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The Effects of Load on E-Selectin Bond Rupture and Bond Formation

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Abstract

Molecular dissociation rates have long been known to be sensitive to applied force. We use a laser trap to provide evidence that rates of association may also be force-dependent. We use the thermal fluctuation assay to study single bonds between E-selectin and sialyl Lewisa (sLea), the sugar on PSGL-1 to which the three selectins bind. Briefly, an E-selectin-coated bead is held in a laser trap and pressed with various compressive loads against the vertical surface of a bead coated with sLea. The time it takes for a bond to form is used to calculate a specific two-dimensional on-rate, \( k_{\text{on}}^{\text{o}} . \) We observe an increase in \( k_{\text{on}}^{\text{o}} \) with increasing compressive force, providing single molecule evidence that on-rate, in addition to off-rate, is influenced by load. By measuring bond lifetimes at known tensile loads, we show that E-selectin, like its family members L- and P-selectin, is capable of forming catch bonds. Our data support a reverse Bell model, in which compressive forces lower the activation energy for binding. Load-dependent on-rates may be a general feature of all intermolecular bonds.

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References

  1. Alon, R., S. Chen, K. D. Puri, E. B. Finger, and T. A. Springer. The kinetics of L-selectin tethers and the mechanics of selectin-mediated rolling. J. Cell Biol. 138:1169–1180, 1997.

    Article  Google Scholar 

  2. Alon, R., D. A. Hammer, and T. A. Springer. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature 374:539–542, 1995.

    Article  Google Scholar 

  3. Bell, G. I. Models for the specific adhesion of cells to cells. Science 200:618–627, 1978.

    Article  Google Scholar 

  4. Beste, M. T., and D. A. Hammer. Selectin catch-slip kinetics encode shear threshold adhesive behavior of rolling leukocytes. Proc. Natl Acad. Sci. USA 105:20716–20721, 2008.

    Article  Google Scholar 

  5. Brunk, D. K., and D. A. Hammer. Quantifying rolling adhesion with a cell-free assay: E-selectin and its carbohydrate ligands. Biophys. J. 72:2820–2833, 1997.

    Article  Google Scholar 

  6. Chen, S., and T. A. Springer. Selectin receptor-ligand bonds: formation limited by shear rate and dissociation governed by the Bell model. Proc. Natl Acad. Sci. USA 98:950–955, 2001.

    Article  Google Scholar 

  7. Chen, W., E. A. Evans, R. P. McEver, and C. Zhu. Monitoring receptor-ligand interactions between surfaces by thermal fluctuations. Biophys. J. 94:694–701, 2008.

    Article  Google Scholar 

  8. Chesla, S. E., P. Selvaraj, and C. Zhu. Measuring two-dimensional receptor-ligand binding kinetics by micropipette. Biophys. J. 75:1553–1572, 1998.

    Article  Google Scholar 

  9. Dembo, M., D. C. Torney, K. Saxman, and D. Hammer. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc. R. Soc. Lond. B. Biol. Sci. 234:55–83, 1988.

    Article  Google Scholar 

  10. Evans, E., A. Leung, V. Heinrich, and C. Zhu. Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc. Natl Acad. Sci. USA 101:11281–11286, 2004.

    Article  Google Scholar 

  11. Finger, E. B., K. D. Puri, R. Alon, M. B. Lawrence, U. H. von Andrian, and T. A. Springer. Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature 379:266–269, 1996.

    Article  Google Scholar 

  12. Florin, E. L., V. T. Moy, and H. E. Gaub. Adhesion forces between individual ligand-receptor pairs. Science 264:415–417, 1994.

    Article  Google Scholar 

  13. Fritz, J., A. G. Katopodis, F. Kolbinger, and D. Anselmetti. Force-mediated kinetics of single P-selectin/ligand complexes observed by atomic force microscopy. Proc. Natl Acad. Sci. USA 95:12283–12288, 1998.

    Article  Google Scholar 

  14. Graves, B. J., R. L. Crowther, C. Chandran, J. M. Rumberger, S. Li, K. S. Huang, D. H. Presky, P. C. Familletti, B. A. Wolitzky, and D. K. Burns. Insight into E-selectin/ligand interaction from the crystal structure and mutagenesis of the lec/EGF domains. Nature 367:532–538, 1994.

    Article  Google Scholar 

  15. Guilford, W. H., D. E. Dupuis, G. Kennedy, J. Wu, J. B. Patlak, and D. M. Warshaw. Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacements in the laser trap. Biophys. J. 72:1006–1021, 1997.

