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PMID: 23812234 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Tuning the kinetics of cadherin adhesion.

The Journal of investigative dermatology ·Vol. 133 ·No. 10 ·2013-10-00 ·Pages 2318-2323

Sivasankar S

Abstract

Cadherins are Ca(2+)-dependent cell-cell adhesion proteins that maintain the structural integrity of the epidermis; their principle function is to resist mechanical force. This review summarizes the biophysical mechanisms by which classical cadherins tune adhesion and withstand mechanical stress. We first relate the structure of classical cadherins to their equilibrium binding properties. We then review the role of mechanical perturbations in tuning the kinetics of cadherin adhesion. In particular, we highlight recent studies that show that cadherins form three types of adhesive bonds: catch bonds, which become longer lived and lock in the presence of tensile force; slip bonds, which become shorter lived when pulled; and ideal bonds, which are insensitive to tugging.

MeSH Terms
Animals Cadherins/physiology Cell Adhesion/physiology Epidermal Cells Epidermis/physiology Extracellular Matrix/physiology Humans Tensile Strength/physiology
Chemicals
Cadherins
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Sivasankar Sanjeevi
Department of Physics and Astronomy, Iowa State University, Ames, Iowa, USA; Ames Laboratory, United States Department of Energy, Ames, Iowa, USA. Electronic address: sivasank@iastate.edu.
References (69)
69 references, click to expand
  1. Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan.
    J Biol Chem. 2004 Jan 16;279(3):2291-8 PMID: 14573602
  2. Mechanotransduction at cadherin-mediated adhesions.
    Curr Opin Cell Biol. 2011 Oct;23(5):523-30 PMID: 21890337
  3. Characterizing the initial encounter complex in cadherin adhesion.
    Structure. 2009 Aug 12;17(8):1075-81 PMID: 19646884
  4. The relationships among adhesion, stratification and differentiation in keratinocytes.
    Cell Death Differ. 1996 Oct;3(4):357-71 PMID: 17180106
  5. Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation.
    Physiol Rev. 2011 Apr;91(2):691-731 PMID: 21527735
  6. The reaction-limited kinetics of membrane-to-surface adhesion and detachment.
    Proc R Soc Lond B Biol Sci. 1988 Jun 22;234(1274):55-83 PMID: 2901109
  7. Transforming binding affinities from three dimensions to two with application to cadherin clustering.
    Nature. 2011 Jul 27;475(7357):510-3 PMID: 21796210
  8. Productive tension: force-sensing and homeostasis of cell-cell junctions.
    Trends Cell Biol. 2011 Sep;21(9):499-505 PMID: 21763139
  9. Two-step adhesive binding by classical cadherins.
    Nat Struct Mol Biol. 2010 Mar;17(3):348-57 PMID: 20190754
  10. Trans-bonded pairs of E-cadherin exhibit a remarkable hierarchy of mechanical strengths.
    Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16472-7 PMID: 15546992
  11. Demonstration of catch bonds between an integrin and its ligand.
    J Cell Biol. 2009 Jun 29;185(7):1275-84 PMID: 19564406
  12. Calcium-dependent homoassociation of E-cadherin by NMR spectroscopy: changes in mobility, conformation and mapping of contact regions.
    J Mol Biol. 2002 Dec 6;324(4):823-39 PMID: 12460580
  13. The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins.
    Structure. 2011 Feb 9;19(2):244-56 PMID: 21300292
  14. Structural studies on desmosomes.
    Biochem Soc Trans. 2008 Apr;36(Pt 2):181-7 PMID: 18363559
  15. Cell adhesion receptors in mechanotransduction.
    Curr Opin Cell Biol. 2008 Oct;20(5):551-6 PMID: 18583124
  16. Cooperativity between trans and cis interactions in cadherin-mediated junction formation.
    Proc Natl Acad Sci U S A. 2010 Oct 12;107(41):17592-7 PMID: 20876147
  17. Lifetime measurements reveal kinetic differences between homophilic cadherin bonds.
    Biophys J. 2006 Feb 15;90(4):1385-95 PMID: 16326909
