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* Institute for Medicine and Engineering, Department of Bioengineering, and Department of Chemical and Biomolecular Engineering, University of Pennsylvania, Philadelphia, Pennsylvania 19104; and Department of Biomedical Engineering, University of Virginia, Charlottesville, Virginia 22908
Correspondence: Address reprint requests to Scott L. Diamond, Institute for Medicine and Engineering, Depts. of Bioengineering and Chemical and Biomolecular Engineering, 1024 Vagelos Research Laboratory, University of Pennsylvania, Philadelphia PA 19104. Tel.: 215-573-5702; Fax: 215-573-7227; E-mail: sld{at}seas.upenn.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONEXPERIMENTAL PROCEDURESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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) of flowing neutrophils with preadhered neutrophils on intercellular adhesion molecule-1 (ICAM-1) or fibrinogen also displayed a maximum of 
0.4–0.45 at a wall shear rate of 100 s–1, an example of thresholding. Primary collision lifetime with no detectable bonding decreased from 130 to 10 ms as wall shear rate increased from 30 to 300 s–1, whereas collision lifetimes with bonding decreased from 300 to 100 ms over this shear range using preadhered neutrophils on ICAM-1, with similar results for fibrinogen. Antibodies against L-selectin, but not against CD11a, CD11b, or CD18, reduced at 100 s–1 by >85%. High resolution imaging detected large scale deformation of the flowing neutrophil during the collision at 100 s–1 with the apparent contact area increasing up to 40 µm2. We observed the formation of long linear string assemblies of neutrophils downstream of neutrophils preadhered to ICAM-1, but not fibrinogen, with a maximum in string formation at 100 s–1. Secondary capture events to the ICAM-1 or fibrinogen coated surfaces after primary collisions were infrequent and short lived, typically lasting from 500 to 3500 ms. Between 5 and 20% of neutrophil interactions with ICAM-1 substrate converted to firm arrest (>3500 ms) and greatly exceeded that observed for fibrinogen, thus defining the root cause of poor string formation on fibrinogen at all shear rates. Additionally, neutrophils mobilized calcium after incorporation into strings. Static adhesion also caused calcium mobilization, as did the subsequent onset of flow. To our knowledge, this is the first report of 1), hydrodynamic thresholding in neutrophil string formation; 2), string formation on ICAM-1 but not on fibrinogen; 3), large cellular deformation due to collisions at a venous shear rate; and 4), mechanosensing through neutrophil ß2-integrin/adhesion. The increased contact area during deformation was likely responsible for the hydrodynamic threshold observed in the primary collision efficiency since no increase in primary collision lifetime was detected as shear forces were increased (for either surface coating). |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONEXPERIMENTAL PROCEDURESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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), whereas the ß2-integrins CD11a/CD18 (leukocyte function-associated antigen-1, LFA-1) and CD11b/CD18 (Mac-1) mediate firm adhesion to endothelial cells, neutrophils, or platelets. Adherent neutrophils can form long linear assemblies (strings) in the direction of flow under in vitro conditions (Lawrence and Springer, 1991; Alon et al., 1996) or on atherosclerotic plaques in vivo (Eriksson et al., 2001).
During neutrophil homotypic interactions, rapid P-selectin ligand glycoprotein-1 (PSGL-1)/L-selectin bond formation mediates capture followed by binding via LFA-1/intercellular adhesion molecule-3 (ICAM-3) and Mac-1/Mac-1 ligand(s) (Taylor et al., 1996; Lynam et al., 1998). Neutrophil LFA-1 also binds ICAM-1 on inflamed endothelium. Mac-1 is a more promiscuous integrin; known ligands include fibrinogen, as well as other less defined ligands on the platelet, neutrophil, and endothelium. The PSGL-1/L-selectin interaction obeys the Bell model for rigid beads {koff = 1.54 s–1 exp(0.037 nm FB/kBT) for 50 < FB < 250 pN} and fixed neutrophils with 0.25 µm nonextending microvilli (Park et al., 2002). However, deformable unfixed neutrophils deviate from Bell model behavior at FB > 100–150 pN (Park et al., 2002) most likely due to microvilli extension (Shao et al., 1998; Schmidtke and Diamond, 2000).