    Article  Google Scholar 

  16. Guilford, W. H., J. A. Tournas, D. Dascalu, and D. S. Watson. Creating multiple time-shared laser traps with simultaneous displacement detection using digital signal processing hardware. Anal. Biochem. 326:153–166, 2004.

    Article  Google Scholar 

  17. Guo, B., and W. H. Guilford. Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc. Natl Acad. Sci. USA 103:9844–9849, 2006.

    Article  Google Scholar 

  18. Ham, A. S., D. J. Goetz, A. L. Klibanov, and M. B. Lawrence. Microparticle adhesive dynamics and rolling mediated by selectin-specific antibodies under flow. Biotechnol. Bioeng. 96:596–607, 2007.

    Article  Google Scholar 

  19. Hanley, W., O. McCarty, S. Jadhav, Y. Tseng, D. Wirtz, and K. Konstantopoulos. Single molecule characterization of P-selectin/ligand binding. J. Biol. Chem. 278:10556–10561, 2003.

    Article  Google Scholar 

  20. Hanley, W. D., D. Wirtz, and K. Konstantopoulos. Distinct kinetic and mechanical properties govern selectin-leukocyte interactions. J. Cell Sci. 117:2503–2511, 2004.

    Article  Google Scholar 

  21. Hulme, E. C., and N. J. M. Birdsall. Strategy and Tactics in Receptor-Binding Studies. Oxford, UK: IRL Press, pp. 63–176, 1992.

    Google Scholar 

  22. Johnson, K. L. Contact Mechanics (2nd ed.). Cambridge, UK: Cambridge University Press, 1985.

    MATH  Google Scholar 

  23. Kimura, N., C. Mitsuoka, A. Kanamori, N. Hiraiwa, K. Uchimura, T. Muramatsu, T. Tamatani, G. S. Kansas, and R. Kannagi. Reconstitution of functional L-selectin ligands on a cultured human endothelial cell line by cotransfection of alpha1→3 fucosyltransferase VII and newly cloned GlcNAcbeta:6-sulfotransferase cDNA. Proc. Natl Acad. Sci. USA 96:4530–4535, 1999.

    Article  Google Scholar 

  24. Kong, F., A. J. Garcia, A. P. Mould, M. J. Humphries, and C. Zhu. Demonstration of catch bonds between an integrin and its ligand. J. Cell Biol. 185:1275–1284, 2009.

    Article  Google Scholar 

  25. Lawrence, M. B., G. S. Kansas, E. J. Kunkel, and K. Ley. Threshold levels of fluid shear promote leukocyte adhesion through selectins (CD62L, P, E). J. Cell Biol. 136:717–727, 1997.

    Article  Google Scholar 

  26. Lou, J., T. Yago, A. G. Klopocki, P. Mehta, W. Chen, V. I. Zarnitsyna, N. V. Bovin, C. Zhu, and R. P. McEver. Flow-enhanced adhesion regulated by a selectin interdomain hinge. J. Cell Biol. 174:1107–1117, 2006.

    Article  Google Scholar 

  27. Lowe, J. B., L. M. Stoolman, R. P. Nair, R. D. Larsen, T. L. Berhend, and R. M. Marks. ELAM-1-dependent cell adhesion to vascular endothelium determined by a transfected human fucosyltransferase cDNA. Cell 63:475–484, 1990.

    Article  Google Scholar 

  28. Lubarsky, G. V., M. R. Davidson, and R. H. Bradley. Elastic modulus, oxidation depth and adhesion force of surface modified polystyrene studied by AFM and XPS. Surf. Sci. 558:135–144, 2004.

    Article  Google Scholar 

  29. Marshall, B. T., M. Long, J. W. Piper, T. Yago, R. P. McEver, and C. Zhu. Direct observation of catch bonds involving cell-adhesion molecules. Nature 423:190–193, 2003.

    Article  Google Scholar 

  30. Mody, N. A., O. Lomakin, T. A. Doggett, T. G. Diacovo, and M. R. King. Mechanics of transient platelet adhesion to von Willebrand factor under flow. Biophys. J. 88:1432–1443, 2005.

    Article  Google Scholar 

  31. Moore, K. L., K. D. Patel, R. E. Bruehl, F. Li, D. A. Johnson, H. S. Lichenstein, R. D. Cummings, D. F. Bainton, and R. P. McEver. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J. Cell Biol. 128:661–671, 1995.

