Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1993 Jun;64(6):1922–1933. doi: 10.1016/S0006-3495(93)81563-7

Granulocyte-endothelium initial adhesion. Analysis of transient binding events mediated by E-selectin in a laminar shear flow.

G Kaplanski 1, C Farnarier 1, O Tissot 1, A Pierres 1, A M Benoliel 1, M C Alessi 1, S Kaplanski 1, P Bongrand 1
PMCID: PMC1262526  PMID: 7690258

Abstract

The adhesion of moving cells to receptor-bearing surfaces is a key step to many important biological processes. Attachment was subjected to extensive modeling. However, the numerical values of kinetic bonding parameters relevant to realistic models of cell adhesion remain poorly known. In this report, we describe the motion of human granulocytes to interleukin-1-activated endothelial cells in presence of a low hydrodynamic drag (a few piconewtons) estimated to be much weaker than a standard ligand-receptor bond. It was thus expected to visualize the formation and rupture of individual bonds. We observed multiple short-time cell arrests with a median duration of 2.43 s. Stop frequency, not duration, was significantly inhibited by anti-E-selectin antibodies. Binding efficiency exhibited an almost linear relationship with the inverse of cell velocity. The distribution of arrest duration was determined: results were consistent with the view that these arrests reflected the formation/dissociation of single ligand-receptor bonds with a spontaneous dissociation rate of 0.5 s-1. The rate of bond formation was on the order of 0.04 s-1 when cells were freely rolling (mean velocity: 19 microns/s) and it exhibited an approximately 10-fold increase after the formation of a first adhesion.

