Article |
2 Department of Microbiology-Immunology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611
3 Max Planck Institute of Colloids and Interfaces, 14424 Potsdam, Germany
Address correspondence to Ronen Alon, Dept. of Immunology, Weizmann Institute of Science, Rehovot 76100, Israel. Tel.: 972-8-9342482. Fax: 972-8-9344141. email: ronalon{at}wicc.weizmann.ac.il
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key Words: selectin; rolling; lymph nodes; aggregation; shear flow
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Transient leukocyte tethers to low density ligands are the smallest adhesive events observable under shear flow (Alon et al., 1995a). Analyses on such quantal L-selectin tethers performed using regular videomicroscopy, i.e., at a 2030-ms resolution, revealed that below critical shear values, L-selectin fails to form functional tethers (Alon et al., 1997). This result sharply contrasted the ability of P- and E-selectins, as well as 4 integrins, to form functional tethers at any subphysiological shear stress tested or at stasis (Alon et al., 1997; de Chateau et al., 2001). This collapse of L-selectin tethering was hence postulated to reflect a unique mechanical property of the L-selectin bond (Puri et al., 1998; Dwir et al., 2000). The ability of L-selectin to form functional tethers was attributed to a critical force required to press the L-selectinexpressing cell onto the substrate and to overcome a repulsive barrier for binding to the selectin ligand (Chen and Springer, 1999). To elucidate the molecular basis of this shear dependence of quantal L-selectin tethers, the building units of L-selectinmediated adhesions, we analyzed L-selectinmediated interactions with low densities of native endothelial and leukocyte-derived ligands at a much higher temporal resolution than previously used to study the kinetics of quantal L-selectin tethers (Alon et al., 1997). Notably, at these shear stresses, both lymphocyte-based and cell-free L-selectin were found to form specific but exceptionally labile adhesive tethers, with lifetimes 30-fold shorter than that estimated from L-selectin tether analysis performed at low time resolution (Alon et al., 1997). Strikingly, these tethers appeared insensitive to increased shear stresses at a range of subthreshold shear rates. Above the threshold shear rate, stabilized tethers formed with up to 14-fold longer duration. This is an exceptional stabilization mechanism by which enhanced shear rate up-regulates L-selectin function.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
Mucin presentation and cellular environment do not alter the kinetic properties of L-selectincarbohydrate bonds
PNAd is comprised of largely extended mucin carriers of carbohydrate L-selectin ligands (Hemmerich and Rosen, 2000). Shear stress has been suggested to directly increase mucin recognition by L-selectin by overcoming a repulsive barrier between the selectin and its counter-receptor (Chen and Springer, 1999). Therefore, we studied the microkinetic properties of L-selectin tethers with a nonmucin ligand, a short L-selectinbinding sulfated sLex-decorated glycopeptide, derived from the major selectin recognition site on PSGL-1, the key leukocyte-expressed glycoprotein ligand of all three selectins (McEver, 2002). The 19mer peptide was presented on an avidin scaffold via a biotin linked to its non glycosylated terminus (Somers et al., 2000) at a site density fivefold lower than that capable of supporting rolling interactions at physiological shear stresses (unpublished data). Interestingly, both the duration of L-selectin tethers to this nonmucin selectin ligand and their corresponding koff, as well as the ability of labile tethers to undergo dramatic stabilization above a threshold shear stress, were indistinguishable from bonds between L-selectin and PNAd (Fig. 2 A). The rate of L-selectinmediated tethering was proportional to the glycopeptide density and was markedly reduced on the corresponding desulfated PSGL-1derived glycopeptide (Fig. 2 A, inset). L-selectinmediated tethering to the sulfated but nonfucosylated isoform of the PSGL-1 peptide was completely eliminated even at coating densities >50,000 sites/µm2 (unpublished data). Thus, the kinetics of L-selectin tethers and their tight shear dependence are independent of mucin presentation of the L-selectin ligand. Furthermore, the interactions of L-selectinexpressing lymphocytes with sulfosialylated L-selectin ligands presented on an endothelial monolayer shared similar bond kinetics and stabilization by shear to interactions measured on cell-free PNAd or PSGL-1derived glycopeptides (Fig. 2 B). Notably, the transition from labile to stable tethers on the monolayer occurred at slightly elevated shear than on PNAd or the PSGL-1 peptide, probably due to the more heterogenous ligand presentation on the monolayer than on the cell-free substrate.
