Transport governs flow-enhanced cell tethering through L-selectin at threshold shear.

Flow-enhanced cell adhesion is a counterintuitive phenomenon that has been observed in several biological systems. Flow augments L-selectin-dependent adhesion by increasing the initial tethering of leukocytes to vascular surfaces and by strengthening their subsequent rolling interactions. Tethering or rolling might be influenced by physical factors that affect the formation or dissociation of selectin-ligand bonds. We recently demonstrated that flow enhanced rolling of L-selectin-bearing microspheres or neutrophils on P-selectin glycoprotein ligand-1 by force decreased bond dissociation. Here, we show that flow augmented tethering of these microspheres or cells to P-selectin glycoprotein ligand-1 by three transport mechanisms that increased bond formation: sliding of the sphere bottom on the surface, Brownian motion, and molecular diffusion. These results elucidate the mechanisms for flow-enhanced tethering through L-selectin.

[1]  Cheng Zhu,et al.  Two-dimensional Kinetics Regulation of αLβ2-ICAM-1 Interaction by Conformational Changes of the αL-Inserted Domain* , 2005, Journal of Biological Chemistry.

[2]  M. U. Nollert,et al.  Tyrosine replacement in P-selectin glycoprotein ligand-1 affects distinct kinetic and mechanical properties of bonds with P- and L-selectin. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Scott L Diamond,et al.  Alterations in the intrinsic properties of the GPIbalpha-VWF tether bond define the kinetics of the platelet-type von Willebrand disease mutation, Gly233Val. , 2003, Blood.

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

[5]  D. Hammer,et al.  Kinetics of adhesion of IgE-sensitized rat basophilic leukemia cells to surface-immobilized antigen in Couette flow. , 1998, Biophysical journal.

[6]  Cheng Zhu,et al.  Distinct molecular and cellular contributions to stabilizing selectin-mediated rolling under flow , 2002, The Journal of cell biology.

[7]  P. Selvaraj,et al.  Quantifying the Impact of Membrane Microtopology on Effective Two-dimensional Affinity* 210 , 2001, The Journal of Biological Chemistry.

[8]  Ariel Solomon,et al.  Avidity enhancement of L-selectin bonds by flow , 2003, The Journal of cell biology.

[9]  Timothy A. Springer,et al.  The Kinetics of L-selectin Tethers and the Mechanics of Selectin-mediated Rolling , 1997, The Journal of cell biology.

[10]  T. Springer,et al.  Quantitation of L-selectin distribution on human leukocyte microvilli by immunogold labeling and electron microscopy. , 1996, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

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

[12]  Eric J. Kunkel,et al.  Threshold Levels of Fluid Shear Promote Leukocyte Adhesion through Selectins (CD62L,P,E) , 1997, The Journal of cell biology.

[13]  M. U. Nollert,et al.  Dimerization of a selectin and its ligand stabilizes cell rolling and enhances tether strength in shear flow , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Cheng Zhu,et al.  Quantifying the Effects of Molecular Orientation and Length on Two-dimensional Receptor-Ligand Binding Kinetics* , 2004, Journal of Biological Chemistry.

[15]  Cheng Zhu,et al.  Direct observation of catch bonds involving cell-adhesion molecules , 2003, Nature.

[16]  P Bongrand,et al.  Diffusion of microspheres in shear flow near a wall: use to measure binding rates between attached molecules. , 2001, Biophysical journal.

[17]  R. McEver.  Selectins: lectins that initiate cell adhesion under flow. , 2002, Current opinion in cell biology.

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

[19]  A. Barclay,et al.  Affinity and Kinetic Analysis of L-selectin (CD62L) Binding to Glycosylation-dependent Cell-adhesion Molecule-1* , 1998, The Journal of Biological Chemistry.

[20]  Brian Savage,et al.  Initiation of Platelet Adhesion by Arrest onto Fibrinogen or Translocation on von Willebrand Factor , 1996, Cell.

[21]  E. Evans.  Probing the relation between force--lifetime--and chemistry in single molecular bonds. , 2001, Annual review of biophysics and biomolecular structure.

[22]  C. Zhu,et al.  Measuring two-dimensional receptor-ligand binding kinetics by micropipette. , 1998, Biophysical journal.

[23]  D. Vestweber,et al.  Mechanisms that regulate the function of the selectins and their ligands. , 1999, Physiological reviews.

[24]  J. Happel,et al.  Low Reynolds number hydrodynamics , 1965 .

[25]  Timothy A. Springer,et al.  An Automatic Braking System That Stabilizes Leukocyte Rolling by an Increase in Selectin Bond Number with Shear , 1999, The Journal of cell biology.

[26]  Cheng Zhu,et al.  Catch bonds govern adhesion through L-selectin at threshold shear , 2004, The Journal of cell biology.

[27]  Cheng Zhu,et al.  Kinetic Measurements of Cell Surface E-Selectin/Carbohydrate Ligand Interactions , 2001, Annals of Biomedical Engineering.

[28]  Jizhong Lou,et al.  Flow-enhanced adhesion regulated by a selectin interdomain hinge , 2006, The Journal of cell biology.

[29]  Viola Vogel,et al.  Bacterial Adhesion to Target Cells Enhanced by Shear Force , 2002, Cell.

[30]  Scott L. Diamond,et al.  Direct Observation of Membrane Tethers Formed during Neutrophil Attachment to Platelets or P-Selectin under Physiological Flow , 2000, The Journal of cell biology.

[31]  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.

[32]  Cheng Zhu,et al.  Low Force Decelerates L-selectin Dissociation from P-selectin Glycoprotein Ligand-1 and Endoglycan* , 2004, Journal of Biological Chemistry.

[33]  R P McEver,et al.  Adhesive Interactions of Leukocytes, Platelets, and the Vessel Wall during Hemostasis and Inflammation , 2001, Thrombosis and Haemostasis.

[34]  P. Selvaraj,et al.  The Membrane Anchor Influences Ligand Binding Two-dimensional Kinetic Rates and Three-dimensional Affinity of FcγRIII (CD16)* , 2000, The Journal of Biological Chemistry.

[35]  T. Springer,et al.  Selectin receptor-ligand bonds: Formation limited by shear rate and dissociation governed by the Bell model. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  P. Bongrand,et al.  Determination of binding strength and kinetics of binding initiation , 1986, Cell Biophysics.