Full text

PDF
1922

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. André P., Gabert J., Benoliel A. M., Capo C., Boyer C., Schmitt-Verhulst A. M., Malissen B., Bongrand P. Wild type and tailless CD8 display similar interaction with microfilaments during capping. J Cell Sci. 1991 Oct;100(Pt 2):329–337. doi: 10.1242/jcs.100.2.329. [DOI] [PubMed] [Google Scholar]
  2. Atherton A., Born G. V. Quantitative investigations of the adhesiveness of circulating polymorphonuclear leucocytes to blood vessel walls. J Physiol. 1972 Apr;222(2):447–474. doi: 10.1113/jphysiol.1972.sp009808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bell G. I., Dembo M., Bongrand P. Cell adhesion. Competition between nonspecific repulsion and specific bonding. Biophys J. 1984 Jun;45(6):1051–1064. doi: 10.1016/S0006-3495(84)84252-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bell G. I. Models for the specific adhesion of cells to cells. Science. 1978 May 12;200(4342):618–627. doi: 10.1126/science.347575. [DOI] [PubMed] [Google Scholar]
  5. Bevilacqua M. P., Pober J. S., Wheeler M. E., Cotran R. S., Gimbrone M. A., Jr Interleukin 1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes, and related leukocyte cell lines. J Clin Invest. 1985 Nov;76(5):2003–2011. doi: 10.1172/JCI112200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cozens-Roberts C., Lauffenburger D. A., Quinn J. A. Receptor-mediated cell attachment and detachment kinetics. I. Probabilistic model and analysis. Biophys J. 1990 Oct;58(4):841–856. doi: 10.1016/S0006-3495(90)82430-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dembo M., Torney D. C., Saxman K., Hammer D. 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. doi: 10.1098/rspb.1988.0038. [DOI] [PubMed] [Google Scholar]
  8. Detmers P. A., Wright S. D., Olsen E., Kimball B., Cohn Z. A. Aggregation of complement receptors on human neutrophils in the absence of ligand. J Cell Biol. 1987 Sep;105(3):1137–1145. doi: 10.1083/jcb.105.3.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dustin M. L., Springer T. A. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature. 1989 Oct 19;341(6243):619–624. doi: 10.1038/341619a0. [DOI] [PubMed] [Google Scholar]
  10. Evans E., Berk D., Leung A. Detachment of agglutinin-bonded red blood cells. I. Forces to rupture molecular-point attachments. Biophys J. 1991 Apr;59(4):838–848. doi: 10.1016/S0006-3495(91)82296-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Foxall C., Watson S. R., Dowbenko D., Fennie C., Lasky L. A., Kiso M., Hasegawa A., Asa D., Brandley B. K. The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis(x) oligosaccharide. J Cell Biol. 1992 May;117(4):895–902. doi: 10.1083/jcb.117.4.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gimbrone M. A., Jr Culture of vascular endothelium. Prog Hemost Thromb. 1976;3:1–28. [PubMed] [Google Scholar]
  13. Gould K., Ramirez-Ronda C. H., Holmes R. K., Sanford J. P. Adherence of bacteria to heart valves in vitro. J Clin Invest. 1975 Dec;56(6):1364–1370. doi: 10.1172/JCI108216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hammer D. A., Apte S. M. Simulation of cell rolling and adhesion on surfaces in shear flow: general results and analysis of selectin-mediated neutrophil adhesion. Biophys J. 1992 Jul;63(1):35–57. doi: 10.1016/S0006-3495(92)81577-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hammer D. A., Lauffenburger D. A. A dynamical model for receptor-mediated cell adhesion to surfaces. Biophys J. 1987 Sep;52(3):475–487. doi: 10.1016/S0006-3495(87)83236-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Harlan J. M. Leukocyte-endothelial interactions. Blood. 1985 Mar;65(3):513–525. [PubMed] [Google Scholar]
  17. Kuijpers T. W., Hakkert B. C., Hart M. H., Roos D. Neutrophil migration across monolayers of cytokine-prestimulated endothelial cells: a role for platelet-activating factor and IL-8. J Cell Biol. 1992 May;117(3):565–572. doi: 10.1083/jcb.117.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lawrence M. B., Springer T. A. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell. 1991 May 31;65(5):859–873. doi: 10.1016/0092-8674(91)90393-d. [DOI] [PubMed] [Google Scholar]
  19. Lee D. A., Hoidal J. R., Garlich D. J., Clawson C. C., Quie P. G., Peterson P. K. Opsonin-independent phagocytosis of surface-adherent bacteria by human alveolar macrophages. J Leukoc Biol. 1984 Dec;36(6):689–701. doi: 10.1002/jlb.36.6.689. [DOI] [PubMed] [Google Scholar]
  20. Mege J. L., Capo C., Benoliel A. M., Bongrand P. Determination of binding strength and kinetics of binding initiation. A model study made on the adhesive properties of P388D1 macrophage-like cells. Cell Biophys. 1986 Apr;8(2):141–160. doi: 10.1007/BF02788478. [DOI] [PubMed] [Google Scholar]
  21. Mege J. L., Capo C., Benoliel A. M., Foa C., Bongrand P. Study of cell deformability by a simple method. J Immunol Methods. 1985 Sep 3;82(1):3–15. doi: 10.1016/0022-1759(85)90219-4. [DOI] [PubMed] [Google Scholar]
  22. Mege J. L., Pouget J., Capo C., Andre P., Benoliel A. M., Serratrice G., Bongrand P. Myotonic dystrophy: defective oxidative burst of polymorphonuclear leukocytes. J Leukoc Biol. 1988 Sep;44(3):180–186. doi: 10.1002/jlb.44.3.180. [DOI] [PubMed] [Google Scholar]
  23. Moore K. L., Varki A., McEver R. P. GMP-140 binds to a glycoprotein receptor on human neutrophils: evidence for a lectin-like interaction. J Cell Biol. 1991 Feb;112(3):491–499. doi: 10.1083/jcb.112.3.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rothstein T. L., Mage M., Jones G., McHugh L. L. Cytotoxic T lymphocyte sequential killing of immobilized allogeneic tumor target cells measured by time-lapse microcinematography. J Immunol. 1978 Nov;121(5):1652–1656. [PubMed] [Google Scholar]
  25. Springer T. A. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. doi: 10.1038/346425a0. [DOI] [PubMed] [Google Scholar]
  26. Tha S. P., Shuster J., Goldsmith H. L. Interaction forces between red cells agglutinated by antibody. II. Measurement of hydrodynamic force of breakup. Biophys J. 1986 Dec;50(6):1117–1126. doi: 10.1016/S0006-3495(86)83556-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tissot O., Pierres A., Foa C., Delaage M., Bongrand P. Motion of cells sedimenting on a solid surface in a laminar shear flow. Biophys J. 1992 Jan;61(1):204–215. doi: 10.1016/S0006-3495(92)81827-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tözeren A., Ley K. How do selectins mediate leukocyte rolling in venules? Biophys J. 1992 Sep;63(3):700–709. doi: 10.1016/S0006-3495(92)81660-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wattenbarger M. R., Graves D. J., Lauffenburger D. A. Specific adhesion of glycophorin liposomes to a lectin surface in shear flow. Biophys J. 1990 Apr;57(4):765–777. doi: 10.1016/S0006-3495(90)82597-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zhu D. Z., Cheng C. F., Pauli B. U. Mediation of lung metastasis of murine melanomas by a lung-specific endothelial cell adhesion molecule. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9568–9572. doi: 10.1073/pnas.88.21.9568. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES