavage is required for the cell adhesive function of uvomorulin. J. Cell Biol. 1990;111:1645–1650. doi: 10.1083/jcb.111.4.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 84.Leckband D., Sivasankar S. Mechanism of homophilic cadherin adhesion. Curr. Opin. Cell Biol. 2000;12:587–592. doi: 10.1016/S0955-0674(00)00136-8. [DOI] [PubMed] [Google Scholar]
- 85.Nagafuchi A. Molecular architecture of adherens junctions. Curr. Opin. Cell Biol. 2001;13:600–603. doi: 10.1016/S0955-0674(00)00257-X. [DOI] [PubMed] [Google Scholar]