|
Enhanced recognition of ligand by L-selectin rescues its adhesion dependence on a threshold shear
Adhesive interactions between cell-free immobilized L-selectin and L-selectin ligands expressed on flowing neutrophils exhibited nearly identical kinetics and shear-dependent stabilization properties as lymphocyte-based L-selectin interacting with cell-free PNAd or PSGL-1 glycopeptides (compare Fig. 3 A with Fig. 1 E and Fig. 2 A). Therefore, we used cell-free L-selectin systems to further address whether specific alterations of the selectin ectodomain may modulate its intrinsic bonding properties at low shear stresses. Ligand recognition by an L-selectin mutant, in which the native EGF domain was substituted with that of P-selectin (Kansas et al., 1994), was next analyzed at a 2-ms resolution. The mutant (termed LPL) retains the selectin specificity and lectin structure of native L-selectin, but supports functional tethers at a 100-fold higher efficiency than wild-type L-selectin at physiological shear stresses (Dwir et al., 2000, 2002). When immobilized at identical densities, cell-free LPL not only supported much higher frequencies of tethers than cell-free L-selectin at any shear stress and density tested (Fig. 3, A and B, insets; unpublished data), but also mediated stable tethers with koff 2030-fold lower than L-selectin tethers even at shear stresses below 0.4 dyn/cm2 (Fig. 3, A and B). Consistent with its higher ligand recognition properties, LPL coated at 2 sites/µm2 could support comparable levels of neutrophil tethers as L-selectin immobilized at 500 sites/µm2 (Fig. 3 C), a density too low to support physiological neutrophil rolling (Dwir et al., 2000, 2002). Under these limiting conditions, the majority of LPL-mediated interactions dissociated at subthreshold shear stresses with similar koff values to bonds mediated by L-selectin. Thus, the labile nature of the selectincarbohydrate bond cannot be corrected by an EGF domain substitution that alters the lectin domain reactivity under shear flow. However, native L-selectin, when encountering sufficiently high density ligand, readily converted its labile tethers into stable tethers even at subthreshold shear stresses. At a subthreshold shear stress, for instance, a 1.5- and 2-fold higher density of ligand not only increased tether formation by L-selectin, but also allowed 20 and 50% of L-selectin bonds, respectively, to undergo 1520-fold stabilization (Fig. 4, PNAd 15 and 20 ng/ml, respectively). Similarly, lymphocytes expressing high L-selectin levels could also stabilize tethers to low density PNAd even at subthreshold shear stresses (unpublished data). Conversely, reduced PNAd density restricted L-selectinmediated tether stabilization even at the permissive shear stress of 0.4 dyn/cm2 (Table I). Thus, the ability to stabilize short-lived L-selectin bonds can be partially reconstituted, even below the shear threshold, when L-selectin (or ligand) can locally associate with sufficiently high densities of ligand (or of L-selectin).
|
|
|
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
However, the present paper suggests a new explanation for the tight dependence of L-selectin adhesiveness on critical shear flow. We demonstrate that at low shear rates, both cell-based and cell-free L-selectin form millisecond-lived tethers with their ligands. Subtle increases in either ligand density (Fig. 4) or in the rate of L-selectin transport over ligand, controlled by the shear rate (Fig. 5, A and B) result, however, in dramatic stabilization of multivalent L-selectin contacts leading to functional adhesive tethers. Thus, the failure of L-selectin to mediate functional adhesion below critical shear stresses is not due to improper recognition of ligand, but reflects a failure to stabilize singular contacts via leukocyte transport over ligand-bearing surface. High resolution videomicroscopy (Videos 14, available at http://www.jcb.org/cgi/content/full/jcb.200303134/DC1) suggests that an L-selectinexpressing cell can rotate onto or translate over the surface as it is held by the lever arm provided by its first ligand-occupied microvillus. Enhanced shear rate increases the probability of encounter with secondary ligand sites by the initially tethered leukocyte (Fig. 1, A and C; Fig. 7, top panels). The fact that stabilization is tightly regulated by the shear rate, rather than shear force experienced by the tethered leukocyte (Fig. 5 B), indicates that force is not a major positive regulator of L-selectin adhesion, at least not at low shear conditions. Thus, labile tethers formed below the shear threshold correspond to single L-selectin bonds, whereas above the shear threshold, the shear rate provides sufficient cellular transport to stabilize a functional multivalent tether (Fig. 7). In principle, the order of magnitude stabilization in the lifetime of this contact could be provided by mere increase in bond number (Chen and Springer, 1999). However, if multiple L-selectin bonds would simply decay in parallel, the 14-fold increase in tether lifetime observed at the shear threshold would predict a five-orders of magnitude increase in L-selectin bond number (Goldstein and Wofsy, 1996). Because a twofold increase in ligand density resulted in about half of L-selectin interactions undergoing a 20-fold stabilization (Fig. 4), mere increase in microvilli engagements and in bond number per microvillar contact could not have accounted for such dramatic stabilization. Therefore, avidity amplification of L-selectin tethers should involve exceptionally fast and local rebinding events between microvillar L-selectin and clusters of carbohydrate ligands on single scaffolds.