  18. Ideal, catch, and slip bonds in cadherin adhesion.
    Proc Natl Acad Sci U S A. 2012 Nov 13;109(46):18815-20 PMID: 23112161
  19. Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting.
    Cell. 2010 May 14;141(4):645-55 PMID: 20478255
  20. Linking molecular affinity and cellular specificity in cadherin-mediated adhesion.
    Proc Natl Acad Sci U S A. 2009 Jul 14;106(28):11594-9 PMID: 19553217
  21. Specificity of cell-cell adhesion by classical cadherins: Critical role for low-affinity dimerization through beta-strand swapping.
    Proc Natl Acad Sci U S A. 2005 Jun 14;102(24):8531-6 PMID: 15937105
  22. Allosteric cross talk between cadherin extracellular domains.
    Biophys J. 2010 Jul 7;99(1):95-104 PMID: 20655837
  23. A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration.
    Dev Cell. 2012 Jan 17;22(1):104-15 PMID: 22169071
  24. Mechanical tugging force regulates the size of cell-cell junctions.
    Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):9944-9 PMID: 20463286
  25. Resolving cadherin interactions and binding cooperativity at the single-molecule level.
    Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):109-14 PMID: 19114658
  26. Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin.
    Cell. 2001 Feb 23;104(4):605-17 PMID: 11239416
  27. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis.
    Development. 1988 Apr;102(4):639-55 PMID: 3048970
  28. Direct observation of catch bonds involving cell-adhesion molecules.
    Nature. 2003 May 8;423(6936):190-3 PMID: 12736689
  29. Structural basis of cell-cell adhesion by cadherins.
    Nature. 1995 Mar 23;374(6520):327-37 PMID: 7885471
  30. The cadherin superfamily in neuronal connections and interactions.
    Nat Rev Neurosci. 2007 Jan;8(1):11-20 PMID: 17133224
  31. Cadherin exits the junction by switching its adhesive bond.
    J Cell Biol. 2011 Mar 21;192(6):1073-83 PMID: 21422232
  32. The minimal essential unit for cadherin-mediated intercellular adhesion comprises extracellular domains 1 and 2.
    J Biol Chem. 2004 Dec 31;279(53):55914-23 PMID: 15485826
  33. Regulation of cadherin-mediated adhesion in morphogenesis.
    Nat Rev Mol Cell Biol. 2005 Aug;6(8):622-34 PMID: 16025097
  34. E-cadherin controls adherens junctions in the epidermis and the renewal of hair follicles.
    EMBO J. 2003 Nov 3;22(21):5723-33 PMID: 14592971
  35. Spatial organization of adhesion: force-dependent regulation and function in tissue morphogenesis.
    EMBO J. 2010 Aug 18;29(16):2753-68 PMID: 20717145
  36. Strength dependence of cadherin-mediated adhesions.
    Biophys J. 2010 Feb 17;98(4):534-42 PMID: 20159149
  37. Conditional targeting of E-cadherin in skin: insights into hyperproliferative and degenerative responses.
    Proc Natl Acad Sci U S A. 2004 Jan 13;101(2):552-7 PMID: 14704278
  38. Multiple cadherin extracellular repeats mediate homophilic binding and adhesion.
    J Cell Biol. 2001 Jul 9;154(1):231-43 PMID: 11449003
  39. N-cadherin-mediated cell motility requires cis dimers.
    Cell Commun Adhes. 2005 Jan-Apr;12(1-2):23-39 PMID: 16371344
  40. {alpha}-Catenin mediates initial E-cadherin-dependent cell-cell recognition and subsequent bond strengthening.
    Proc Natl Acad Sci U S A. 2008 Nov 25;105(47):18331-6 PMID: 19017792
  41. E-cadherin functions as a cis-dimer at the cell-cell adhesive interface in vivo.
    Nat Struct Biol. 1999 Apr;6(4):310-2 PMID: 10201395
  42. N-glycosylation alters cadherin-mediated intercellular binding kinetics.
    J Cell Sci. 2012 May 15;125(Pt 10):2478-85 PMID: 22344255
  43. C-cadherin ectodomain structure and implications for cell adhesion mechanisms.
    Science. 2002 May 17;296(5571):1308-13 PMID: 11964443
  44. Thinking outside the cell: how cadherins drive adhesion.
    Trends Cell Biol. 2012 Jun;22(6):299-310 PMID: 22555008
