Skip to main content
SpringerLink
Log in

Leukocyte Adhesion Dynamics in Shear Flow

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Of the white blood cells that traverse the circulation, the polymorphonuclear leukocytes commonly called neutrophils, are the most numerous, numbering ∼5000 per microliter of blood. In a sense, these cells are the emergency response unit within the body's circulatory highway since they are the first to be recruited at sites of tissue trauma, infection, or inflammation. The chief function of neutrophils is the capture, phagocytosis, and degradation of foreign invaders. To carry out this critical function, neutrophils sense infection via chemotactic receptors that trigger cellular activation upon ligation of as few as 10–100 bacterial or chemokine peptides. Despite this acute sensitivity to stimuli, neutrophils circulate in healthy individuals largely in a passive state, with a very low efficiency of capture and arrest on quiescent endothelium. Here, we define the efficiency as the fraction of all cells passing by a given length of vessel wall that is captured and achieves firm adhesion. Within seconds of chemotactic signaling, adhesion molecules expressed on the plasma membrane of neutrophils are activated and a rapid boost in the efficiency of stable adhesion is detected. This occurs for both homotypic neutrophil–neutrophil adhesion and neutrophil capture and adhesion on inflamed endothelium. With such large numbers of circulating neutrophils, and with their inherent capability to rapidly adhere to postcapillary venular endothelium, the body has evolved a diverse set of mechanisms to regulate the inflammatory cascade that begins with intracellular signaling and leads to cell arrest and extravasation at sites of tissue insult. In this article we will focus on the interplay between particle–fluid dynamics that involve the shear and normal forces that transport cells transversely and axially within the vessel, and the activation and interaction of adhesion molecules that involve receptor–ligand bond formation that enables the neutrophils to resist wall shear stress and adhere to specific sites of inflammation. © 2002 Biomedical Engineering Society.

PAC2002: 8719Tt, 8717-d, 8714Ee, 8380Lz

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Alon, R., S. Chen, R. Fuhlbrigge, K. D. Puri, and T. A. Springer. The kinetics and shear threshold of transient and rolling interactions of L–selectin with its ligand on leukocytes. Proc. Natl. Acad. Sci. U.S.A. 95:11631–11636, 1998.

    Google Scholar 

  2. Alon, R., T. Feizi, C. T. Yuen, R. C. Fuhlbrigge, and T. A. Springer. Glycolipid ligands for selectins support leukocyte tethering and rolling under physiologic flow conditions. J. Immunol. 154:5356–5366, 1995.

    Google Scholar 

  3. Alon, R., R. C. Fuhlbrigge, E. B. Finger, and T. A. Springer. 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, 1996.

    Google Scholar 

  4. 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 (London) 374:539–542, 1995.

    Google Scholar 

  5. Anderson, D. C., T. K. Kishimoto, and C. W. Smith. Leukocyte adhesion deficiency and other disorders of leukocyte adherence and motility. In: The Metabolic and Molecular Bases of Inherited Disease, edited by C. R. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle. New York: McGraw–Hill, 1995, pp. 3955–3994.

    Google Scholar 

  6. Anderson, D. C., F. C. Schmalstieg, S. Kohl, M. A. Arnaout, B. J. Hughes, M. F. Tosi, G. J. Buffone, B. R. Brinkley, W. D. Dickey, J. S. Abramson, T. A. Springer, L. A. Boxer, J. M. Hollers, and C. W. Smith. Abnormalities of polymorphonuclear leukocyte function associated with a heritable deficiency of high molecular weight surface glycoproteins (GP138): Common relationship to diminished cell adherence. J. Clin. Invest. 74:536–551, 1984.

    Google Scholar 

  7. Anderson, D. C., and T. A. Springer. Leukocyte adhesion deficiency: An inherited defect in the Mac–1, LFA–1 and p150, 95 glycoproteins. Annu. Rev. Med. 38:175–194, 1987.

    Google Scholar 

  8. Arp, P., and S. G. Mason. Orthokinetic collisions of hard spheres in simple shear flow. Can. J. Chem. 54:3760–3774, 1976.

    Google Scholar 

  9. Atherton, A., and G. V. R. Born. Relationship between the velocity of rolling granulocytes and that of the blood flow in venules. J. Physiol. Paris 233:157–165, 1973.

    Google Scholar 

  10. Bartok, W., and S. G. Mason. Particle motions in sheared suspensions. V. Rigid rods and collision doublets of spheres. J. Colloid Sci. 12:243–262, 1957.