These millisecond-rebinding events are favored by cytoskeletal anchorage of L-selectin, a process dependent on the cytoplasmic tail of L-selectin (Kansas et al., 1994; Dwir et al., 2001). However, the present paper suggests that below the shear threshold, individual L-selectin bonds form, but also break very rapidly before selectin anchorage provides stabilization to the newly formed tether (Fig. 7). Thus, contacts formed below the shear threshold and lasting 4 ms are insufficient for the L-selectin tail to stabilize the nascent selectin-mediated tether (Fig. 6 B). Critical cellular transport over ligand is mandatory for initial stabilization of this tether because once the contact is prolonged to 30 ms (Fig. 6 B), the cytoplasmic tail of L-selectin can now participate in further tether stabilization (Fig. 6 B). Interestingly, the cytoplasmic tail facilitates both preformed and ligand-induced cytoskeletal anchorage of L-selectin (Pavalko et al., 1995; Evans et al., 1999), and so, stabilization of the nascent L-selectin tether may involve both the primary ligand-occupied L-selectin and its neighbor L-selectin molecules on the same ligand-occupied microvillus (Fig. 7).
Bond lifetime has been predicted to decrease with any increased loading forces (Bell, 1978), and this has been experimentally confirmed with several types of counter-receptors both by single-bond force spectroscopy measurements (Merkel et al., 1999; Evans et al., 2001) and by measurements of bond duration between counter-receptors experiencing increasing shear forces (Alon et al., 1995a; Pierres et al., 1996; Ramachandran et al., 1999). Nevertheless, over a range of low subthreshold shear stresses generated by increasing shear rates at a fixed medium viscosity (Fig. 1 E) or by increasing viscosity at a fixed rate (Fig. 5 B), the koff of single L-selectin bonds remained practically force insensitive. Thus, L-selectin bonds are adapted to increase their avidity to surface-bound ligands at low physiological shear stresses with little cost in stress-enhanced bond rupture. Such a mechanism could potentially enhance the formation of other multivalent receptor-mediated bonds, including shear-promoted platelet tethering to von Willebrand factor (Doggett et al., 2002). Successful selectin anchoring to the cytoskeleton, driven by ligand occupancy, may also increase the duration of the selectin tether, reducing its sensitivity to rupture by forces. Indeed, the higher the force loading at higher shear stresses, the higher is the contribution of L-selectin anchorage to stabilization of selectin tethers (Dwir et al., 2001).
