Avidity enhancement of L-selectin bonds by flow: Shear-promoted rotation of leukocytes turn labile bonds into functional tethers

Journal of Cell Biology

Volumn 163, Issue 3, 2003, Pages 649-659

  Dwir, Oren ^a   Solomon, Ariel ^a   Mangan, Shmuel ^a   Kansas, Geoffrey S ^b   Schwarz, Ulrich S ^c   Alon, Ronen ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b NORTHWESTERN UNIVERSITY   (United States)

^c MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

Author keywords

Aggregation; Lymph nodes; Rolling; Selectin; Shear flow

Indexed keywords

BETA1 INTEGRIN; CARBOHYDRATE; L SELECTIN; LIGAND; MUCIN; PADGEM PROTEIN; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; CELL ADHESION; CELL TRANSPORT; CHEMICAL BOND; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; DISSOCIATION; HUMAN; HUMAN CELL; LEUKOCYTE AGGREGATION; LYMPH NODE; MICROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; ROTATION; SHEAR FLOW; SHEAR RATE; SHEAR STRESS; UMBILICAL VEIN; VIDEORECORDING;

BINDING SITES; CELL ADHESION; CELL LINE; CHEMOTAXIS, LEUKOCYTE; ENDOTHELIUM, VASCULAR; HUMANS; INTEGRIN ALPHA4BETA1; L-SELECTIN; LEUKOCYTES; LIGANDS; MUCINS; STRESS, MECHANICAL;

EID: 0242425839     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200303134     Document Type: Article

References (45)

1. 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. 374:539-542.
2. 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. 128:1243-1253.
3. 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. 138:1169-1180.
4. 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. 95:11631-11636.
5. Bell, G. 1978. Models for the specific adhesion of cells to cells. Science. 200:618-627.
6. 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. 114:343-349.
7. 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. α4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell. 80:413-422.
8. 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.
9. 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. 97:11262-11267.
10. 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.
11. 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. 98:950-955.
12. 2+-dependent firm adhesion modalities for the α4β7-MAdCAM-1 interaction. Biochemistry. 40:13972-13979.
13. Dembo, M., D.C. Totney, 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. 234:55-83.
14. 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 GPIbα-vWF tether bond. Biophys. J. 83:194-205.
15. Dwir, O., F. Shimron, C. Chen, M.S. Singer, S.D. Rosen, and R. Alon. 1998. Gly-CAM-1 supports leukocyte rolling in flow: evidence for a greater dynamic stability of L-selectin rolling of lymphocytes than of neutrophils. Cell. Adhes. Commun. 6:349-370.
16. 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. 275:18682-18691.
17. 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. 155:145-156.
18. 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. 277:21130-21139.
19. 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. 98:3784-3789.
20. 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. 162:3615-3624.
21. 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. 276:13891-13901.
22. 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. 379:266-269.
23. 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. 135:837-848.
24. Goldstein, B., and C. Wofsy. 1996. Why is it so hard to dissociate multivalent antigens from cell-surface antibodies? Immunol. Today. 17:77-80.
25. 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.
26. Hemmerich, S., and S.D. Rosen. 2000. Carbohydrate sulfotransferases in lymphocyte homing. Glycobiology. 10:849-856.
27. 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. 15:237-247.
28. 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: 461-470.
29. 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. 124:609-618.
30. 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 α1,3 fucosyltransferase VII and newly cloned GlcNAcβ:6-sulfotransferase cDNA. Proc. Natl. Acad. Sci. USA. 96:4530-4535.
31. 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.
32. 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.
33. McEver, R.P. 2002. Selectins: lectins that initiate cell adhesion under flow. Curr. Opin. Cell Biol. 14:581-586.
34. 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: 32506-32513.
35. Merkel, R., P. Nassoy, A. Leung, K. Ritchie, and E. Evans. 1999. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 397:50-53.
36. 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 Gly-CAM-1. J. Biol. Chem. 273:763-770.
37. 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 α-actinin:receptor positioning in microvilli does not require interaction with α-actinin. J. Cell Biol. 129:1155-1164.
38. 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. 93:15114-15118.
39. 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. 392:930-933.
40. 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. 96:13771-13776.
41. Rosen, S.D., and C.R. Bertozzi. 1994. The selectins and their ligands. Curr. Opin. Cell Biol. 6:663-673.
42. 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. 77:3371-3383.
43. 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. 91:154-164.
44. 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. 103:467-479.
45. Thomas, W.E., E. Trintchina, M. Forero, V. Vogel, and E.V. Sokurenko. 2002. Bacterial adhesion to target cells enhanced by shear force. Cell. 109:913-923.