    Article  Google Scholar 

  32. Park, S. E., R. Ryoo, W. S. Ahn, C. W. Lee, and J. S. Chang. Nanotechnology in mesostructured materials, Vol 146: Proceedings of the 3rd International Mesostructured Materials Symposium, p. 393, 2003.

  33. 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. Comparison of PSGL-1 microbead and neutrophil rolling: microvillus elongation stabilizes P-selectin bond clusters. Biophys. J. 82:1835–1847, 2002.

    Article  Google Scholar 

  34. Paschall, C. D., W. H. Guilford, and M. B. Lawrence. Enhancement of L-selectin, but not P-selectin, bond formation frequency by convective flow. Biophys. J. 94:1034–1045, 2008.

    Article  Google Scholar 

  35. Pereverzev, Y. V., O. V. Prezhdo, M. Forero, E. V. Sokurenko, and W. E. Thomas. The two-pathway model for the catch-slip transition in biological adhesion. Biophys. J. 89:1446–1454, 2005.

    Article  Google Scholar 

  36. Phan, U. T., T. T. Waldron, and T. A. Springer. Remodeling of the lectin-EGF-like domain interface in P- and L-selectin increases adhesiveness and shear resistance under hydrodynamic force. Nat. Immunol. 7:883–889, 2006.

    Article  Google Scholar 

  37. Phillips, M. L., E. Nudelman, F. C. Gaeta, M. Perez, A. K. Singhal, S. Hakomori, and J. C. Paulson. ELAM-1 mediates cell adhesion by recognition of a carbohydrate ligand, sialyl-Lex. Science 250:1130–1132, 1990.

    Article  Google Scholar 

  38. Pierce, G. W. The Songs of Insects. Cambridge, MA: Harvard University Press, 1948.

    Google Scholar 

  39. Puri, K. D., E. B. Finger, and T. A. Springer. The faster kinetics of L-selectin than of E-selectin and P-selectin rolling at comparable binding strength. J. Immunol. 158:405–413, 1997.

    Google Scholar 

  40. Ramachandran, V., M. U. Nollert, H. Qiu, W. J. Liu, R. D. Cummings, C. Zhu, and R. P. McEver. 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, 1999.

    Article  Google Scholar 

  41. Ramachandran, V., T. Yago, T. K. Epperson, M. M. Kobzdej, M. U. Nollert, R. D. Cummings, C. Zhu, and R. P. McEver. Dimerization of a selectin and its ligand stabilizes cell rolling and enhances tether strength in shear flow. Proc. Natl Acad. Sci. USA 98:10166–10171, 2001.

    Article  Google Scholar 

  42. Rinko, L. J., M. B. Lawrence, and W. H. Guilford. The molecular mechanics of P- and L-selectin lectin domains binding to PSGL-1. Biophys. J. 86:544–554, 2004.

    Article  Google Scholar 

  43. Sarangapani, K. K., T. Yago, A. G. Klopocki, M. B. Lawrence, C. B. Fieger, S. D. Rosen, R. P. McEver, and C. Zhu. Low force decelerates L-selectin dissociation from P-selectin glycoprotein ligand-1 and endoglycan. J. Biol. Chem. 279:2291–2298, 2004.

    Article  Google Scholar 

  44. Smith, M. J., E. L. Berg, and M. B. Lawrence. A direct comparison of selectin-mediated transient, adhesive events using high temporal resolution. Biophys. J. 77:3371–3383, 1999.

    Article  Google Scholar 

  45. Somers, W. S., J. Tang, G. D. Shaw, and R. T. Camphausen. 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, 2000.

    Article  Google Scholar 

  46. Spillmann, C. M., E. Lomakina, and R. E. Waugh. Neutrophil adhesive contact dependence on impingement force. Biophys. J. 87:4237–4245, 2004.

    Article  Google Scholar 

  47. Springer, T. A. Structural basis for selectin mechanochemistry. Proc. Natl Acad. Sci. USA 106:91–96, 2009.

    Article  Google Scholar 

  48. Sun, G., Y. Zhang, B. Huo, and M. Long. Surface-bound selectin-ligand binding is regulated by carrier diffusion. Eur. Biophys. J. 38:701–711, 2009.

    Article  Google Scholar 

  49. Suonpaa, M., E. Markela, T. Stahlberg, and I. Hemmila. Europium-labelled streptavidin as a highly sensitive universal label indirect time-resolved immunofluorometry of FSH and TSH. J. Immunol. Methods 149:247–253, 1992.