Our finding that the lifetime of unstressed singular L-selectin bonds falls in the range of 4 ms should lead to reevaluation of previous affinity measurements of monovalent L-selectin bonds. The kon of selectin ligand association previously estimated from BIAcore analyses to be in the order of 105 M-1s-1 (Nicholson et al., 1998) may be in fact much higher, approaching a value of 2.3 x 106 M-1s-1, well within the range of the P-selectinPSGL-1 association rate (4.4 x 106 M-1s-1; Mehta et al., 1998). This value may explain the high efficiency by which L-selectin, although the shortest of all selectins, efficiently captures flowing leukocytes to endothelial surfaces and adherent leukocytes. Our new kinetic results also explain why L-selectin partially loses its shear threshold requirement when interacting with multivalent glycoprotein ligands such as GlyCAM-1 (Dwir et al., 1998) or with ligand clusters such as sLex-bearing glycolipids or polysulfated polymers (Finger et al., 1996). High valency L-selectin ligands in extravascular tissues including the basal aspects of HEV (Hemmerich et al., 2001) may thus stably associate with and signal through lymphocyte L-selectin in shear-free settings. Clearly, L-selectin transport over these multivalent ligands is not required to produce multivalent tethers. Similarly, L-selectin ligands chemically modified to prolong their selectin occupancy do not require shear to generate stable tethers (Puri et al., 1998; Greenberg et al., 2000). In conclusion, the specialized kinetic properties of native L-selectin carbohydrate interactions depicted in this paper may reflect an evolutionary pressure to down-regulate L-selectin interactions with carbohydrate ligands abundantly expressed on circulating leukocytes, and possibly on subsets of blood vessels. These carbohydrates may serve as a pool of emergency ligands that can abruptly promote L-selectindependent leukocyte capture to blood vessels and other leukocytes in response to abruptly elevated shear, without de novo ligand synthesis or translocation.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Cells
The tail-deleted analogue L358stop, lacking the 15 carboxyl-terminal cytoplasmic residues, and LPL, L-selectin in which the EGF-like domain of L-selectin has been replaced with the homologous P-selectin domain, were described elsewhere (Kansas et al., 1994; Dwir et al., 2001). These constructs and full-length human L-selectin were stably expressed in 300.19 pre B cells as described previously (Dwir et al., 2000, 2001). The human umbilical vein endothelial cellderived line, ECV-304 (LS12), stably transfected with FucTVII and N-acetylglucosamine 6-O-sulfotransferase (Kimura et al., 1999), was a gift from Dr. R. Kannagi (Aichi Cancer Center, Nagoya, Japan). Cells were maintained in RPMI 1640/10% FCS, 2 mM glutamine, and antibiotics. Peripheral blood granulocytes were isolated from anti-coagulated blood after dextran sedimentation and density separation over Ficoll-Hypaque (Dwir et al., 2000).
Preparation of ligand-coated substrates for flow experiments
PNAd diluted to 5100 ng/ml in coating medium (PBS supplemented with 20 mM bicarbonate, pH 8.5) were adsorbed onto a polystyrene plate for 15 h at 4°C. DREG-200 and sVCAM-1 diluted in the same coating medium were coated at 37°C for 2 h. All substrates were washed and blocked with PBS supplemented with 2% human serum albumin (PBS/HSA). The ligand density of PNAd was expressed as input-coating concentrations (ng/ml). PSGL-1derived monobiotinylated glycopeptides were immobilized on avidin-coated substrates as described previously (Dwir et al., 2002). Coating densities were determined by coating equimolar input densities of [14C]biotin (Amersham Biosciences). Cell-free L-selectin and LPL mutant were each derived from lysates of the corresponding transfected 300.19 cells, and were captured on plates coated with the selectin tail-specific mAb CA21, as described previously (Dwir et al., 2000).
Laminar flow assays
Plates coated with adhesive ligands or cell monolayers were assembled in a parallel plate laminar flow chamber, and laminar flow adhesion assays were performed as described previously (Dwir et al., 2000). Cells resuspended in cell-binding medium H/H medium (HBSS/10 mM Hepes, pH 7.4), supplemented with 2 mM CaCl2 at 12 x 106 cells/ml were perfused at RT through the flow chamber at desired flow rates, generated by an automated syringe pump (Harvard Apparatus). Media viscosity was increased from 1 to 2.6 cP by supplementing it with 6% (wt/vol) Ficoll (Mr = 400,000; Sigma-Aldrich) as described previously (Chen and Springer, 2001). Cellular interactions were visualized with a 20x objective (Diaphot 300; Nikon). Cells were videotaped at either a 0.02-s resolution with a CCD camera (model LIS-700; Applitech) or at a 0.002-s resolution with a high speed camera (Kodak Motion Corder Analyzer, FASTCAM-SUPER 500; Kodak). For L-selectin inhibition, leukocytes were perfused in medium supplemented with 2 mM EGTA or preincubated with 1 µg/ml DREG-200 or 50 µg/ml fucoidin. For PSGL-1 inhibition on neutrophils, leukocytes were presuspended with 1 µg/ml KPL-1.