    Google Scholar 

  11. Bell, G. I. Models for the specific adhesion of cells to cells. A theoretical framework for adhesion mediated by reversible bonds between cell surface molecules. Science 200:618–627, 1978.

    Google Scholar 

  12. Bennett, T. A., C. M. G. Schammel, E. B. Lynam, D. A. Guyer, A. Mellors, B. Edwards, S. Rogelj, and L. A. Sklar. Evidence for a third component in neutrophil aggregation: Potential roles of O–linked glycoproteins as L–selectin counter–structures. J. Leukoc Biol. 58:510–518, 1995.

    Google Scholar 

  13. Bongrand, P., C. Capo, J.–L. Mege, and A.–M. Benoliel. Use of hydrodynamic flows to study cell adhesion. In: Physical Basis of Cell–Cell Adhesion, edited by P. Bongrand. Boca Raton, FL: Chemical Rubber, 1998, pp. 125–156.

    Google Scholar 

  14. Brenner, B., S. Junge, A. Birle, S. Kadel, and O. Linderkamp. Surfactant modulates intracellular signaling of the adhesion receptor L–selectin. Pediatr. Res. 48:283–288, 2000.

    Google Scholar 

  15. Butcher, E. C. Leukocyte–endothelial cell recognition: Three (or more) steps to specificity and diversity. Cell 67:1033–1036, 1991.

    Google Scholar 

  16. Chen, S., and T. A. Springer. An automatic braking system that stabilizes leukocyte rolling by an increase in selectin bond number with shear. J. Cell Biol. 144:185–200, 1999.

    Google Scholar 

  17. Cokelet, G. R., and H. L. Goldsmith. Decreased hydrodynamic resistance in the two–phase flow of blood through small vertical tubes at low flow rate. Circ. Res. 68:1–17, 1991.

    Google Scholar 

  18. Craddock, P. R., D. E. Hammerschmidt, C. F. Moldow, O. Yamada, and H. S. Jacob. Granulocyte aggregation as a manifestation of membrane interactions with complement. Possible role in leukocyte margination, microvascular occlusion, and endothelial damage. Semin Hematol. 16:140, 1979.

    Google Scholar 

  19. Craddock, P. R., D. E. Hammerschmidt, J. G. White, A. P. Dalmasso, and H. S. Jacob. Complement (C5a)–induced granulocyte aggregation in vitro: A possible mechanism of complement–mediated leukostasis and leukopenia. J. Clin. Invest. 60:260–274, 1977.

    Google Scholar 

  20. Curtis, A. S. G., and L. M. Hocking. Collision efficiency of equal spherical particles in a shear flow. The influence of London–van der Waals forces. Trans. Faraday Soc. 66:1381–1390, 1970.

    Google Scholar 

  21. Doerschuk, C. M., M. F. Allard, and J. C. Hogg. Neutrophil kinetics in rabbits during infusion of zymosan–activated plasma. J. Appl. Physiol. 67:88–95, 1989.

    Google Scholar 

  22. Doerschuk, C. M., R. K. Winn, and J. M. Harlan. Mechanisms of neutrophil emigration. In: Leukocyte Adhesion Molecules: Structure, Function, and Regulation, edited by T. A. Springer, D. C. Anderson, A. S. Rosenthal, and R. Rothlein. New York: Springer, 1989, pp. 87–94.

    Google Scholar 

  23. Dore, M., S. I. Simon, B. J. Hughes, M. L. Entman, and C. W. Smith. P–selectin–and CD18–mediated recruitment of canine neutrophils under conditions of shear stress. Vet. Pathol. 32:258–268, 1995.

    Google Scholar 

  24. Doyle, N. A., S. D. Bhagwan, B. B. Meek, G. J. Kutkoski, D. A. Steeber, T. F. Tedder, and C. M. Doerschuk. Neutrophil margination, sequestration, and emigration in the lungs of L–selectin–deficient mice. J. Clin. Invest. 99:526–533, 1997.

    Google Scholar 

  25. Engler, R. L., M. D. Dahlgren, D. D. Morris, M. A. Peterson, and G. W. Schmid–Schonbein. Role of leukocytes in response to acute myocardial ischemia and reflow in dogs. Am. J. Physiol. 251:H314–H323, 1986.

    Google Scholar 

  26. Eriksson, E. E., X. Xie, J. Werr, P. Thoren, and L. Lindbom. 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, 2001.