In several circumstances, neutrophil adhesion can display unexpectedly increased adhesiveness in the presence of increasing force loading. This diverse set of observations with neutrophils include single cell and population measurements: 1), a threshold requirement for shear stress to facilitate rolling on selectins (Lawrence et al., 1997; Finger et al., 1996); 2), increase in rolling flux as shear rate is increased in vivo (Lawrence et al., 1997) and in vitro (Greenberg et al., 2000); 3), stable rolling of individual cells under flow that destabilizes when flow stops (Lawrence et al., 1997); 4), increased collision efficiency during homotypic aggregation of N-formyl-L-methionyl-L-leucyl-L-phenylalanine (fMLP)-activated neutrophils (Taylor et al., 1996); 5) flow-induced aggregation of resting neutrophils in suspension that deaggregate upon cessation of flow (Goldsmith et al., 2001); and 6), a plateauing in rolling velocity as wall shear rate is continually increased (Lawrence and Springer, 1993; Chen and Springer, 1999). Multiple mechanisms at the cellular and/or molecular level may underlie these distinct observations. In general, hydrodynamic thresholding refers to a biphasic adhesion phenomenon that displays an increase in adhesion with force loading followed by a decrease in adhesion as forces become exceedingly high. In this work, we reserve the term thresholding as a description of macroscopic systems that display force-enhanced adhesion. Relating macroscopic cellular observations to underlying molecular phenomena often requires the titration of receptor densities to limiting dilutions and various consistency tests of the discrete event data sets (Zhu et al., 2002). Thresholding is also seen for the platelet glycoproteinIb/von Willebrand factor (GPIb/vWF) A1 interaction, a bond with a high zero-stress off-rate (koff(0) = 3.45 s–1) with a reactive compliance (
= 0.06 nm) that is strictly positive for 36 < FB <145 pN (Doggett et al., 2002), as it is for selectins.
Hydrodynamic thresholding can be viewed as the net effect of force loading and convection on processes that modulate bond formation and processes that modulate bond disruption over a regime of increasing hydrodynamic flow. The rolling dynamics of neutrophils can also be influenced by membrane tether pulling that shields bonds from force loading (Schmidtke and Diamond, 2000; Park et al., 2002) or by cellular deformation that enhances the rolling contact area (Lei et al., 1999). Interestingly, membrane tether formation on P-selectin (Schmidtke and Diamond, 2000) occurs over the same shear rate regime as hydrodynamic thresholding (Lawrence et al., 1997). Although tangential convection of surfaces relative to each other (Chang and Hammer, 1999) may enhance the overall on-rate (kon) during capture of a flowing cell or bead, it remains unstudied the contribution of this mechanism during stable rolling after the velocity of the neutrophil has decreased considerably from its free stream velocity. Normal convective effects may also occur as the bonds at the tailing edge of the contact area facilitate compression at the leading edge of new membrane normal to the wall. Although living neutrophils are very soft and deformable in rolling assays, thresholding has also been observed in a bead system (Greenberg et al., 2000). Laboratory observations of polystyrene bead deformation at forces as low as 40 pN preclude strict conclusions about the role of deformation during bead thresholding. Even the flow-enhanced angular rotation of a cell or rigid bead around a single bond of finite length may facilitate the formation of the next bond, via a normal convective mechanism as a receptor moves closer to the surface. Chen and Springer (1999) developed a Monte Carlo simulation that predicted an increase in bond number with an increase in shear and also calculated the shear threshold below which rolling would not be seen in the system. This shear threshold was calculated to be 0.4–0.8 dyne/cm2 for neutrophil rolling on peripheral lymph node addressin (PNAd), which compares well with the observed value of 0.4–0.5 dyne/cm2.
Another hallmark of neutrophil rolling interactions in parallel-plate chambers is the formation of string assemblies of neutrophils. Linear strings of adherent neutrophils in the direction of shear flow have been visualized for neutrophil rolling on P-selectin, E-selectin, and human umbilical vein endothelial cells (HUVECs), as well as in vivo on mouse atherosclerotic lesions. Treatment of neutrophils with antibodies blocking either L-selectin or PSGL-1 block the formation of strings in vitro, indicating that the formation of strings depends upon homotypic neutrophil interactions.