  45. Tight junctions/adherens junctions: basic structure and function.
    J Invest Dermatol. 2007 Nov;127(11):2525-32 PMID: 17934504
  46. Structure-function analysis of cell adhesion by neural (N-) cadherin.
    Neuron. 1998 Jun;20(6):1153-63 PMID: 9655503
  47. Structural basis of calcium-induced E-cadherin rigidification and dimerization.
    Nature. 1996 Mar 28;380(6572):360-4 PMID: 8598933
  48. Molecular design principles underlying β-strand swapping in the adhesive dimerization of cadherins.
    Nat Struct Mol Biol. 2011 Jun;18(6):693-700 PMID: 21572446
  49. Direct measurements of multiple adhesive alignments and unbinding trajectories between cadherin extracellular domains.
    Biophys J. 2001 Apr;80(4):1758-68 PMID: 11259289
  50. Functional analysis of the structural basis of homophilic cadherin adhesion.
    Biophys J. 2003 Jun;84(6):4033-42 PMID: 12770907
  51. Catch bonds govern adhesion through L-selectin at threshold shear.
    J Cell Biol. 2004 Sep 13;166(6):913-23 PMID: 15364963
  52. Bacterial adhesion to target cells enhanced by shear force.
    Cell. 2002 Jun 28;109(7):913-23 PMID: 12110187
  53. Two stage cadherin kinetics require multiple extracellular domains but not the cytoplasmic region.
    J Biol Chem. 2008 Jan 25;283(4):1848-56 PMID: 17999960
  54. Convergence of Wnt, beta-catenin, and cadherin pathways.
    Science. 2004 Mar 5;303(5663):1483-7 PMID: 15001769
  55. A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation.
    EMBO J. 1999 Apr 1;18(7):1738-47 PMID: 10202138
  56. Biophysical properties of cadherin bonds do not predict cell sorting.
    J Biol Chem. 2008 Oct 17;283(42):28454-63 PMID: 18552401
  57. Proteolytic E-cadherin activation followed by solution NMR and X-ray crystallography.
    EMBO J. 2004 Apr 21;23(8):1699-708 PMID: 15071499
  58. The crystal structure of human E-cadherin domains 1 and 2, and comparison with other cadherins in the context of adhesion mechanism.
    J Mol Biol. 2007 Oct 19;373(2):401-11 PMID: 17850815
  59. Physically based principles of cell adhesion mechanosensitivity in tissues.
    Rep Prog Phys. 2012 Nov;75(11):116601 PMID: 23085962
  60. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis.
    Genes Dev. 2006 Dec 1;20(23):3199-214 PMID: 17158740
  61. Calcium site mutations in cadherin: impact on adhesion and evidence of cooperativity.
    Biochemistry. 2006 Jun 6;45(22):6930-9 PMID: 16734428
  62. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner.
    J Cell Biol. 2010 Jun 28;189(7):1107-15 PMID: 20584916
  63. Adhesive and lateral E-cadherin dimers are mediated by the same interface.
    Mol Cell Biol. 2003 Nov;23(22):7965-72 PMID: 14585958
  64. Similarities between heterophilic and homophilic cadherin adhesion.
    Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15434-9 PMID: 17023539
  65. Lateral dimerization is required for the homophilic binding activity of C-cadherin.
    J Cell Biol. 1996 Oct;135(2):487-96 PMID: 8896604
  66. The mechanism of cell adhesion by classical cadherins: the role of domain 1.
    J Cell Sci. 2005 Feb 15;118(Pt 4):711-21 PMID: 15671061
  67. Desmosomes: new perspectives on a classic.
    J Invest Dermatol. 2007 Nov;127(11):2499-515 PMID: 17934502
  68. Desmosomes at a glance.
    J Cell Sci. 2009 Dec 15;122(Pt 24):4401-7 PMID: 19955337
  69. Calcium binding and homoassociation of E-cadherin domains.
    Biochemistry. 1997 Jun 24;36(25):7697-705 PMID: 9201910
Article Info
Journal
The Journal of investigative dermatology
Abbr.
J Invest Dermatol
ISSN
1523-1747
DOI
10.1038/jid.2013.229
Email
sivasank@iastate.edu
Published
2013-10-00
Epub
2013-00-27
Pages
2318-2323
Language
English
Region
United States
NLM ID
0426720
PMCID
PMC3773255
Subset
IM
Grants
NIAMS NIH HHS · R13 AR009431 · United States
External Links
PubMed source DOI: 10.1038/jid.2013.229 PMC Full Text View journal details
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