Home LiteratureArticle Details
PMID: 21796210 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Transforming binding affinities from three dimensions to two with application to cadherin clustering.

Nature ·Vol. 475 ·No. 7357 ·2011-07-27 ·Pages 510-3

Wu Y, Vendome J, Shapiro L, Ben-Shaul A, Honig B

Abstract

Membrane-bound receptors often form large assemblies resulting from binding to soluble ligands, cell-surface molecules on other cells and extracellular matrix proteins. For example, the association of membrane proteins with proteins on different cells (trans-interactions) can drive the oligomerization of proteins on the same cell (cis-interactions). A central problem in understanding the molecular basis of such phenomena is that equilibrium constants are generally measured in three-dimensional solution and are thus difficult to relate to the two-dimensional environment of a membrane surface. Here we present a theoretical treatment that converts three-dimensional affinities to two dimensions, accounting directly for the structure and dynamics of the membrane-bound molecules. Using a multiscale simulation approach, we apply the theory to explain the formation of ordered, junction-like clusters by classical cadherin adhesion proteins. The approach features atomic-scale molecular dynamics simulations to determine interdomain flexibility, Monte Carlo simulations of multidomain motion and lattice simulations of junction formation. A finding of general relevance is that changes in interdomain motion on trans-binding have a crucial role in driving the lateral, cis-, clustering of adhesion receptors.

MeSH Terms
Cadherins/chemistry,metabolism Computer Simulation Membrane Glycoproteins/chemistry,metabolism Membrane Proteins/chemistry,metabolism Models, Molecular Molecular Dynamics Simulation Monte Carlo Method Platelet Glycoprotein GPIb-IX Complex Protein Binding Protein Structure, Quaternary Protein Structure, Tertiary
Chemicals
Cadherins Membrane Glycoproteins Membrane Proteins Platelet Glycoprotein GPIb-IX Complex adhesion receptor
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Wu Yinghao
Department of Biochemistry and Molecular Biophysics, Columbia University, New York, New York 10032, USA.
Vendome Jeremie
Shapiro Lawrence
Ben-Shaul Avinoam
Honig Barry
References (21)
21 references, click to expand
  1. GROMACS: fast, flexible, and free.
    J Comput Chem. 2005 Dec;26(16):1701-18 PMID: 16211538
  2. Anisotropy of fluctuation dynamics of proteins with an elastic network model.
    Biophys J. 2001 Jan;80(1):505-15 PMID: 11159421
  3. TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity.
    Nature. 2010 Feb 18;463(7283):963-7 PMID: 20164930
  4. Identification of self through two-dimensional chemistry and synapses.
    Annu Rev Cell Dev Biol. 2001;17:133-57 PMID: 11687486
  5. Immunoglobulin superfamily cell adhesion molecules: zippers and signals.
    Curr Opin Cell Biol. 2007 Oct;19(5):543-50 PMID: 17935964
  6. Models for the specific adhesion of cells to cells.
    Science. 1978 May 12;200(4342):618-27 PMID: 347575
  7. Red blood cell membrane fluctuations and shape controlled by ATP-induced cytoskeletal defects.
    Biophys J. 2005 Mar;88(3):1859-74 PMID: 15613626
  8. The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins.
    Structure. 2011 Feb 9;19(2):244-56 PMID: 21300292
  9. 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
  10. 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
  11. 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
  12. Type II cadherin ectodomain structures: implications for classical cadherin specificity.
    Cell. 2006 Mar 24;124(6):1255-68 PMID: 16564015
  13. Nanoscale increases in CD2-CD48-mediated intermembrane spacing decrease adhesion and reorganize the immunological synapse.
    J Biol Chem. 2008 Dec 5;283(49):34414-22 PMID: 18826951
  14. Low affinity interaction of human or rat T cell adhesion molecule CD2 with its ligand aligns adhering membranes to achieve high physiological affinity.
    J Biol Chem. 1997 Dec 5;272(49):30889-98 PMID: 9388235
  15. Cell adhesion molecules, signal transduction and cell growth.
    Curr Opin Cell Biol. 1999 Dec;11(6):737-44 PMID: 10600702
  16. Building-block approach for determining low-frequency normal modes of macromolecules.
    Proteins. 2000 Oct 1;41(1):1-7 PMID: 10944387
  17. C-cadherin ectodomain structure and implications for cell adhesion mechanisms.
    Science. 2002 May 17;296(5571):1308-13 PMID: 11964443
  18. Cell adhesion. Competition between nonspecific repulsion and specific bonding.
    Biophys J. 1984 Jun;45(6):1051-64 PMID: 6743742
  19. Spontaneous assembly and active disassembly balance adherens junction homeostasis.
    Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3528-33 PMID: 20133579
  20. Visualization of CD2 interaction with LFA-3 and determination of the two-dimensional dissociation constant for adhesion receptors in a contact area.
    J Cell Biol. 1996 Feb;132(3):465-74 PMID: 8636222
  21. A coarse-grained normal mode approach for macromolecules: an efficient implementation and application to Ca(2+)-ATPase.
    Biophys J. 2002 Nov;83(5):2457-74 PMID: 12414680
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2011-07-27
Epub
2011-00-27
Pages
510-3
Language
English
Region
England
NLM ID
0410462
PMCID
PMC3167384
Subset
IM
Grants
NIGMS NIH HHS · R01 GM062270 · United States
NIGMS NIH HHS · R01 GM062270-07 · United States
NIGMS NIH HHS · R01GM062270-07 · United States
Howard Hughes Medical Institute · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com