Since the collision of flowing neutrophils with adherent neutrophils provides experimental advantages unique to both rolling assays (good visualization) and aggregation assays (discrete collisions), we used high speed, high resolution videomicroscopy to probe these events. This assay may help in the determination of receptor dynamics and capture probabilities during assembly processes in inflammation and thrombosis.
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EXPERIMENTAL PROCEDURES |
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Cell isolation
Human blood was obtained via venipuncture from healthy adult donors and was mixed with anticoagulant sodium citrate (nine parts blood/one part citrate). Neutrophils were isolated by centrifugation with a separation medium (Robbins Scientific, Sunnyvale, CA) as previously described (Schmidtke and Diamond, 2000; Goel and Diamond, 2001). Neutrophils were counted and diluted with a 2% solution of human serum albumin in HBS to a final concentration of 106 cells/ml. The suspension buffer of sterile HBS (Invitrogen, Carlsbad, CA; manufacturer specification of low endotoxin, <10 endotoxin units/ml) was used for all perfusion studies. For cells labeled with calcium-sensitive dye, cells were incubated for 20 min with Fluo-4 (9.1 µM) before dilution. In some experiments, cells were preincubated for 20 min with 20 µg/ml mAb before perfusion.
Microcapillary flow chambers and imaging
Rectangular glass capillaries (Vitrocom, Mountain Lakes, NJ) having a cross section of 0.2 x 2.0 mm, a length of 7 cm, and a wall thickness of 0.15 mm were used as flow chambers, as described previously (Schmidtke and Diamond, 2000; Goel and Diamond, 2001). Chambers were incubated with recombinant human ICAM-1 (1 µg/ml) or fibrinogen (100 µg/ml) for 120 min at room temperature and rinsed with HBS for 10 min. Neutrophils were perfused into the chambers using a syringe pump (Harvard Apparatus, South Natick, MA) and then preadhered for 10 min under static conditions. The wall shear stress (
w) upon the surface of the chamber was calculated from the solution of the Navier-Stokes equation for laminar flow of a Newtonian fluid: w = (6Qµ)/(B2W), where Q represents the flow rate (cm3/s), µ is the viscosity (0.01 Poise at room temperature), B is the total plate separation (0.02 cm), and W is the width (0.2 cm). The wall shear rate, 
w, is calculated from w = 6Q/B2W. For differential interference contrast (DIC) microscopy, a Zeiss Axiovert 135 microscope (Thornwood, NY) with a 63x (NA 1.40) oil immersion objective lens (Plan Apochromate) was used. For experiments where fluorescence imaging was needed, a GenIISys focused image intensifier charge-coupled device (DAGE-MTI, Michigan City, IN) was attached to the microscope. For high speed, high resolution studies, images were captured using a MotionCorder Analyzer high speed digital camera (Eastman Kodak, Rochester, NY) at an imaging rate of 240 frames per second (fps). The images were played back at 5 fps or frame-by-frame to videotape for analysis.
Analysis of neutrophil rolling and adhesion
When unstimulated neutrophils were perfused over neutrophils adherent to ICAM-1 or fibrinogen-coated surfaces, two different types of interactions occurred: collisions with the attached cells and subsequent collision with the surface (Fig. 1). In a primary collision, the flowing neutrophil collided with and rolled over an adherent neutrophil. In the absence of observable binding (acute reductions in motion or a pause before escape), the interaction time from arrival to departure fell within a narrow, hydrodynamically expected range with the approach and escape velocity being essentially the same. Cells that had collisions lasting longer than this range that also had detectable pauses before escape were scored as adhesive interactions. The ratio of adhesive collisions to total collisions was defined as the primary collision efficiency. This efficiency is not the same as used in bulk aggregation studies analyzed with population balances (Taylor et al., 1996; Tandon and Diamond, 1998). Binding events lasting <5 ms cannot be distinguished from hydrodynamic interactions at 240 fps and therefore were not binned as adhesive interactions. Thus, the measured value of represents a minimal estimate of bonding at 63x and 240 fps. For flowing cells that made bonds during the primary collision (detectable pause before escape) and had a detectable secondary interaction with the surface (2°), we then measured the lifetime of this secondary interaction (Fig. 1). Cells with no detectable bonding during the primary collision had exceedingly low capture probability downstream of the primary target cell, as expected from L-selectin and PSGL-1 antibody experiments that greatly reduce string formation (Alon et al., 1996). Of cells with a primary collision (with or without binding), the secondary capture efficiency (2°) was rather small (2° < 0.032 at 100 s–1), as expected for a surface lacking a selectin. Since 2° was so small in the absence of a selectin on the surface, it was not practical to measure this parameter. This low value of 2° was also consistent with poor cell capture by surfaces (ICAM-1 or fibrinogen) lacking preadherent neutrophils. Based on the histogram of 2° adhesion times, any neutrophil adhering to the surface for longer than 3.5 s was considered to be firmly adherent, and all such interactions were binned together. Likewise, interactions that lasted from 500 to 3500 ms were binned together as transient adhesions. Adhesions between 0 and 500 ms were binned as highly transient. A time of 500 ms was chosen as the cutoff between transient and highly transient events because 75% of the interactions observed lasted less than 500 ms, on average, over all the shear rates and surface coatings.