    Google Scholar 

  27. Etzioni, A., M. Frydman, S. Pollack, I. Avidor, M. L. Phillips, J. C. Paulson, and R. Gershoni–Barugh. Brief report: Recurrent severe infections caused by a novel leukocyte adhesion deficiency. N. Engl. J. Med. 327:1789–1792, 1992.

    Google Scholar 

  28. Evans, E. Looking inside molecular bonds at biological interfaces with dynamic force spectroscopy. Biophys. Chem. 82:83–97, 1999.

    Google Scholar 

  29. Evans, E., A. Leung, D. Hammer, and S. Simon. Chemically distinct transition states govern rapid dissociation of single L–selectin bonds under force. PNAS 98:3784–3789, 2001.

    Google Scholar 

  30. Evans, E., and K. Ritchie. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541–1555, 1997.

    Google Scholar 

  31. Evans, E., and A. Yeung. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys. J. 56:151–160, 1989.

    Google Scholar 

  32. Fewell, M. E., and J. D. Hellums. The secondary flow of Newtonian fluids in cone–and plate viscometers. Trans. Soc. Rheol. 21:535–565, 1977.

    Google Scholar 

  33. Finger, E. B., K. Purl, R. Alon, M. B. Lawrence, U. H. von Andrian, and T. A. Springer. Adhesion through L–selectin requires a threshold hydrodynamic shear. Nature (London) 379:266–269, 1996.

    Google Scholar 

  34. Fuhlbrigge, R. C., R. Alon, K. D. Puri, J. B. Lowe, and T. A. Springer. Sialylated, fucosylated ligands for L–selectin expressed on leukocytes mediate tethering and rolling adhesions in physiologic flow conditions. J. Cell Biol. 135:837–848, 1996.

    Google Scholar 

  35. Fung, Y. C. Biomechanics. Mechanical Properties of Living Tissues. New York: Springer, 1993.

    Google Scholar 

  36. Goboury, J. P., and P. Kubes. Reductions in physiologic shear rates lead to CD11/CD18–dependent, selectin–independent leukocyte rolling in vivo. Blood 83:345–350, 1994.

    Google Scholar 

  37. Goldsmith, H. L. Red cell motions and wall interactions in tube flow. Fed. Proc. 30:1578–1588, 1971.

    Google Scholar 

  38. Goldsmith, H. L., A. T. Quinn, G. Drury, C. Spanos, F. A. McIntosh, and S. I. Simon. Dynamics of neutrophil aggregation in couette flow revealed by videomicroscopy: Effect of shear rate on two–body Collision efficiency and doublet lifetime. Biophys. J. 81:2020–2034, 2001.

    Google Scholar 

  39. Gopalan, P. K., C. W. Smith, H. Lu, E. L. Berg, L. V. McIntire, and S. I. Simon. Neutrophil CD18–dependent arrest on ICAM–1 in shear flow can be activated through L–selectin. J. Immunol. 158:367–375, 1997.

    Google Scholar 

  40. Guyer, D. A., K. L. Moore, E. B. Lynam, C. M. G. Schammel, S. Rogelj, R. P. McEver, and L. A. Sklar. P–selectin glycoprotein ligand–1 (PSGL–1) is a ligand for L–selectin in neutrophil aggregation. Blood 88:2415–2421, 1996.

    Google Scholar 

  41. Hammerschmidt, D. E., P. R. Craddock, J. McCullough, R. S. Kronenberg, A. P. Dalmasso, and H. S. Jacob. Complement activation and pulmonary leukostasis during nylon fiber filtration leukapheresis. Blood 51:721–730, 1978.

    Google Scholar 

  42. Hentzen, E. R., S. Neelamegham, G. S. Kansas, J. A. Benanti, L. V. McIntire, C. W. Smith, and S. I. Simon. Sequential binding of CD11a/CD18 and CD11b/CD18 defines neutrophil capture and stable adhesion to intercellular adhesion molecule–1. Blood 95:911–920, 1999.

    Google Scholar 

  43. Jones, D. A., O. Abbassi, L. V. McIntire, R. P. McEver, and C. W. Smith. P–selectin mediates neutrophil rolling on histamine–stimulated endothelial cells. Biophys. J. 65:1560–1569, 1993.

