Catch bonds govern adhesion through L-selectin at threshold shear

Flow-enhanced cell adhesion is an unexplained phenomenon that might result from a transport-dependent increase in on-rates or a force-dependent decrease in off-rates of adhesive bonds. L-selectin requires a threshold shear to support leukocyte rolling on P-selectin glycoprotein ligand-1 (PSGL-1) and other vascular ligands. Low forces decrease L-selectin–PSGL-1 off-rates (catch bonds), whereas higher forces increase off-rates (slip bonds). We determined that a force-dependent decrease in off-rates dictated flow-enhanced rolling of L-selectin–bearing microspheres or neutrophils on PSGL-1. Catch bonds enabled increasing force to convert short-lived tethers into longer-lived tethers, which decreased rolling velocities and increased the regularity of rolling steps as shear rose from the threshold to an optimal value. As shear increased above the optimum, transitions to slip bonds shortened tether lifetimes, which increased rolling velocities and decreased rolling regularity. Thus, force-dependent alterations of bond lifetimes govern L-selectin–dependent cell adhesion below and above the shear optimum. These findings establish the first biological function for catch bonds as a mechanism for flow-enhanced cell adhesion.

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

[2]  R. Alon,et al.  Avidity enhancement of L-selectin bonds by flow , 2003, The Journal of cell biology.

[3]  Justin E. Molloy,et al.  Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers , 2003, Nature Cell Biology.

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

[5]  M. Shimaoka,et al.  Transition From Rolling to Firm Adhesion Is Regulated by the Conformation of the I Domain of the Integrin Lymphocyte Function-associated Antigen-1* , 2002, The Journal of Biological Chemistry.

[6]  K. Ley,et al.  Viscosity‐Independent Velocity of Neutrophils Rolling on P‐Selectin In Vitro or In Vivo , 2002, Microcirculation.

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

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

[9]  R. Isberg,et al.  Dancing with the Host Flow-Dependent Bacterial Adhesion , 2002, Cell.

[10]  Scott L. Diamond,et al.  Selectin-Like Kinetics and Biomechanics Promote Rapid Platelet Adhesion in Flow: The GPIbα-vWF Tether Bond , 2002 .

[11]  S. Diamond,et al.  Selectin-like kinetics and biomechanics promote rapid platelet adhesion in flow: the GPIb/spl alpha/-vWF tether bond , 2002, Proceedings of the Second Joint 24th Annual Conference and the Annual Fall Meeting of the Biomedical Engineering Society] [Engineering in Medicine and Biology.

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

[13]  William F Walker,et al.  Comparison of PSGL-1 microbead and neutrophil rolling: microvillus elongation stabilizes P-selectin bond clusters. , 2002, Biophysical journal.

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

[15]  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.

[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]  G. Truskey,et al.  Effect of contact time and force on monocyte adhesion to vascular endothelium. , 2001, Biophysical journal.

[18]  Evan Evans,et al.  Chemically distinct transition states govern rapid dissociation of single L-selectin bonds under force , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[19]  S. Weinbaum,et al.  Dynamic contact forces on leukocyte microvilli and their penetration of the endothelial glycocalyx. , 2001, Biophysical journal.

[20]  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.

[21]  C. Dong,et al.  Influence of cell deformation on leukocyte rolling adhesion in shear flow. , 1999, Journal of biomechanical engineering.

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

[23]  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.

[24]  Richard D. Cummings,et al.  Affinity and Kinetic Analysis of P-selectin Binding to P-selectin Glycoprotein Ligand-1* , 1998, The Journal of Biological Chemistry.

[25]  R M Hochmuth,et al.  Static and dynamic lengths of neutrophil microvilli. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Timothy A. Springer,et al.  Modifying the mechanical property and shear threshold of L-selectin adhesion independently of equilibrium properties , 1998, Nature.

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

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

[29]  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.

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

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

[32]  H. H. Lipowsky,et al.  Leukocyte margination and deformation in mesenteric venules of rat. , 1989, The American journal of physiology.

[33]  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.

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

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

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

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

[38]  P. Bongrand,et al.  Motion of cells sedimenting on a solid surface in a laminar shear flow. , 1992, Biophysical journal.