High temporal resolution microkinetics of individual leukocytes was analyzed on video segments recorded at 500 frames/s (2 ms), and cell-tracking analysis was performed with the WSCAN-Array-3 software as described previously (Dwir et al., 2001). Motions of cells perfused at shear rates lower than 30 s-1 were manually analyzed from played back segments. Initial tethers were defined as those freely flowing cells moving closest to the lower wall of the flow chamber, which transiently tethered to the adhesive substrate at least once during a 670-µm-long path. Initial tethers or pauses of leukocytes reversibly interacting with the adhesive substrates were defined as displacements of <0.1 µm within three or more consecutive frames. Pauses <4 ms were considered nonspecific, as they could not be eliminated by blocking selectin function. The natural log of the number of pauses with a given duration after pause initiation was plotted against pause duration. A first-order dissociation plot yielded a straight line with the slope equal to -koff. The error on each koff value was derived by linear regression analysis. In experiments with L-selectin expressing 300.19 lymphocytes, the force on the bond was calculated to be 180 pN per 1 dyn/cm2 wall shear stress using a diameter of 12 µm and assigning a bond angle of 50°. In neutrophils, the force on the bond was estimated to be 120 pN per 1 dyn/cm2 (Alon et al., 1997).
Online supplemental material
Videos 1 and 3 are digitized videos recorded with a high speed camera (at 500 frames/s) of a representative L-selectintransfected pre B lymphocyte tethering to PNAd at shear stresses of 0.3 and 0.4 dyn/cm2, respectively. Videos 2 and 4 are control experiments depicting an L-selectintransfected lymphocyte preblocked with the L-selectin mAb DREG-200 and perfused at 0.3 and 0.4 dyn/cm2, respectively, over the same PNAd. The frame number and time (in seconds) elapsed from the beginning of the recording is shown. Also included is a supplementary section describing results and discussion of high speed camera analysis of transient P-selectinmediated neutrophil tethers determined at low shear stresses. Online supplemental material available at http://www.jcb.org/cgi/content/full/jcb.200303134/DC1.
![]() |
Acknowledgments |
---|
G.S. Kansas was supported by National Institutes of Health grant 5-R24-HL64831. U.S. Schwarz is supported by the Emmy-Noether-Programme of the German Science Foundation. Parts of this work were supported by the United States Israel Binational Science Foundation (to R. Alon and G.S. Kansas), by the Israel Science Foundation founded by the Israel Academy of Sciences and Humanities (to R. Alon) and by the Abisch-Frenkel Foundation (to R. Alon). R. Alon is the Incumbent of The Tauro Career Development Chair in Biomedical Research.
Submitted: 20 March 2003
Accepted: 4 September 2003
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Alon, R., D.A. Hammer, and T.A. Springer. 1995a. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature. 374:539542.[CrossRef][Medline]
Alon, R., P.D. Kassner, M.W. Carr, E.B. Finger, M.E. Hemler, and T.A. Springer. 1995b. The integrin VLA-4 supports tethering and rolling in flow on VCAM-1. J. Cell Biol. 128:12431253.[Abstract]
Alon, R., S. Chen, K.D. Puri, E.B. Finger, and T.A. Springer. 1997. The kinetics of L-selectin tethers and the mechanics of selectin-mediated rolling. J. Cell Biol. 138:11691180.
Alon, R., S. Chen, R. Fuhlbrigge, K.D. Puri, and T.A. Springer. 1998. The kinetics and shear threshold of transient and rolling interactions of L-selectin with its ligand on leukocytes. Proc. Natl. Acad. Sci. USA. 95:1163111636.
Bell, G. 1978. Models for the specific adhesion of cells to cells. Science. 200:618627.[Medline]
Berg, E.L., M.K. Robinson, R.A. Warnock, and E.C. Butcher. 1991. The human peripheral lymph node vascular addressin is a ligand for LECAM-1, the peripheral lymph node homing receptor. J. Cell Biol. 114:343349.[Abstract]
Berlin, C., R.F. Bargatze, J.J. Campbell, U.H. von Andrian, M.C. Szabo, S.R. Hasslen, R.D. Nelson, E.L. Berg, S.L. Erlandsen, and E.C. Butcher. 1995. 4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell. 80:413422.[Medline]
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. 76:12801292.