    Google Scholar 

  44. Jung, U., K. E. Norman, K. Scharffetter–Kochanek, A. L. Beaudet, and K. Ley. Transit time of leukocytes rolling through venules controls cytokine–induced inflammatory cell recruitment in vivo. J. Clin. Invest. 102:1526–1533, 1998.

    Google Scholar 

  45. Kansas, G. S. Selectins and their ligands: Current concepts and controversies. Blood 88:3259–3287, 1996.

    Google Scholar 

  46. Kishimoto, T. K. The selectins. In: Structure, Function, and Regulation of Molecules Involved in Leukocyte Adhesion, edited by P. E. Lipsky, R. Rothlein, T. K. Kishimoto, R. B. Faanes, and C. W. Smith. New York: Springer, 1993, pp. 107–134.

    Google Scholar 

  47. Kuijpers, T. W., L. Koenderman, R. S. Weening, A. J. Verhoeven, and D. Roos. Continuous cell activation is necessary for stable interaction of complement receptor type 3 with its counter–structure in the aggregation response of human neutrophils. Eur. J. Immunol. 20:501–508, 1990.

    Google Scholar 

  48. 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.

    Google Scholar 

  49. Lawrence, M. B., and T. A. Springer. Leukocytes roll on a selectin at physiologic flow rates: Distinction from and prerequisite for adhesion through integrins. Cell 65:859–873, 1991.

    Google Scholar 

  50. Lehr, H.–A., A. S. Weyrich, R. K. Saetzler, A. Jurek, K. E. Arfors, G. A. Zimmerman, S. M. Prescott, and T. M. McIntyre. Vitamin C blocks inflammatory platelet–activating factor mimetics created by cigarette smoking. J. Clin. Invest. 99:2358–2364, 1997.

    Google Scholar 

  51. Lu, H., C. M. Ballantyne, and C. W. Smith. LFA–1 (CD11a/CD18) triggers hydrogen peroxide production by canine neutrophils. J. Leukoc Biol. 68:73–80, 2000.

    Google Scholar 

  52. Lu, H., C. W. Smith, J. Perrard, D. Bullard, L. Tang, S. B. Shappell, M. L. Entman, A. L. Beaudet, and C. M. Ballantyne. LFA–1 is sufficient in mediating neutrophil emigration in Mac–1 deficient mice. J. Clin. Invest. 99:1340–1350, 1997.

    Google Scholar 

  53. Lupher, Jr., M. L., E. A. Harris, C. R. Beals, L. Sui, R. C. Liddington, and D. E. Staunton. Cellular activation of leukocyte function–associated antigen–1 and its affinity are regulated at the i domain allosteric site. J. Immunol. 167:1431–1439, 2001.

    Google Scholar 

  54. Lynam, E. B., S. I. Simon, Y. P. Rochon, and L. A. Sklar. Lipopolysaccharide enhances CD11b/CD18 function but inhibits neutrophil aggregation. Blood 83:3303–3311, 1994.

    Google Scholar 

  55. McDonagh, P. F., D. S. Wilson, H. Iwamura, C. W. Smith, S. K. Williams, and J. G. Copeland. CD18 Antibody treatment limits early myocardial reperfusion injury after initial leukocyte deposition. J. Surg. Res. 64:139–149, 1996.

    Google Scholar 

  56. Melder, R. J., J. Yuan, L. L. Munn, and R. K. Jain. Erythrocytes enhance lymphocyte rolling and arrest in vivo. Microvasc. Res. 59:316–322, 2000.

    Google Scholar 

  57. Merkel, R., P. Nassoy, A. Leung, K. Ritchie, and E. Evans. Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy (Comments). Nature (London) 397:50–53, 1999.

    Google Scholar 

  58. Mitchell, D. J., P. Li, P. H. Reinhardt, and P. Kubes. Importance of L–selectin–dependent leukocyte–leukocyte interactions in human whole blood. Blood 95:2954–2959, 2000.

    Google Scholar 

  59. Munn, L. L., R. J. Melder, and R. K. Jain. Role of erythrocytes in leukocyte–endothelial interactions: Mathematical model and experimental validation. Biophys. J. 71:466–478, 1996.

    Google Scholar 

  60. Neelamegham, S., A. D. Taylor, A. R. Burns, C. W. Smith, and S. I. Simon. Hydrodynamic shear shows distinct roles for LFA–1 and Mac–1 in neutrophil adhesion to intercellular adhesion molecule–1. Blood 92:1626–1638, 1998.

