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Mechanisms for Flow-Enhanced Cell Adhesion

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Abstract

Cell adhesion is mediated by specific receptor–ligand bonds. In several biological systems, increasing flow has been observed to enhance cell adhesion despite the increasing dislodging fluid shear forces. Flow-enhanced cell adhesion includes several aspects: flow augments the initial tethering of flowing cells to a stationary surface, slows the velocity and increases the regularity of rolling cells, and increases the number of rollingly adherent cells. Mechanisms for this intriguing phenomenon may include transport-dependent acceleration of bond formation and force-dependent deceleration of bond dissociation. The former includes three distinct transport modes: sliding of cell bottom on the surface, Brownian motion of the cell, and rotational diffusion of the interacting molecules. The latter involves a recently demonstrated counterintuitive behavior called catch bonds where force prolongs rather than shortens the lifetimes of receptor–ligand bonds. In this article, we summarize our recently published data that used dimensional analysis and mutational analysis to elucidate the above mechanisms for flow-enhanced leukocyte adhesion mediated by L-selectin-ligand interactions.

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References

  1. Doggett T. A., G. Girdhar, A. Lawshe, J. L. Miller, I. J. Laurenzi, S. L. Diamond, T. G. Diacovo 2003 Alterations in the intrinsic properties of the GPIbalpha-VWF tether bond define the kinetics of the platelet-type von Willebrand disease mutation, Gly233Val. Blood 102, 152–160

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  3. Goldman, A. J., R. G. Cox and H. Brenner. Slow viscous motion of a sphere parallel to a plane wall. II. Couette flow. Chem Eng Sci 22, 653660, 1967

    Article  CAS  Google Scholar 

  4. 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, D. K. Burns 1994 Insight into E-selectin/ligand interaction from the crystal structure and mutagenesis of the lec/EGF domains. Nature 367, 532–538

    Article  PubMed  CAS  Google Scholar 

  5. Happel J., H. Brenner 1991 Low Reynolds Number Hydrodynamics. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  6. Kansas G. S., K. B. Saunders, K. Ley, A. Zakrzewicz, R. M. Gibson, B. C. Furie, B. Furie, 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  9. Lou J., C. Zhu 2007 A structure-based sliding-rebinding mechanism for catch bonds. Biophys J 92, 1471–1485

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  11. Mege J. L., C. Capo, A. M. Benoliel, P. Bongrand 1986 Determination of binding strength and kinetics of binding initiation. A model study made on the adhesive properties of P388D1 macrophage-like cells. Cell Biophys 8, 141–160

    PubMed  CAS  Google Scholar 

  12. Phan U. T., T. T. Waldron, T. A. Springer 2006 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

    Article  PubMed  CAS  Google Scholar 

  13. Ramachandran V., M. Williams, T. Yago, D. W. Schmidtke, R. P. McEver 2004 Dynamic alterations of membrane tethers stabilize leukocyte rolling on P-selectin. Proc Nat. Acad Sci U S A 101, 13519–13524

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  15. Savage B., E. Saldivar, Z. M. Ruggeri 1996 Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 84, 289–297

    Article  PubMed  CAS  Google Scholar 

  16. Schmidtke D. W., 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, 719–730

    Article  PubMed  CAS  Google Scholar 

  17. Somers W. S., J. Tang, G. D. Shaw, 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

    Article  PubMed  CAS  Google Scholar 

  18. Thomas W. E., E. Trintchina, M. Forero, V. Vogel, E. V. Sokurenko 2002 Bacterial adhesion to target cells enhanced by shear force. Cell 109, 913–923

    Article  PubMed  CAS  Google Scholar 

  19. Yago, T., A. Leppanen, H. Qiu, W. D. Marcus, M. U. Nollert, C. Zhu, R. D. Cummings and R. P. McEver. Distinct molecular and cellular contributions to stabilizing selectin-mediated rolling under flow. J Cell Biol 787–799, 2002

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  21. Yago T., V. I. Zarnitsyna, A. G. Klopocki, R. P. McEver, C. Zhu. 2007 Transport governs flow-enhanced cell tethering through L-selectin at threshold shear. Biophys J 92, 330–342

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge the contributions of our co-workers who produced the original data8,20,21 which are summarized here. This work was supported by National Institutes of Health grants AI44902 (CZ) and HL65631 (RPM).

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Authors and Affiliations

  1. Coulter Department of Biomedical Engineering, Georgia Institute of Technology, Atlanta, GA, 30332, USA

    Cheng Zhu & Veronika I. Zarnitsyna

  2. Woodruff School of Mechanical Engineering, Georgia Institute of Technology, Atlanta, GA, 30332, USA

    Cheng Zhu & Veronika I. Zarnitsyna

  3. Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, 30332, USA

    Cheng Zhu & Jizhong Lou

  4. Cardiovascular Biology Research Program, Oklahoma Medical Research Foundation, University of Oklahoma Health Sciences Center, Oklahoma City, OK, 73104, USA

    Tadayuki Yago & Rodger P. McEver

  5. Department of Biochemistry and Molecular Biology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, 73104, USA

    Rodger P. McEver

Authors
  1. Cheng Zhu
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  2. Tadayuki Yago
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  3. Jizhong Lou
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  4. Veronika I. Zarnitsyna
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  5. Rodger P. McEver
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Corresponding author

Correspondence to Cheng Zhu.

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Zhu, C., Yago, T., Lou, J. et al. Mechanisms for Flow-Enhanced Cell Adhesion. Ann Biomed Eng 36, 604–621 (2008). https://doi.org/10.1007/s10439-008-9464-5

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  • DOI: https://doi.org/10.1007/s10439-008-9464-5

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