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PMID: 12032299 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Binding strength and activation state of single fibrinogen-integrin pairs on living cells.

Litvinov RI, Shuman H, Bennett JS, Weisel JW

Abstract

Integrin activation states determine the ability of these receptors to mediate cell-matrix and cell-cell interactions. The prototypic example of this phenomenon is the platelet integrin, alphaIIbbeta3. In unstimulated platelets, alphaIIbbeta3 is inactive, whereas exposing platelets to an agonist such as ADP or thrombin enables alphaIIbbeta3 to bind ligands such as fibrinogen and von Willebrand factor. To study the regulation of integrin activation states at the level of single molecules, we developed a model system based on laser tweezers, enabling us to determine the rupture forces required to separate single ligand-receptor pairs by using either purified proteins or intact living cells. Here, we show that rupture forces of individual fibrinogen molecules and either purified alphaIIbbeta3 or alphaIIbbeta3 on the surface of living platelets were 60 to 150 pN with a peak yield strength of 80-100 pN. Platelet stimulation using either ADP or the thrombin receptor-activating peptide enhanced the accessibility but not the adhesion strength of single alphaIIbbeta3 molecules, indicating that there are only two states of alphaIIbbeta3 activation. Thus, we found it possible to use laser tweezers to measure the regulation of forces between individual ligand-receptor pairs on living cells. This methodology can be applied to the study of other regulated cell membrane receptors using the ligand-receptor yield strength as a direct measure of receptor activation/inactivation state.

