Multiparticle adhesive dynamics. Interactions between stably rolling cells.

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.

[1]  D. Torney,et al.  The reaction-limited kinetics of membrane-to-surface adhesion and detachment , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  R K Jain,et al.  Role of erythrocytes in leukocyte-endothelial interactions: mathematical model and experimental validation. , 1996, Biophysical journal.

[3]  G. B. Jeffery On the Steady Rotation of a Solid of Revolution in a Viscous Fluid , 1915 .

[4]  Sangtae Kim,et al.  Microhydrodynamics: Principles and Selected Applications , 1991 .

[5]  D. Hammer,et al.  Sialyl Lewis(x)-mediated, PSGL-1-independent rolling adhesion on P-selectin. , 2000, Biophysical journal.

[6]  D. Hammer,et al.  Sialyl Lewis(x)/E-selectin-mediated rolling in a cell-free system. , 1996, Biophysical journal.

[7]  H. Goldsmith,et al.  Margination of leukocytes in blood flow through small tubes. , 1984, Microvascular research.

[8]  D. Hammer,et al.  Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow , 1995, Nature.

[9]  E. Kunkel,et al.  Role of primary and secondary capture for leukocyte accumulation in vivo. , 1998, Circulation research.

[10]  E L Berg,et al.  A direct comparison of selectin-mediated transient, adhesive events using high temporal resolution. , 1999, Biophysical journal.

[11]  M. Bevilacqua,et al.  Endothelial-leukocyte adhesion molecules in human disease. , 1994, Annual review of medicine.

[12]  P Bongrand,et al.  Cell adhesion. Competition between nonspecific repulsion and specific bonding. , 1984, Biophysical journal.

[13]  D. Hammer,et al.  Cell-free rolling mediated by L-selectin and sialyl Lewis(x) reveals the shear threshold effect. , 2000, Biophysical journal.

[14]  D. Hammer,et al.  The state diagram for cell adhesion under flow: leukocyte rolling and firm adhesion. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Timothy A. Springer,et al.  Adhesion through L-selectin requires a threshold hydrodynamic shear , 1996, Nature.

[16]  S. G. Mason,et al.  The microrheology of colloidal dispersions: XIII. Trajectories of orthokinetic pair collisions of latex spheres in a cationic polyelectrolyte , 1981 .

[17]  A. Beaudet,et al.  Infectious susceptibility and severe deficiency of leukocyte rolling and recruitment in E-selectin and P-selectin double mutant mice , 1996, The Journal of experimental medicine.

[18]  R. G. Cox,et al.  Slow viscous motion of a sphere parallel to a plane wall , 1967 .

[19]  C. Pozrikidis,et al.  Regular Article: A Spectral-Element Method for Particulate Stokes Flow , 1999 .

[20]  T. Springer,et al.  Leukocytes roll on a selectin at physiologic flow rates: Distinction from and prerequisite for adhesion through integrins , 1991, Cell.

[21]  S. Simon,et al.  Neutrophil Tethering on E-Selectin Activates β2 Integrin Binding to ICAM-1 Through a Mitogen-Activated Protein Kinase Signal Transduction Pathway1 , 2000, The Journal of Immunology.

[22]  D. Hammer,et al.  Adhesive dynamics simulations of sialyl-Lewis(x)/E-selectin-mediated rolling in a cell-free system. , 2000, Biophysical journal.

[23]  D. Vestweber,et al.  Molecular mechanisms that control leukocyte extravasation: the selectins and the chemokines. , 1999, Histochemistry and cell biology.

[24]  J. Sherwood,et al.  Stokesian dynamics simulations of particle trajectories near a plane , 1991 .

[25]  H. H. Lipowsky,et al.  In vivo mechanical properties of leukocytes during adhesion to venular endothelium. , 1991, Biorheology.

[26]  R. G. Cox,et al.  Slow viscous motion of a sphere parallel to a plane wall—I Motion through a quiescent fluid , 1967 .

[27]  K. Ley,et al.  Variation in the velocity, deformation, and adhesion energy density of leukocytes rolling within venules. , 1996, Circulation research.

[28]  E. Evans,et al.  Dynamic strength of molecular adhesion bonds. , 1997, Biophysical journal.

[29]  D. A. Hammer,et al.  Quantifying rolling adhesion with a cell-free assay: E-selectin and its carbohydrate ligands. , 1997, Biophysical journal.

[30]  S. G. Mason,et al.  The microrheology of colloidal dispersions. IX. Effects of simple and polyelectrolytes on rotation of doublets of spheres , 1979 .

[31]  H. Brenner The slow motion of a sphere through a viscous fluid towards a plane surface , 1961 .

[32]  N. Phan-Thien,et al.  Completed double layer in half-space: a boundary element method , 1992 .

[33]  R. Jain,et al.  Erythrocytes enhance lymphocyte rolling and arrest in vivo. , 2000, Microvascular research.

[34]  G. I. Bell Models for the specific adhesion of cells to cells. , 1978, Science.

[35]  M. El-Sabban,et al.  Dynamics of neutrophil rolling over stimulated endothelium in vitro. , 1994, Biophysical journal.

[36]  L. Lasky Selectin-carbohydrate interactions and the initiation of the inflammatory response. , 1995, Annual review of biochemistry.

[37]  D. Hammer,et al.  Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow , 1995, Nature.

[38]  D. Hammer,et al.  The forward rate of binding of surface-tethered reactants: effect of relative motion between two surfaces. , 1999, Biophysical journal.

[39]  D. Hammer,et al.  Sialyl LewisX-Mediated, PSGL-1-Independent RollingAdhesion on P-selectin , 2000 .

[40]  D. Hammer,et al.  Simulation of cell rolling and adhesion on surfaces in shear flow: general results and analysis of selectin-mediated neutrophil adhesion. , 1992 .