Enhancement of L-selectin, but not P-selectin, bond formation frequency by convective flow

Biophysical Journal

Volumn 94, Issue 3, 2008, Pages 1034-1045

  Paschall, Christopher D ^a   Guilford, William H ^a,b   Lawrence, Michael B ^a  

^a University of Virginia   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

L SELECTIN; LIGAND; P SELECTIN GLYCOPROTEIN LIGAND 1; PADGEM PROTEIN;

ARTICLE; BLOOD VESSEL WALL; HYDRODYNAMICS; LEUKOCYTE; MICROSCOPY; PROTEIN BINDING; SHEAR FLOW; SHEAR STRESS; THROMBOCYTE;

EID: 38549178855     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.098707     Document Type: Article

References (63)

1. Lawrence, M. B. 1999. Selectin-carbohydrate interactions in shear flow. Curr. Opin. Chem. Biol. 3:659-664.
2. Ley, K., editor. 2001. Physiology of Inflammation. Oxford University Press, New York.
3. Walcheck, B., K. L. Moore, R. P. McEver, and T. K. Kishimoto. 1996. Neutrophil-neutrophil interactions under hydrodynamic shear stress involve L-selectin and PSGL-1: a mechanism that amplifies initial leukocyte accumulation on P-selectin in vitro. J. Clin. Invest. 98:1081-1087.
4. Alon, R., R. C. Fuhlbrigge, E. B. Finger, and T. A. Springer. 1996. Interactions through L-selectin between leukocytes and adherent leukocytes nucleate rolling adhesions on selectins and VCAM-1 in shear flow. J. Cell Biol. 135:849-865.
5. 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. 194:205-218.
6. 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 (CD62L) binding to glycosylation-dependent cell-adhesion molecule-1. J. Biol. Chem. 273:763-770.
7. 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.
8. Rinko, L. J., M. B. Lawrence, and W. H. Guilford. 2004. The molecular mechanics of P- and L-selectin lectin domains binding to PSGL-1. Biophys. J. 86:544-554.
9. Puri, K. D., E. B. Finger, and T. A. Springer. 1997. The faster kinetics of L-selectin than of E-selectin and P-selectin rolling at comparable binding strength. J. Immunol. 158:405-413.
10. 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.
11. Rosen, S. D. 2004. Ligands for L-selectin: homing, inflammation, and beyond. Annu. Rev. Immunol. 22:129-156.
12. 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.
13. 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.
14. 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.
15. Park, E. Y., 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.
16. Smith, M. J., B. R. Smith, M. B. Lawrence, and K. R. Snapp. 2004. Functional analysis of the combined role of the O-linked branching enzyme core 2 β1-6-N-glucosaminyltransferase and dimerization of P-selectin glycoprotein ligand-1 in rolling on P-selectin. J. Biol. Chem. 279:21984-21991.
17. Sang Won Ham, A., D. J. Goetz, A. L. Klibanov, and M. B. Lawrence. 2007. Microparticle adhesive dynamics and rolling mediated by selectin-specific antibodies under flow. Biotechnol. Bioeng. 96:596-607.
18. Green, C. E., U. Y. Schaff, M. R. Sarantos, A. F. Lum, D. E. Staunton, and S. I. Simon. 2006. Dynamic shifts in LFA-1 affinity regulate neutrophil rolling, arrest, and transmigration on inflamed endothelium. Blood. 107:2101-2111.
19. Lum, A. F., C. E. Green, G. R. Lee, D. E. Staunton, and S. I. Simon. 2002. Dynamic regulation of LFA-1 activation and neutrophil arrest on intercellular adhesion molecule 1 (ICAM-1) in shear flow. J. Biol. Chem. 277:20660-20670.
20. 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.
21. Cheezum, M. K., W. F. Walker, and W. H. Guilford. 2001. Quantitative comparison of algorithms for tracking single fluorescent particles. Biophys. J. 81:2378-2388.