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RESULTS |
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) were calculated for interactions between flowing neutrophils and those adherent to ICAM-1 or fibrinogen for a range of wall shear rates (30–300 s–1). In addition, the average interaction times were measured for both primary and secondary interactions. A maximum in = 0.45 for ICAM-1 coated surfaces or = 0.40 for fibrinogen coated surfaces occurred for collisions with neutrophils at 100 s–1 (Fig. 2, A and B). More than 30 collisions were analyzed at each shear rate to allow a reasonable sampling of the upstream cross sectional area except on fibrinogen at 300 s–1. No successful collisions with binding were detectable at w = 400 s–1 (not shown), indicating that hydrodynamic interactions lasting under 5 ms produce no binding lasting longer than 5 ms. A cluster of several L-selectin/PSGL-1 bonds would be required for detection at 240 fps imaging at 400 s–1 when shear forces exceed 400 pN.
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w increased from 30 to 300 s–1 (Fig. 2, C and D). These values are considerably shorter than observed for transient capture of flowing neutrophils to adherent platelets via PSGL-1/P-selectin bonding (Schmidtke and Diamond, 2000). Multiple bonds are likely detected in neutrophil-neutrophil or neutrophil-platelet collisions observed under physiological conditions due to the abundance of the receptors on the cells, based on comparison with assays in which single bond interactions dominate. To identify receptors that contribute to the primary collision efficiencies, monoclonal antibodies against CD11a, CD11b, and CD18, as well as against CD62L (L-selectin), were incubated with neutrophils before efficiency studies (Fig. 3). The anti-CD18, CD11a, and CD11b antibodies had no significant effect on the primary collision efficiency. The mAb against CD62L significantly reduced the collision efficiency of the cells. These results indicate that L-selectin, but not the ß2-integrins, mediated the 100–300-ms bonding during collision of neutrophils where both PSGL-1 and L-selectin were presented in their native membranes.
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) have pointed to the competing effects of deformation and increased shear as a reason for the shear thresholding effects seen in the neutrophil homotypic collision efficiency. Using high speed imaging at 100 s–1, the deformation of a flowing neutrophil during a collision with an ICAM-1 anchored neutrophil was clearly observed (Fig. 4). Within the first 20 ms of the collision, compression was detected. By 46 ms, the full development of an adhesive contact area had grown to 40 µm2 as the rolling cell experienced maximal shear. By the conclusion of the interaction at 221 ms, the contact area was reduced to less than 12 µm2 and the cell rebounded to a near spherical shape. For this off-center collision with both cells in a focal plane near the surface, the combination of adhesion and hydrodynamics caused large changes in cell shape even at 100 s–1. The rate of bond formation may increase due to a growth of the contact area and enhanced compression of the opposing membranes together.
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) was essentially the same for the two surfaces (Fig. 2, A and B).
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w 
30 s–1, indicating a hydrodynamic shear threshold for secondary capture of neutrophils to ICAM-1 and fibrinogen-coated surfaces lacking selectins. At w = 100 s–1, the average secondary interaction time was greater on ICAM-1 than fibrinogen (
= 850 ms for ICAM-1 vs. 330 ms for fibrinogen). Of those cells having any detectable secondary bonding interaction with ICAM-1, an increasing number from 5 to 20% achieved firm adhesion (>3500 ms) as w increased from 30 to 200 s–1, which is an additional instance of thresholding. Firm arrest to fibrinogen after primary collision was only sporadically detected and represented the root cause of poor string formation on fibrinogen. This suggests that LFA-1 and Mac-1 bind ICAM-1 faster than Mac-1 can bind fibrinogen. No firm adhesion lasting >3500 s was detected on either surface at w = 300 s–1.