    Google Scholar 

  61. Neelamegham, S., A. D. Taylor, J. D. Hellums, M. Dembo, C. W. Smith, and S. I. Simon. Modeling the reversible kinetics of neutrophil aggregation under hydrodynamic shear. Biophys. J. 72:1527–1540, 1997.

    Google Scholar 

  62. Neelamegham, S., A. D. Taylor, H. Shankaran, C. W. Smith, and S. I. Simon. Shear and time–dependent changes in Mac–1, LFA–1, and ICAM–3 binding regulate neutrophil homotypic adhesion. J. Immunol. 164:3798–3805, 2000.

    Google Scholar 

  63. Okuyama, M., J. Kambayashi, M. Sakon, and M. Monden. LFA–1/ICAM–3 mediates neutrophil homotypic aggregation under fluid shear stress. J. Cell. Biochem. 60:550–559, 1996.

    Google Scholar 

  64. 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. U.S.A. 98:10166–10171, 2001.

    Google Scholar 

  65. Rochon, Y. P., and M. M. Frojmovic. Dynamics of human neutrophil aggregation evaluated by flow cytometry. J. Leukoc Biol. 50:434–443, 1991.

    Google Scholar 

  66. Schmid–Schonbein, G. W., S. Usami, R. Skalak, and S. Chien. The interaction of leukocytes and erythrocytes in capillary and post–capillary vessels. Microvasc. Res. 19:45–70, 1980.

    Google Scholar 

  67. Schmidtke, D. W., and S. L. Diamond. Direct observation of membrane tethers formed during neutrophil attachment to platelets or P–selectin under physiological flow. J. Cell Biol. 149:719–730, 2000.

    Google Scholar 

  68. Shankaran, H., and S. Neelamegham. Nonlinear flow affects hydrodynamic forces and neutrophil adhesion rates in coneplate viscometers. Biophys. J. 80:2631–2648, 2001.

    Google Scholar 

  69. Sigal, A., A. D. Bleijs, V. Grabovsky, S. J. van Vliet, O. Dwir, C. G. Figdor, Y. van Kooyk, and R. Alon. The LFA–1 integrin supports rolling adhesions on ICAM–1 under physiological shear flow in a permissive cellular environment. J. Immunol. 165:442–452, 2000.

    Google Scholar 

  70. Simon, S. I., A. R. Burns, A. D. Taylor, P. K. Gopalan, E. B. Lynam, L. A. Sklar, and C. W. Smith. L–Selectin (CD62L) crosslinking signals neutrophil adhesive functions via the Mac–1 (CD11b/CD18) β 2–integrin. J. Immunol. 155:1502–1514, 1995.

    Google Scholar 

  71. Simon, S. I., J. D. Chambers, and L. A. Sklar. Flow cytometric analysis and modeling of cell–cell adhesive interactions: The neutrophil as a model. J. Cell Biol. 111:2747–2756, 1990.

    Google Scholar 

  72. Simon, S. I., Y. Hu, D. Vestweber, and C. W. Smith. Neutrophil tethering on E–selectin activates β2 integrin binding to ICAM–1 through a mitrogen–activated protein kinase signal transduction pathway. J. Immunol. 164:4348–4358, 2000.

    Google Scholar 

  73. Simon, S. I., S. Neelamegham, A. Taylor, and C. W. Smith. The multistep process of homotypic neutrophil aggregation: A review of the molecules and effects of hydrodynamics. Cell Adhes Commun. 6:263–276, 1998.

    Google Scholar 

  74. Simon, S. I., Y. P. Rochon, E. B. Lynam, C. W. Smith, D. C. Anderson, and L. A. Sklar. Beta2–integrin and L–selectin are obligatory receptors in neutrophil aggregation. Blood 82:1097–1106, 1993.

    Google Scholar 

  75. Smith, C. W. Endothelial adhesion molecules and their role in inflammation. Can. J. Physiol. Pharmacol. 71:76–87, 1993.

    Google Scholar 

  76. Smith, C. W., A. R. Burns, and S. I. Simon. 1998. Cooperative signaling between leukocytes and endothelium mediating firm attachment. In: Vascular Adhesion Molecules and Inflammation, edited by J. D. Pearson. Basel: Birkhauser, 1998, pp. 39–64.

    Google Scholar 

  77. 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.