22. Gelles, J., B. J. Schnapp, and M. P. Sheetz. 1988. Tracking kinesin-driven movements with nanometre-scale precision. Nature. 331:450-453.
23. Goldman, A. J., R. G. Cox, and H. Brenner. 1967. Slow viscous motion of a sphere parallel to a plane wall-I. Motion through a quiescent fluid. Chem. Eng. Sci. 22:637-651.
24. Sarangapani, K. K., T. Yago, A. G. Klopocki, M. B. Lawrence, C. B. Fieger, S. D. Rosen, R. P. McEver, and C. Zhu. 2004. Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J. Biol. Chem. 279:2291-2298.
25. Yago, T., J. Wu, C. D. Wey, A. G. Klopocki, C. Zhu, and R. P. McEver. 2004. Catch bonds govern adhesion through L-selectin at threshold shear. J. Cell Biol. 166:913-923.
26. Schwarz, U. S., and R. Alon. 2004. L-selectin-mediated leukocyte tethering in shear flow is controlled by multiple contacts and cytoskeletal anchorage facilitating fast rebinding events. Proc. Natl. Acad. Sci. USA. 101:6940-6945.
27. Benedek, G. B., and F. M. H. Villars. 2000. Physics with Illustrative Examples from Medicine and Biology. Springer, New York.
28. Pierres, A., A.-M. Benoliel, C. Zhu, and P. Bongrand. 2001. Diffusion of microspheres in shear flow near a wall: use to measure binding rates between attached molecules. Biophys. J. 81:25-42.
29. Ramachandran, V., M. Williams, T. Yago, D. W. Schmidtke, and R. P. McEver. 2004. Dynamic alterations of membrane tethers stabilize leukocyte rolling on P-selectin. Proc. Natl. Acad. Sci. USA. 101:13519-13524.
30. 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.
31. 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.
32. Alon, R., D. A. Hammer, and T. A. Springer. 1995. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature. 374:539-542.
33. Huang, J., J. Chen, S. E. Chesla, T. Yago, P. Mehta, R. P. McEver, C. Zhu, and M. Long. 2004. Quantifying the effects of molecular orientation and length on two-dimensional receptor-ligand binding kinetics. J. Biol. Chem. 279:44915-44923.
34. Hanley, W. D., D. Wirtz, and K. Konstantopoulos. 2004. Distinct kinetic and mechanical properties govern selectin-leukocyte interactions. J. Cell Sci. 117:2503-2511.
35. Zhu, C., M. Long, S. E. Chesla, and P. Bongrand. 2002. Measuring receptor/ligand interaction at the single-bond level: experimental and interpretative issues. Ann. Biomed. Eng. 30:305-314.
36. 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.
37. Tees, D. F., R. E. Waugh, and D. A. Hammer. 2001. A microcantilever device to assess the effect of force on the lifetime of selectin-carbohydrate bonds. Biophys. J. 80:668-682.
38. Bhatia, S. K., M. R. King, and D. A. Hammer. 2003. The state diagram for cell adhesion mediated by two receptors. Biophys. J. 84:2671-2690.
39. Rodgers, S. D., R. T. Camphausen, and D. A. Hammer. 2000. Sialyl Lewis(x)-mediated, PSGL-1-independent rolling adhesion on P-selectin. Biophys. J. 79:694-706.
40. DiVietro, J. A., D. C. Brown, L. A. Sklar, R. S. Larson, and M. B. Lawrence. 2007. Immobilized stromal cell-derived factor-1alpha triggers rapid VLA-4 affinity increases to stabilized lymphocyte tethers on VCAM-1 and subsequently initiate firm adhesion. J. Immunol. 178:3903-3905.
41. Dwir, O., G. S. Kansas, and R. Alon. 2001. Cytoplasmic anchorage of L-selectin controls leukocyte capture and rolling by increasing the mechanical stability of the selectin tether. J. Cell Biol. 155:145-156.
42. 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.
43. 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.