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= 2.68 ± 0.77) was closer to the center line (y = 0) of the adherent cell, whereas there was no migration toward the center line after release for nonbonding cells ( = 6.10 ± 1.24). This difference in release trajectories due to bonding may focus and facilitate string formation into linear chains as opposed to a more branched structure. Also, an asymmetry of approach and release trajectories was detected, potentially influenced by deformation in the cell membranes, especially in the case where bonds form between the interacting cells.
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in simulations of hard sphere collisions. The former case of asymmetry between adhesive cells appears to be a novel observation in this context. Also, for both adhesive and nonadhesive collisions the distribution of y values appears to be narrower after collision than before collision.
In a new observation, membrane tether formation was discovered in trajectory data at the termination of the collision where a cell translates without rotation at a steady and reduced velocity. Membrane tether formation between L-selectin and PSGL-1 was more pronounced at 200 than at 100 s–1. A tether forming event at a wall shear rate of 200 s–1 (Fig. 9 B) had a membrane extension rate of 11.7 µm/s for a 1.46-µm tether that grew for 100 ms. Tether initiation, elongation, and cell release is shown below the graph. The average tether life decreased as the wall shear rate was increased from 100 to 200 s–1 (= 487 and 250 ms, p < 0.05). The average tether length was 1.1 and 2.7 µm at 100 and 200 s–1, considerable shorter than those observed between PSGL-1 and P-selectin (Schmidtke and Diamond, 2000).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONEXPERIMENTAL PROCEDURESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Further analysis of secondary capture on ICAM-1 or fibrinogen demonstrated radically different dynamics (Fig. 6). The fraction of cells that exhibited either transient or firm adhesion to ICAM-1 was constant at 30% for shear rates between 30 and 300 s–1. In contrast, transient adhesion to the fibrinogen surface was only seen for limited shear rates (30–100 s–1), and the fraction adhering to fibrinogen was much lower than that seen on ICAM-1. Firm adhesive events (defined as events lasting longer than 3500 ms) on fibrinogen were only sporadic. Thus, the overall adhesiveness of neutrophils to a fibrinogen-coated surface is much less than that of an ICAM-1 coated surface. These results indicate that the strings of neutrophils seen on ICAM-1 are most likely the result of secondary interactions between ß2-integrins and ICAM-1.
An analysis of calcium activation profiles revealed that neutrophils activate during string formation and adhesion of cells to the surface (Fig. 7). Further analysis of calcium mobilization in the neutrophils revealed that cells activate upon application of a shear stress to adherent cells (Fig. 8). This activation is rapid upon initiation of fluid shear, and always less than the calcium response seen when the cells initially adhere to the surface.
Clearly, thresholding is most easily detected in systems with high off-rates (koff) such as detected for selectins and the GPIb/vWF A1 domain (Doggett et al., 2002) and in systems of low ligand density. It remains unclear to what extent hydrodynamic thresholding requires catch bonding, a positive reactive compliance in the Bell model over a portion of the force regime, as was recently detected by atomic force microscopy for monomeric and dimeric P-selectin/PSGL-1 bonds (Marshall et al., 2003). Neutrophil thresholding is best observed with rolling on L-selectin. Neutrophil rolling fluxes on L-selectin or PSGL-1 peak at 100 s–1 (Fbond 100 pN), whereas the peak bond lifetime for P-selectin/PSGL-1 detectable with atomic force microscopy occurs at a very lower force of 25 pN (Zhu et al., 2002) that already approaches hemodynamic conditions of stasis (<0.25 s–1) where rouloeaux formation would dominate any pathophysiology. The kon and koff values for L-selectin are generally viewed as being higher than those for P-selectin. This translates into better capture and faster rolling, in addition to a higher reactive compliance in rolling assays (Smith et al., 1999; Zhang and Neelamegham, 2002).