Chang, K.C., D.F. Tees, and D.A. Hammer. 2000. The state diagram for cell adhesion under flow: leukocyte rolling and firm adhesion. Proc. Natl. Acad. Sci. USA. 97:1126211267.
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. 144:185200.
Chen, S., and T.A. Springer. 2001. Selectin receptor-ligand bonds: Formation limited by shear rate and dissociation governed by the Bell model. Proc. Natl. Acad. Sci. USA. 98:950955.
de Chateau, M., S. Chen, A. Salas, and T.A. Springer. 2001. Kinetic and mechanical basis of rolling through an integrin and novel Ca2+-dependent rolling and Mg2+-dependent firm adhesion modalities for the 4ß7-MAdCAM-1 interaction. Biochemistry. 40:1397213979.[CrossRef][Medline]
Dembo, M., D.C. Torney, K. Saxman, and D.A. Hammer. 1988. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc. R. Soc. Lond. B. Biol. Sci. 234:5583.[Medline]
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. 83:194205.
Dwir, O., F. Shimron, C. Chen, M.S. Singer, S.D. Rosen, and R. Alon. 1998. GlyCAM-1 supports leukocyte rolling in flow: evidence for a greater dynamic stability of L-selectin rolling of lymphocytes than of neutrophils. Cell. Adhes. Commun. 6:349370.[Medline]
Dwir, O., G.S. Kansas, and R. Alon. 2000. An activated L-selectin mutant with conserved equilibrium binding properties but enhanced ligand recognition under shear flow. J. Biol. Chem. 275:1868218691.
Dwir, O., G.S. Kansas, and R. Alon. 2001. The cytoplasmic tail of L-selectin regulates leukocyte capture and rolling by controlling the mechanical stability of selectin:ligand tethers. J. Cell Biol. 155:145156.
Dwir, O., D.A. Steeber, U.S. Schwarz, R.T. Camphausen, G.S. Kansas, T.F. Tedder, and R. Alon. 2002. L-selectin dimerization enhances tether formation to properly spaced ligand. J. Biol. Chem. 277:2113021139.
Evans, E., A. Leung, D. Hammer, and S. Simon. 2001. Chemically distinct transition states govern rapid dissociation of single L-selectin bonds under force. Proc. Natl. Acad. Sci. USA. 98:37843789.
Evans, S.S., D.M. Schleider, L.A. Bowman, M.L. Francis, G.S. Kansas, and J.D. Black. 1999. Dynamic association of L-selectin with the lymphocyte cytoskeletal matrix. J. Immunol. 162:36153624.
Feigelson, S.W., V. Grabovsky, E. Winter, L.L. Chen, R.B. Pepinsky, T. Yednock, D. Yablonski, R. Lobb, and R. Alon. 2001. The Src kinase p56(lck) up-regulates VLA-4 integrin affinity. Implications for rapid spontaneous and chemokine-triggered T cell adhesion to VCAM-1 and fibronectin. J. Biol. Chem. 276:1389113901.
Finger, E.B., K.D. Puri, R. Alon, M.B. Lawrence, U.H. von Andrian, and T.A. Springer. 1996. Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature. 379:266269.[CrossRef][Medline]
Fuhlbrigge, R.C., R. Alon, K.D. Puri, J.B. Lowe, and T.A. Springer. 1996. Sialylated, fucosylated ligands for L-selectin expressed on leukocytes mediate tethering and rolling adhesions in physiologic flow conditions. J. Cell Biol. 135:837848.[Abstract]
Goldstein, B., and C. Wofsy. 1996. Why is it so hard to dissociate multivalent antigens from cell-surface antibodies? Immunol. Today. 17:7780.[CrossRef][Medline]
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. 79:23912402.
Hemmerich, S., and S.D. Rosen. 2000. Carbohydrate sulfotransferases in lymphocyte homing. Glycobiology. 10:849856.