44. Dustin, M. L., S. K. Bromley, M. M. Davis, and C. Zhu. 2001. Identification of self through two-dimensional chemistry and synapses. Annu. Rev. Cell Dev. Biol. 17:133-157.
45. Puri, K. D., and T. A. Springer. 1996. A Schiff base with mildly oxidized carbohydrate ligands stabilizes L-selectin and not P-selectin or E-selectin rolling adhesions in shear flow. J. Biol. Chem. 271:5404-5413.
46. Marshall, B. T., K. K. Sarangapani, J. Wu, M. B. Lawrence, R. P. McEver, and C. Zhu. 2006. Measuring molecular elasticity by atomic force microscope cantilever fluctuations. Biophys. J. 90:681-692.
47. Spillmann, C. M., E. Lomakina, and R. E. Waugh. 2004. Neutrophil adhesive contact dependence on impingement force. Biophys. J. 87:4237-4245.
48. Li, P., P. Selvaraj, and C. Zhu. 1999. Analysis of competition binding between soluble and membrane-bound ligands for cell surface receptors. Biophys. J. 77:3394-3406.
49. Long, M., H. L. Goldsmith, D. F. Tees, and C. Zhu. 1999. Probabilistic modeling of shear-induced formation and breakage of doublets cross-linked by receptor-ligand bonds. Biophys. J. 76:1112-1128.
50. 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. 234:55-83.
51. Erdmann, T., and U. S. Schwarz. 2004. Stability of adhesion clusters under constant force. Phys. Rev. Lett. 92:108102.
52. Snapp, K. R., C. E. Heitzig, and G. S. Kansas. 2002. Attachment of the PSGL-1 cytoplasmic domain to the actin cytoskeleton is essential for leukocyte rolling on P-selectin. Blood. 99:4494-4502.
53. Alonso-Lebrero, J. L., J. M. Serrador, C. Dominguez-Jimenez, O. Barreiro, A. Luque, M. A. del Pozo, K. Snapp, G. Kansas, R. Schwartz-Albiez, H. Furthmayr, F. Lozano, and F. Sanchez-Madrid. 2000. Polarization and interaction of adhesion molecules P-selectin glycoprotein ligand 1 and intercellular adhesion molecule 3 with moesin and ezrin in myeloid cells. Blood. 95:2413-2419.
54. Pereverzev, Y. V., O. V. Prezhdo, M. Forero, E. V. Sokurenko, and W. E. Thomas. 2005. The two-pathway model for the catch-slip transition in biological adhesion. Biophys. J. 89:1446-1454.
55. 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.
56. Faucheux, L. P., and A. J. Libchaber. 1994. Confined Brownian motion. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics. 49:5158-5163.
57. Kaplanski, G., C. Farnarier, O. Tissot, A. Pierres, A.-M. Benoliel, M. C. Alessi, S. Kaplanski, and P. Bongrand. 1993. Granulocyte-endothelium initial adhesion. Analysis of transient binding events mediated by E-selectin in a laminar shear flow. Biophys. J. 64:1922-1933.
58. Goldman, A. J., R. G. Cox, and H. Brenner. 1967. Slow viscous motion of a sphere parallel to a plane wall-II. Couette flow. Chem. Eng. Sci. 22:653-660.
59. Piper, J. W., R. A. Swerlick, and C. Zhu. 1998. Determining force dependence of two-dimensional receptor-ligand binding affinity by centrifugation. Biophys. J. 74:492-513.
60. Chesla, S. E., P. Selvaraj, and C. Zhu. 1998. Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys. J. 75:1553-1572.
61. Galkina, E., A. Kadl, J. Sanders, D. Varughese, I. J. Sarembock, and K. Ley. 2006. Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. J. Exp. Med. 203:1273-1282.
62. Kadash, K. E., M. B. Lawrence, and S. L. Diamond. 2004. Neutrophil string formation: hydrodynamic thresholding and cellular deformation during cell collisions. Biophys. J. 86:4030-4039.
63. Lawrence, M. B., D. F. Bainton, and T. A. Springer. 1994. Neutrophil tethering to and rolling on E-selectin are separable by a requirement for L-selectin. Immunity. 1:137-145.