The two- to threefold increase in to a maximal value of 0.4 as w increased from 30 to 100 s–1 was consistent with the fourfold increase to 0.4 seen in bulk aggregation assays as increased from 100 to 400 s–1 (Taylor et al., 1996) since peak forces in our assay are greater and sustained in comparison to those for rotating doublets in a linear shear field (Tandon and Diamond, 1998). From flow chamber data and calculated cell fluxes to the adherent cell, Zhang and Neelamegham (2002) derived a cell-cell capture efficiency to be 0.2 at low shear rates (50 and 100 s–1), and 0.07 at 200 s–1, reasonable estimates for an ensemble average.
We found in our system that most neutrophils that experienced a secondary interaction attached to the ICAM-1 surface 1.5–2 cell diameters downstream from the initial adherent cell (data not shown) at 100 s–1. These results were obtained by measuring the distance between the center of the adherent cell and the outer edge of the rolling cell when it first forms an adhesive interaction with the chamber surface. This result differs from the results found by King et al. (2001), where they determined that sialyl Lewisx coated beads tended to attach to a P-selectin surface from four to five cell diameters downstream from an adherent sphere. However, there are some differences between the two systems. First, flowing sialyl Lewisx coated beads do not experience adhesive interactions with adhered beads. In our system, flowing neutrophils bond via PSGL-1/L-selectin during primary collisions. Second, in our system the neutrophils were captured to a surface that was essentially free of selectins, aside from any putative neutrophil microparticles that may be present on the surface. This low or near-zero concentration of surface-presented selectin reduces the overall adhesiveness of these surfaces to neutrophil adhesion.
In summary, we provide insight into the dynamics of neutrophil adhesion under various shear flow conditions. We have shown how ß2-integrins affect the formation of neutrophil strings, which have been observed in vivo and are therefore not an in vitro artifact as previously hypothesized (Kunkel et al., 1998). We also have demonstrated a shear threshold in neutrophil-neutrophil primary collisions, which may be caused by the subsecond deformation of neutrophils upon collision after L-selectin bond formation. Finally, calcium activation upon onset of shear stress for neutrophils adhering to an ICAM-1 surface indicates a role of ß2-integrins as mechanosensors. With a better understanding of neutrophil dynamics of adhesion and activation, and clarification of the roles of LFA-1, Mac-1, and L-selectin in these dynamics, both drug development and computer modeling for thrombosis and inflammation may be improved.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONEXPERIMENTAL PROCEDURESRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Submitted on October 9, 2003; accepted for publication January 30, 2004.
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REFERENCES |
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Chang, K. C., and D. A. Hammer. 1999. The forward rate of binding of surface-tethered reactants: effect of relative motion between two surfaces. Biophys. J. 76:1280–1292.
Chen, S., and T. A. Springer. 1999. An automatic braking system that stabilizes leukocyte rolling by an increase in selectin bond number with shear. J. Cell Biol. 144:185–200.
Doggett, T. A., G. Girdhar, A. Lawshe, D. W. Schmidtke, I. J. Laurenzi, S. L. Diamond, and T. G. Diacovo. 2002. Selectin-like kinetics and biomechanics promote rapid platelet adhesion in flow: the GPIb
-vWF tether bond. Biophys. J. 83:194–205.
Eriksson, E. E., X. Xie, J. Werr, P. Thoren, and L. Lindbom. 2001. Importance of primary capture and L-selectin-dependent secondary capture in leukocyte accumulation in inflammation and atherosclerosis in vivo. J. Exp. Med. 194:205–217.
Finger, E. B., K. D. Puri, R. Alon, M. B. Lawrence, U. H. von Adrian, and T. A. Springer. 1996. Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature. 379:266–269.[CrossRef][Medline]
Goel, M. S., and S. L. Diamond. 2001. Neutrophil enhancement of fibrin deposition under flow through platelet-dependent and -independent mechanisms. Arterioscler. Thromb. Vasc. Biol. 12:2093–2098.
Goldsmith, H. L., T. A. Quinn, G. Drury, C. Spanos, F. A. McIntosh, and S. I. Simon. 2001. Dynamics of neutrophil aggregation in Couette flow revealed by videomicroscopy: effect of shear rate on two-body collision efficiency and doublet lifetime. Biophys. J. 81:2020–2034.
Greenberg, A. W., D. K. Brunk, and D. A. Hammer. 2000. Cell-free rolling mediated by L-selectin and sialyl Lewis(x) reveals the shear threshold effect. Biophys. J. 79:2391–2402.
