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. 2001 Aug;81(2):799–813. doi: 10.1016/S0006-3495(01)75742-6

Multiparticle adhesive dynamics. Interactions between stably rolling cells.

M R King 1, D A Hammer 1
PMCID: PMC1301554  PMID: 11463626

Abstract

A novel numerical simulation of adhesive particles (cells) reversibly interacting with an adhesive surface under flow is presented. Particle--particle and particle--wall hydrodynamic interactions in low Reynolds number Couette flow are calculated using a boundary element method that solves an integral representation of the Stokes equation. Molecular bonds between surfaces are modeled as linear springs and stochastically formed and broken according to postulated descriptions of force-dependent kinetics. The resulting simulation, Multiparticle Adhesive Dynamics, is applied to the problem of selectin-mediated rolling of hard spheres coated with leukocyte adhesion molecules (cell-free system). Simulation results are compared to flow chamber experiments performed with carbohydrate-coated spherical beads rolling on P-selectin. Good agreement is found between theory and experiment, with the main observation being a decrease in rolling velocity with increasing concentration of rolling cells or increasing proximity between rolling cells. Pause times are found to increase and deviation motion is found to decrease as pairs of rolling cells become closer together or align with the flow.

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Selected References

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

  1. Alon R., Hammer D. A., Springer T. A. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature. 1995 Apr 6;374(6522):539–542. doi: 10.1038/374539a0. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Bevilacqua M. P., Nelson R. M., Mannori G., Cecconi O. Endothelial-leukocyte adhesion molecules in human disease. Annu Rev Med. 1994;45:361–378. doi: 10.1146/annurev.med.45.1.361. [DOI] [PubMed] [Google Scholar]
  5. Brunk D. K., Goetz D. J., Hammer D. A. Sialyl Lewis(x)/E-selectin-mediated rolling in a cell-free system. Biophys J. 1996 Nov;71(5):2902–2907. doi: 10.1016/S0006-3495(96)79487-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brunk D. K., Hammer D. A. Quantifying rolling adhesion with a cell-free assay: E-selectin and its carbohydrate ligands. Biophys J. 1997 Jun;72(6):2820–2833. doi: 10.1016/S0006-3495(97)78924-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bullard D. C., Kunkel E. J., Kubo H., Hicks M. J., Lorenzo I., Doyle N. A., Doerschuk C. M., Ley K., Beaudet A. L. Infectious susceptibility and severe deficiency of leukocyte rolling and recruitment in E-selectin and P-selectin double mutant mice. J Exp Med. 1996 May 1;183(5):2329–2336. doi: 10.1084/jem.183.5.2329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chang K. C., Hammer D. A. Adhesive dynamics simulations of sialyl-Lewis(x)/E-selectin-mediated rolling in a cell-free system. Biophys J. 2000 Oct;79(4):1891–1902. doi: 10.1016/S0006-3495(00)76439-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chang K. C., Hammer D. A. The forward rate of binding of surface-tethered reactants: effect of relative motion between two surfaces. Biophys J. 1999 Mar;76(3):1280–1292. doi: 10.1016/S0006-3495(99)77291-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chang K. C., Tees D. F., Hammer D. A. The state diagram for cell adhesion under flow: leukocyte rolling and firm adhesion. Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11262–11267. doi: 10.1073/pnas.200240897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Damiano E. R., Westheider J., Tözeren A., Ley K. Variation in the velocity, deformation, and adhesion energy density of leukocytes rolling within venules. Circ Res. 1996 Dec;79(6):1122–1130. doi: 10.1161/01.res.79.6.1122. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Ebnet K., Vestweber D. Molecular mechanisms that control leukocyte extravasation: the selectins and the chemokines. Histochem Cell Biol. 1999 Jul;112(1):1–23. doi: 10.1007/s004180050387. [DOI] [PubMed] [Google Scholar]
  14. Evans E., Ritchie K. Dynamic strength of molecular adhesion bonds. Biophys J. 1997 Apr;72(4):1541–1555. doi: 10.1016/S0006-3495(97)78802-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Finger E. B., Puri K. D., Alon R., Lawrence M. B., von Andrian U. H., Springer T. A. Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature. 1996 Jan 18;379(6562):266–269. doi: 10.1038/379266a0. [DOI] [PubMed] [Google Scholar]
  16. Goetz D. J., el-Sabban M. E., Pauli B. U., Hammer D. A. Dynamics of neutrophil rolling over stimulated endothelium in vitro. Biophys J. 1994 Jun;66(6):2202–2209. doi: 10.1016/S0006-3495(94)81016-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Goldsmith H. L., Spain S. Margination of leukocytes in blood flow through small tubes. Microvasc Res. 1984 Mar;27(2):204–222. doi: 10.1016/0026-2862(84)90054-2. [DOI] [PubMed] [Google Scholar]
  18. Greenberg A. W., Brunk D. K., Hammer D. A. Cell-free rolling mediated by L-selectin and sialyl Lewis(x) reveals the shear threshold effect. Biophys J. 2000 Nov;79(5):2391–2402. doi: 10.1016/S0006-3495(00)76484-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Kunkel E. J., Chomas J. E., Ley K. Role of primary and secondary capture for leukocyte accumulation in vivo. Circ Res. 1998 Jan 9;82(1):30–38. doi: 10.1161/01.res.82.1.30. [DOI] [PubMed] [Google Scholar]
  21. Lasky L. A. Selectin-carbohydrate interactions and the initiation of the inflammatory response. Annu Rev Biochem. 1995;64:113–139. doi: 10.1146/annurev.bi.64.070195.000553. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Lipowsky H. H., Riedel D., Shi G. S. In vivo mechanical properties of leukocytes during adhesion to venular endothelium. Biorheology. 1991;28(1-2):53–64. doi: 10.3233/bir-1991-281-206. [DOI] [PubMed] [Google Scholar]
  24. Melder R. J., Yuan J., Munn L. L., Jain R. K. Erythrocytes enhance lymphocyte rolling and arrest in vivo. Microvasc Res. 2000 Mar;59(2):316–322. doi: 10.1006/mvre.1999.2223. [DOI] [PubMed] [Google Scholar]
  25. Munn L. L., Melder R. J., Jain R. K. Role of erythrocytes in leukocyte-endothelial interactions: mathematical model and experimental validation. Biophys J. 1996 Jul;71(1):466–478. doi: 10.1016/S0006-3495(96)79248-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rodgers S. D., Camphausen R. T., Hammer D. A. Sialyl Lewis(x)-mediated, PSGL-1-independent rolling adhesion on P-selectin. Biophys J. 2000 Aug;79(2):694–706. doi: 10.1016/S0006-3495(00)76328-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Simon S. I., Hu Y., Vestweber D., Smith C. W. Neutrophil tethering on E-selectin activates beta 2 integrin binding to ICAM-1 through a mitogen-activated protein kinase signal transduction pathway. J Immunol. 2000 Apr 15;164(8):4348–4358. doi: 10.4049/jimmunol.164.8.4348. [DOI] [PubMed] [Google Scholar]
  28. Smith M. J., Berg E. L., Lawrence M. B. A direct comparison of selectin-mediated transient, adhesive events using high temporal resolution. Biophys J. 1999 Dec;77(6):3371–3383. doi: 10.1016/S0006-3495(99)77169-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

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