Biophysical basis of cadherin mediated cell-cell adhesion.

Classical cadherin transmembrane cell-cell adhesion proteins play essential roles in tissue morphogenesis and in mediating tissue integrity. Cadherin ectodomains from opposing cells interact to form load-bearing trans dimers that mechanically couple cells. Cell-cell adhesion is believed to be strengthened by cis clustering of cadherins on the same cell surface. This review summarizes biophysical studies of the structure, interaction kinetics and biomechanics of classical cadherin ectodomains. We first discuss the structure and equilibrium binding kinetics of classical cadherin trans and cis dimers. We then discuss how mechanical stimuli alters the kinetics of cadherin interaction and tunes adhesion. Finally, we highlight open questions on the role of mechanical forces in influencing cadherin structure, function and organization on the cell surface.

[1]  R. Zaidel-Bar,et al.  Actin-delimited adhesion-independent clustering of E-cadherin forms the nanoscale building blocks of adherens junctions. , 2015, Developmental cell.

[2]  C. Kay,et al.  Multiple cadherin extracellular repeats mediate homophilic binding and adhesion , 2001, The Journal of cell biology.

[3]  Brenton D Hoffman,et al.  Towards a Dynamic Understanding of Cadherin-Based Mechanobiology. , 2015, Trends in cell biology.

[4]  L Shapiro,et al.  Linking molecular affinity and cellular specificity in cadherin-mediated adhesion , 2009, Proceedings of the National Academy of Sciences.

[5]  Cheng Zhu,et al.  Catch bonds govern adhesion through L-selectin at threshold shear , 2004, The Journal of cell biology.

[6]  B. Honig,et al.  T-cadherin structures reveal a novel adhesive binding mechanism , 2010, Nature Structural &Molecular Biology.

[7]  Peter D. Kwong,et al.  Structural basis of cell-cell adhesion by cadherins , 1995, Nature.

[8]  Sami Alom Ruiz,et al.  Mechanical tugging force regulates the size of cell–cell junctions , 2010, Proceedings of the National Academy of Sciences.

[9]  Cheng Zhu,et al.  Direct observation of catch bonds involving cell-adhesion molecules , 2003, Nature.

[10]  B. Honig,et al.  E-cadherin junction formation involves an active kinetic nucleation process , 2015, Proceedings of the National Academy of Sciences.

[11]  Wayne A. Hendrickson,et al.  Structure-Function Analysis of Cell Adhesion by Neural (N-) Cadherin , 1998, Neuron.

[12]  Fabiana Bahna,et al.  Molecular design principles underlying β-strand swapping in the adhesive dimerization of cadherins , 2011, Nature Structural &Molecular Biology.

[13]  T. Boggon,et al.  C-Cadherin Ectodomain Structure and Implications for Cell Adhesion Mechanisms , 2002, Science.

[14]  D. Leckband,et al.  A Computational Model for Kinetic Studies of Cadherin Binding and Clustering. , 2016, Biophysical journal.

[15]  B. Gumbiner,et al.  Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function , 1997, Current Biology.

[16]  M. Dembo,et al.  Kinetics of cell detachment: peeling of discrete receptor clusters. , 1994, Biophysical journal.

[17]  S. Rakshit,et al.  Ideal, catch, and slip bonds in cadherin adhesion , 2012, Proceedings of the National Academy of Sciences.

[18]  D. Torney,et al.  The reaction-limited kinetics of membrane-to-surface adhesion and detachment , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[19]  R. Tampé,et al.  The formation of ordered nanoclusters controls cadherin anchoring to actin and cell–cell contact fluidity , 2015, The Journal of cell biology.

[20]  Cheng Zhu,et al.  Low Force Decelerates L-selectin Dissociation from P-selectin Glycoprotein Ligand-1 and Endoglycan* , 2004, Journal of Biological Chemistry.

[21]  B. Honig,et al.  The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. , 2011, Structure.

[22]  S. Grzesiek,et al.  Proteolytic E‐cadherin activation followed by solution NMR and X‐ray crystallography , 2004, The EMBO journal.

[23]  E. Parisini,et al.  The crystal structure of human E-cadherin domains 1 and 2, and comparison with other cadherins in the context of adhesion mechanism. , 2007, Journal of molecular biology.

[24]  B. Honig,et al.  Cooperativity between trans and cis interactions in cadherin-mediated junction formation , 2010, Proceedings of the National Academy of Sciences.

[25]  T. Kodama,et al.  Identification and characterization of the X-dimer of human P-cadherin: implications for homophilic cell adhesion. , 2014, Biochemistry.

[26]  T. Lecuit,et al.  Principles of E-Cadherin Supramolecular Organization In Vivo , 2013, Current Biology.

[27]  W. Weis,et al.  Re-solving the Cadherin-Catenin-Actin Conundrum* , 2006, Journal of Biological Chemistry.

[28]  R. Jernigan,et al.  Molecular determinants of cadherin ideal bond formation: Conformation-dependent unbinding on a multidimensional landscape , 2016, Proceedings of the National Academy of Sciences.

[29]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[30]  T. Lecuit,et al.  E-cadherin junctions as active mechanical integrators in tissue dynamics , 2015, Nature Cell Biology.

[31]  W. Weis,et al.  Structure and biochemistry of cadherins and catenins. , 2009, Cold Spring Harbor perspectives in biology.

[32]  D. Hammer,et al.  Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow , 1995, Nature.

[33]  F. Amblard,et al.  Endocytosis is required for E-cadherin redistribution at mature adherens junctions , 2009, Proceedings of the National Academy of Sciences.

[34]  W. Nelson,et al.  Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. , 2006, Genes & development.

[35]  B. Honig,et al.  Two-step adhesive binding by classical cadherins , 2010, Nature Structural &Molecular Biology.

[36]  Julia Brasch,et al.  Structural and energetic determinants of adhesive binding specificity in type I cadherins , 2014, Proceedings of the National Academy of Sciences.

[37]  J. Waschke,et al.  Atomic Force Microscopy Provides New Mechanistic Insights into the Pathogenesis of Pemphigus , 2018, Front. Immunol..

[38]  O. Pertz,et al.  A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E‐cadherin homoassociation , 1999, The EMBO journal.

[39]  Yinghao Wu,et al.  Transforming binding affinities from 3D to 2D with application to cadherin clustering , 2011, Nature.

[40]  Andrew R. Fisher,et al.  Dissociation of bimolecular αIIbβ3-fibrinogen complex under a constant tensile force. , 2011, Biophysical journal.

[41]  B. Kidd,et al.  Structural Basis for Mechanical Force Regulation of the Adhesin FimH via Finger Trap-like β Sheet Twisting , 2010, Cell.

[42]  G. Berx,et al.  Involvement of members of the cadherin superfamily in cancer. , 2009, Cold Spring Harbor perspectives in biology.

[43]  O. Blaschuk,et al.  Identification of a cadherin cell adhesion recognition sequence. , 1990, Developmental biology.

[44]  Matthew D. Langer,et al.  N-glycosylation alters cadherin-mediated intercellular binding kinetics , 2012, Journal of Cell Science.

[45]  D E Leckband,et al.  Cadherin adhesion and mechanotransduction. , 2014, Annual review of cell and developmental biology.

[46]  Hui Li,et al.  Resolving the molecular mechanism of cadherin catch bond formation , 2014, Nature Communications.

[47]  B. Honig,et al.  Mechanism of E-cadherin dimerization probed by NMR relaxation dispersion , 2013, Proceedings of the National Academy of Sciences.

[48]  Jacquelyn A. Kunkel,et al.  Adhesion through single peptide aptamers. , 2011, The journal of physical chemistry. A.

[49]  S. Chu,et al.  Resolving cadherin interactions and binding cooperativity at the single-molecule level , 2009, Proceedings of the National Academy of Sciences.

[50]  Steven Chu,et al.  Characterizing the initial encounter complex in cadherin adhesion. , 2009, Structure.

[51]  Cheng Zhu,et al.  JCB_200810002 1275..1284 , 2009 .

[52]  B. Honig,et al.  Thinking outside the cell: how cadherins drive adhesion. , 2012, Trends in cell biology.

[53]  M. Ikura,et al.  Structural basis of calcium-induced E-cadherin rigidification and dimerization , 1996, Nature.

[54]  Mitsuhiko Ikura,et al.  Structural basis of calcium-induced E-cadherin rigidification and dimerization , 1996 .

[55]  A Kusumi,et al.  Single molecule imaging of green fluorescent proteins in living cells: E-cadherin forms oligomers on the free cell surface. , 2001, Biophysical journal.

[56]  A. Yap,et al.  A bigger picture: classical cadherins and the dynamic actin cytoskeleton , 2012, Nature Reviews Molecular Cell Biology.

[57]  Viola Vogel,et al.  Bacterial Adhesion to Target Cells Enhanced by Shear Force , 2002, Cell.