Guyer, D. A., K. L. Moore, E. B. Lynam, C. M. G. Schammel, S. Rogelj, R. P. McEver, and L. A. Sklar. 1996. P-selectin glycoprotein ligand-1 (PSGL-1) is a ligand for L-selectin in neutrophil aggregation. Blood. 88:2415–2421.
King, M. R., and D. A. Hammer. 2001. Multiparticle adhesive dynamics: hydrodynamic recruitment of rolling leukocytes. Proc. Natl. Acad. Sci. USA. 98:14919–14924.
King, M. R., S. D. Rodgers, and D. A. Hammer. 2001. Hydrodynamic collisions suppress fluctuations in the rolling velocity of adhesive blood cells. Langmuir. 17:4139–4143.[CrossRef]
Kunkel, E. J., J. E. Chomas, and K. Ley. 1998. Role of primary and secondary capture for leukocyte accumulation in vivo. Circ. Res. 82:30–38.
Lawrence, M. B., G. S. Kansas, E. J. Kunkel, and K. Ley. 1997. Threshold levels of fluid shear promote leukocyte adhesion through selectins (CD62L,P,E). J. Cell Biol. 136:717–727.
Lawrence, M. B., and T. A. Springer. 1991. Leukocytes roll on a selectin at physiological flow-rates: distinction from and a prerequisite for adhesion through integrins. Cell. 65:859–873.[CrossRef][Medline]
Lawrence, M. B., and T. A. Springer. 1993. Neutrophils roll on E-selectin. J. Immunol. 151:6338–6346.[Abstract]
Lei, X., M. B. Lawrence, and C. Dong. 1999. Influence of cell deformation on leukocyte rolling adhesion in shear flow. J. Biomech. Eng. 121:636–643.[Medline]
Lynam, E., L. A. Sklar, A. D. Taylor, S. Neelamegham, B. S. Edwards, C. W. Smith, and S. I. Simon. 1998. ß2 integrins mediate stable adhesion in collisional interactions between neutrophils and ICAM-1 expressing cells. J. Leukoc. Biol. 62:622–630.
Marshall, B. T., M. Long, J. W. Piper, T. Yago, R. P. McEver, and C. Zhu. 2003. Direct observation of catch bonds involving cell-adhesion molecules. Nature. 423:190–193.[CrossRef][Medline]
Park, E. Y. H., M. J. Smith, E. S. Stropp, K. R. Snapp, J. A. DiVietro, W. F. Walker, D. W. Schmidtke, S. L. Diamond, and M. B. Lawrence. 2002. Comparison of PSGL-1 microbead and neutrophil rolling: microvillus elongation stabilizes P-selectin bond clusters. Biophys. J. 82:1835–1847.
Schmidtke, D. W., and S. L. Diamond. 2000. Direct observation of membrane tethers formed during neutrophil attachment to platelets or P-selectin under physiological flow. J. Cell Biol. 149:719–729.
Shao, J. Y., H. P. Ting-Bell, and R. M. Hochmuth. 1998. Static and dynamic lengths of neutrophil microvilli. Proc. Natl. Acad. Sci. USA. 95:6797–6802.
Smith, M. J., E. L. Berg, and M. B. Lawrence. 1999. A direct comparison of selectin-mediated, adhesive events using high temporal resolution. Biophys. J. 77:3371–3383.
Tandon, P., and S. L. Diamond. 1998. Kinetics of ß2-integrin and L-selectin binding during neutrophil aggregation in shear flow. Biophys. J. 75:3163–3178.
Taylor, A. D., S. Neelamegham, J. D. Hellums, C. W. Smith, and S. I. Simon. 1996. Molecular dynamics of the transition from L-selectin to ß2-integrin dependent neutrophil adhesion under defined hydrodynamic shear. Biophys. J. 71:3488–3500.
Zhang, Y., and S. Neelamegham. 2002. Estimating the efficiency of cell capture and arrest in flow chambers: study of neutrophil binding via E-selectin and ICAM-1. Biophys. J. 83:1934–1952.
Zhu, C., M. Long, S. E. Chesla, and P. Bongrand. 2002. Measuring receptor/ligand interaction at the single-bond level: experimental and interpretive issues. Ann. Biomed. Eng. 30:305–314.[CrossRef][Medline]
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