    Article  Google Scholar 

  50. Svoboda, K., and S. M. Block. Biological applications of optical forces. Annu. Rev. Biophys. Biomol. Struct. 23:247–285, 1994.

    Article  Google Scholar 

  51. Tees, D. F., R. E. Waugh, and D. A. Hammer. A microcantilever device to assess the effect of force on the lifetime of selectin-carbohydrate bonds. Biophys. J. 80:668–682, 2001.

    Article  Google Scholar 

  52. Thomas, W. For catch bonds, it all hinges on the interdomain region. J. Cell Biol. 174(7):911–913, 2006.

    Article  Google Scholar 

  53. Thomas, W. E., M. Forero, O. Yakovenko, L. M. Nilsson, P. Vicini, E. V. Sokurenko, and V. Vogel. Catch bond model derived from allostery explains force-activated bacterial adhesion. Biophys. J. 90:753–764, 2006.

    Article  Google Scholar 

  54. Thomas, W. E., L. M. Nilsson, M. Forero, E. V. Sokurenko, and V. Vogel. Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli. Mol. Microbiol. 53:1545–1557, 2004.

    Article  Google Scholar 

  55. Ushakova, N. A., M. E. Preobrazhenskaya, M. I. Bird, R. Priest, A. V. Semenov, A. V. Mazurov, N. E. Nifantiev, T. V. Pochechueva, O. E. Galanina, and N. V. Bovin. Monomeric and multimeric blockers of selectins: comparison of in vitro and in vivo activity. Biochemistry (Moscow) 70:432–439, 2005.

    Article  Google Scholar 

  56. Varki, A. Selectin ligands. Proc. Natl Acad. Sci. USA 91:7390–7397, 1994.

    Article  Google Scholar 

  57. Vu-Quoc, L., X. Zhang, and L. Lesburg. A normal force-displacement model for contacting spheres accounting for plastic deformation: force-driven formulation. J. Appl. Mech. 67:363–371, 2000.

    Article  MATH  Google Scholar 

  58. Waldron, T. T., and T. A. Springer. Transmission of allostery through the lectin domain in selectin-mediated cell adhesion. Proc. Natl Acad. Sci. USA 106:85–90, 2009.

    Article  Google Scholar 

  59. Wild, M. K., M. C. Huang, U. Schulze-Horsel, P. A. van der Merwe, and D. Vestweber. Affinity, kinetics, and thermodynamics of E-selectin binding to E-selectin ligand-1. J. Biol. Chem. 276:31602–31612, 2001.

    Article  Google Scholar 

  60. Xia, L., M. Sperandio, T. Yago, J. M. McDaniel, R. D. Cummings, S. Pearson-White, K. Ley, and R. P. McEver. P-selectin glycoprotein ligand-1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J. Clin. Invest. 109:939–950, 2002.

    Google Scholar 

  61. Yago, T., J. Wu, C. D. Wey, A. G. Klopocki, C. Zhu, and R. P. McEver. Catch bonds govern adhesion through L-selectin at threshold shear. J. Cell Biol. 166:913–923, 2004.

    Article  Google Scholar 

  62. Zhu, C., M. Long, S. E. Chesla, and P. Bongrand. Measuring receptor/ligand interaction at the single-bond level: experimental and interpretative issues. Ann. Biomed. Eng. 30:305–314, 2002.

    Article  Google Scholar 

  63. Zou, X., V. R. Shinde Patil, N. M. Dagia, L. A. Smith, M. J. Wargo, K. A. Interliggi, C. M. Lloyd, D. F. Tees, B. Walcheck, M. B. Lawrence, and D. J. Goetz. PSGL-1 derived from human neutrophils is a high-efficiency ligand for endothelium-expressed E-selectin under flow. Am. J. Physiol. Cell Physiol. 289:C415–C424, 2005.

    Article  Google Scholar 

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Acknowledgments

The authors thank Sasha Klibanov, Michael Lawrence, and Brian Schmidt of the University of Virginia for helpful discussions. The authors also acknowledge the support of the Department of Biomedical Engineering at the University of Virginia, and the National Institutes of Health (EB002185).

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  1. Department of Biomedical Engineering, University of Virginia, 800759, Charlottesville, VA, 22908, USA

    Jeremy H. Snook & William H. Guilford

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Snook, J.H., Guilford, W.H. The Effects of Load on E-Selectin Bond Rupture and Bond Formation. Cel. Mol. Bioeng. 3, 128–138 (2010). https://doi.org/10.1007/s12195-010-0110-6

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