Hemmerich, S., A. Bistrup, M.S. Singer, A. van Zante, J.K. Lee, D. Tsay, M. Peters, J.L. Carminati, T.J. Brennan, K. Carver-Moore, et al. 2001. Sulfation of L-selectin ligands by an HEV-restricted sulfotransferase regulates lymphocyte homing to lymph nodes. Immunity. 15:237247.[Medline]
Kahn, J., R.H. Ingraham, F. Shirley, G.I. Migaki, and T.K. Kishimoto. 1994. Membrane proximal cleavage of L-selectin: identification of the cleavage site and a 6-kD transmembrane peptide fragment of L-selectin. J. Cell Biol. 125:461470.[Abstract]
Kansas, G.S., K.B. Saunders, K. Ley, A. Zakrzewicz, R.M. Gibson, B.C. Furie, B. Furie, and T.F. Tedder. 1994. A role for the epidermal growth factor-like domain of P-selectin in ligand recognition and cell adhesion. J. Cell Biol. 124:609618.[Abstract]
Kimura, N., C. Mitsuoka, A. Kanarmori, N. Hiraiwa, K. Uchimura, T. Muramatsu, T. Tamatani, G.S. Kansas, and R. Kannagi. 1999. Reconstitution of functional L-selectin ligands on a cultured human endothelial cell line by cotransfection of 1,3 fucosyltransferase VII and newly cloned GlcNAcß:6-sulfotransferase cDNA. Proc. Natl. Acad. Sci. USA. 96:45304535.
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. 136:717727.
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. 423:190193.[CrossRef][Medline]
McEver, R.P. 2002. Selectins: lectins that initiate cell adhesion under flow. Curr. Opin. Cell Biol. 14:581586.[CrossRef][Medline]
Mehta, P., R.D. Cummings, and R.P. McEver. 1998. Affinity and kinetic analysis of P-selectin binding to P-selectin glycoprotein ligand-1. J. Biol. Chem. 273:3250632513.
Merkel, R., P. Nassoy, A. Leung, K. Ritchie, and E. Evans. 1999. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 397:5053.[CrossRef][Medline]
Nicholson, M.W., A.N. Barclay, M.S. Singer, S.D. Rosen, and P.A. van der Merwe. 1998. Affinity and kinetic analysis of L-selectin binding to GlyCAM-1. J. Biol. Chem. 273:763770.
Pavalko, F.M., D.M. Walker, L. Graham, M. Goheen, C.M. Doerschuk, and G.S. Kansas. 1995. The cytoplasmic domain of L-selectin interacts with cytoskeletal proteins via -actinin:receptor positioning in microvilli does not require interaction with
-actinin. J. Cell Biol. 129:11551164.[Abstract]
Pierres, A., A.M. Benoliel, P. Bongrand, and P.A. van der Merwe. 1996. Determination of the lifetime and force dependence of interactions of single bonds between surface-attached CD2 and CD48 adhesion molecules. Proc. Natl. Acad. Sci. USA. 93:1511415118.
Puri, K.D., S. Chen, and T.A. Springer. 1998. Modifying the mechanical property and shear threshold of L-selectin adhesion independently of equilibrium properties. Nature. 392:930933.[CrossRef][Medline]
Ramachandran, V., M.U. Nollert, H. Qiu, W.J. Liu, R.D. Cummings, C. Zhu, and R.P. McEver. 1999. Tyrosine replacement in P-selectin glycoprotein ligand-1 affects distinct kinetic and mechanical properties of bonds with P- and L-selectin. Proc. Natl. Acad. Sci. USA. 96:1377113776.
Rosen, S.D., and C.R. Bertozzi. 1994. The selectins and their ligands. Curr. Opin. Cell Biol. 6:663673.[Medline]
Smith, M.J., E.L. Berg, and M.B. Lawrence. 1999. A direct comparison of selectin-mediated transient, adhesive events using high temporal resolution. Biophys. J. 77:33713383.
Snapp, K.R., H. Ding, K. Atkins, R. Warnke, F.W. Luscinskas, and G.S. Kansas. 1998. A novel P-selectin glycoprotein ligand-1 monoclonal antibody recognizes an epitope within the tyrosine sulfate motif of human PSGL-1 and blocks recognition of both P- and L-selectin. Blood. 91:154164.
Somers, W.S., J. Tang, G.D. Shaw, and R.T. Camphausen. 2000. Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to sLe(x) and PSGL-1. Cell. 103:467479.[Medline]
Thomas, W.E., E. Trintchina, M. Forero, V. Vogel, and E.V. Sokurenko. 2002. Bacterial adhesion to target cells enhanced by shear force. Cell. 109:913923.[Medline]
Related Article