MeSH Terms
Binding Sites Blood Platelets/physiology,ultrastructure Cell Membrane/physiology Fibrinogen/chemistry,physiology,ultrastructure Humans Lasers Microscopy, Electron Platelet Glycoprotein GPIIb-IIIa Complex/chemistry,physiology,ultrastructure Probability Stress, Mechanical von Willebrand Factor/chemistry,physiology
Chemicals
Platelet Glycoprotein GPIIb-IIIa Complex von Willebrand Factor Fibrinogen
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Litvinov Rustem I
Department of Cell and Developmental Biology, University of Pennsylvania School of Medicine, Philadelphia, PA 19104-6058, USA.
Shuman Henry
Bennett Joel S
Weisel John W
References (32)
32 references, click to expand
  1. Effects of ligand-mimetic peptides Arg-Gly-Asp-X (X = Phe, Trp, Ser) on alphaIIbbeta3 integrin conformation and oligomerization.
    Biochemistry. 1999 Nov 2;38(44):14461-74 PMID: 10545168
  2. Redistribution of alpha-granule membrane glycoprotein IIb/IIIa (integrin alpha IIb beta 3) to the surface membrane of human platelets during the release reaction.
    J Electron Microsc (Tokyo). 1994 Oct;43(5):282-9 PMID: 7535331
  3. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor.
    Cell. 1996 Jan 26;84(2):289-97 PMID: 8565074
  4. Binding of a fibrinogen mimetic stabilizes integrin alphaIIbbeta3's open conformation.
    Protein Sci. 2001 Aug;10(8):1614-26 PMID: 11468358
  5. Mechanical anchoring strength of L-selectin, beta2 integrins, and CD45 to neutrophil cytoskeleton and membrane.
    Biophys J. 1999 Jul;77(1):587-96 PMID: 10388783
  6. A structural basis for integrin activation by the cytoplasmic tail of the alpha IIb-subunit.
    Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1450-5 PMID: 10677482
  7. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules.
    Science. 1996 Feb 9;271(5250):795-9 PMID: 8628994
  8. Efficiency of platelet adhesion to fibrinogen depends on both cell activation and flow.
    Biophys J. 2000 Jun;78(6):2834-43 PMID: 10827966
  9. Resting platelets contain a substantial centrally located pool of glycoprotein IIb-IIIa complex which may be accessible to some but not other extracellular proteins.
    J Biol Chem. 1986 Nov 15;261(32):15242-51 PMID: 2429967
  10. Probing the relation between force--lifetime--and chemistry in single molecular bonds.
    Annu Rev Biophys Biomol Struct. 2001;30:105-28 PMID: 11340054
  11. Characteristics of a membrane reservoir buffering membrane tension.
    Biophys J. 1999 Oct;77(4):1992-2002 PMID: 10512819
  12. Inhibition of fibrinogen binding to stimulated human platelets by a monoclonal antibody.
    Proc Natl Acad Sci U S A. 1983 May;80(9):2417-21 PMID: 6302680
  13. Forces of a single-beam gradient laser trap on a dielectric sphere in the ray optics regime.
    Biophys J. 1992 Feb;61(2):569-82 PMID: 19431818
  14. Two-dimensional tracking of ncd motility by back focal plane interferometry.
    Biophys J. 1998 Feb;74(2 Pt 1):1074-85 PMID: 9533719
  15. Versatile optical traps with feedback control.
    Methods Enzymol. 1998;298:460-89 PMID: 9751903
  16. Time and force dependence of the rupture of glycoprotein IIb-IIIa-fibrinogen bonds between latex spheres.
    Biophys J. 2000 Mar;78(3):1195-206 PMID: 10692309
  17. Studying receptor-mediated cell adhesion at the single molecule level.
    Cell Adhes Commun. 1998 Jul;5(5):375-95 PMID: 9789685
  18. A new murine monoclonal antibody reports an activation-dependent change in the conformation and/or microenvironment of the platelet glycoprotein IIb/IIIa complex.
    J Clin Invest. 1985 Jul;76(1):101-8 PMID: 2991335
  19. Platelet receptor recognition site on human fibrinogen. Synthesis and structure-function relationship of peptides corresponding to the carboxy-terminal segment of the gamma chain.
    Biochemistry. 1984 Apr 10;23(8):1767-74 PMID: 6326808
  20. Structural biology of glycoprotein IIb-IIIa.
    Trends Cardiovasc Med. 1996 Jan;6(1):31-6 PMID: 21232272
  21. Optical trapping and manipulation of neutral particles using lasers.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):4853-60 PMID: 9144154
  22. Complementary roles for receptor clustering and conformational change in the adhesive and signaling functions of integrin alphaIIb beta3.
    J Cell Biol. 1998 Jun 29;141(7):1685-95 PMID: 9647659
  23. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy.
    Nature. 1999 Jan 7;397(6714):50-3 PMID: 9892352
  24. Single integrin molecule adhesion forces in intact cells measured by atomic force microscopy.
    Biochem Biophys Res Commun. 1999 Jun 16;259(3):645-50 PMID: 10364472
  25. Adhesion forces between individual ligand-receptor pairs.
    Science. 1994 Apr 15;264(5157):415-7 PMID: 8153628
  26. Effect of calcium on the stability of the platelet membrane glycoprotein IIb-IIIa complex.
    J Biol Chem. 1985 Jul 5;260(13):7875-81 PMID: 2409078
  27. Increased surface expression of the membrane glycoprotein IIb/IIIa complex induced by platelet activation. Relationship to the binding of fibrinogen and platelet aggregation.
    Blood. 1987 Aug;70(2):475-83 PMID: 3607284
  28. Novel platelet inhibitors.
    Annu Rev Med. 2001;52:161-84 PMID: 11160773
  29. Intermolecular forces and energies between ligands and receptors.
    Science. 1994 Oct 14;266(5183):257-9 PMID: 7939660
  30. Biological applications of optical forces.
    Annu Rev Biophys Biomol Struct. 1994;23:247-85 PMID: 7919782
  31. Analysis of GPIIb/IIIa receptor number by quantification of 7E3 binding to human platelets.
    Blood. 1996 Aug 1;88(3):907-14 PMID: 8704248
  32. Detection and characterization of individual intermolecular bonds using optical tweezers.
    Biophys J. 2001 Jun;80(6):2976-86 PMID: 11371470
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2002-05-28
Pages
7426-31
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC124247
Subset
IM
Grants
NHLBI NIH HHS · HLBI 30954 · United States
NHLBI NIH HHS · HLBI 57407 · United States
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