    Google Scholar 

  78. Smolen, J. E., T. K. Petersen, C. Koch, S. J. O'Keefe, W. A. Hanlon, S. Seo, D. Pearson, M. C. Fossett, and S. I. Simon. L–selectin signaling of neutrophil adhesion and degranulation involves p38 MAP kinase. J. Biol. Chem. 275:15876–15884, 2000.

    Google Scholar 

  79. Smoluchowski, M. V. Versuch einer mathematischen theorie der koagulationskinetik kolloider losungen. Z. Phys. Chem. (Leipzig) 92:129–168, 1917.

    Google Scholar 

  80. Springer, T. A. Adhesion receptors of the immune system. Nature (London) 346:425–434, 1990.

    Google Scholar 

  81. Springer, T. A. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 76:301–314, 1994.

    Google Scholar 

  82. Tandon, P., and S. L. Diamond. Kinetics of beta2–integrin and L–selectin bonding during neutrophil aggregation in shear flow. Biophys. J. 75:3163–3178, 1998.

    Google Scholar 

  83. Taylor, A. D., S. Neelamegham, J. D. Hellums, C. W. Smith, and S. I. Simon. Molecular dynamics of of the transition from L–selectin–to β2–integrin–dependent neutrophil adhesion under defined hydrodynamic shear. Biophys. J. 71:3488–3500, 1996.

    Google Scholar 

  84. Tees, D. F. J., O. Coenen, and H. L. Goldsmith. Interaction forces between red cells agglutinated by antibody. IV. Time and force dependence of break–up. Biophys. J. 65:1318–1334, 1993.

    Google Scholar 

  85. Tha, S. P., and H. L. Goldsmith. Interaction forces between red cells agglutinated by antibody. I. Theoretical. Biophys. J. 50:1109–1116, 1986.

    Google Scholar 

  86. Tsang, Y. T. M., S. Neelamegham, Y. Hu, E. L. Berg, A. R. Burns, C. W. Smith, and S. I. Simon. Synergy between L–selectin signaling and chemotactic activation during neutrophil adhesion and transmigration. J. Immunol. 159:4566–4577, 1997.

    Google Scholar 

  87. van de Ven, T. G. M. Colloidal Hydrodynamics. San Diego: Academic, 1989.

    Google Scholar 

  88. van de Ven, T. G. M., and S. G. Mason. The microrheology of colloidal dispersions. VII. Orthokinetic doublet formation of spheres. Colloid Polym. Sci. 255:468–479, 1977.

    Google Scholar 

  89. Vestweber, D., and J. E. Blanks. Mechanisms that regulate the function of the selectins and their ligands. Physiol. Rev. 79:181–213, 1999.

    Google Scholar 

  90. von Andrian, U. H., E. M. Berger, J. D. Chambers, L. Ramezani, H. Ochs, J. M. Harlan, J. C. Paulson, A. Etzioni, and K.–E. Arfors. In vivo behavior of neutrophils from two patients with distinct inherited leukocyte adhesion deficiency syndromes. J. Clin. Invest. 91:2893–2897, 1993.

    Google Scholar 

  91. von Andrian, U. H., J. D. Chambers, L. M. McEvoy, R. F. Bargatze, K.–E. Arfors, and E. C. Butcher. Two step model of leukocyte–endothelial cell interaction in inflammation: Distinct roles for LECAM–1 and the leukocyte beta2–integrins in vivo. Proc. Natl. Acad. Sci. U.S.A. 88:7538–7542, 1991.

    Google Scholar 

  92. von Andrian, U. H., P. Hansell, J. D. Chambers, E. M. Berger, I. T. Filho, E. C. Butcher, and K.–E. Arfors. L–selectin function is required for beta2–integrin–mediated neutrophil adhesion at physiologic shear rates in vivo. Am. J. Physiol. 263:H1034–H1044, 1992.

    Google Scholar 

  93. Waddell, T. K., L. Kialkow, C. K. Chan, T. K. Kishimoto, and G. P. Downey. Signaling functions of L–selectin. J. Biol. Chem. 270:15403–15410, 1995.

    Google Scholar 

  94. Walcheck, B., K. L. Moore, R. P. McEver, and T. K. Kishimoto. 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, 1996.

    Google Scholar 

  95. Xia, Z., and M. M. Frojmovic. Aggregation efficiency of activated normal or fixed platelets in a simple shear field: Effect of shear and fibrinogen occupancy. Biophys. J. 66:2190–2201, 1994.

    Google Scholar 

  96. Youker, K. A., J. Beirne, J. Lee, L. H. Michael, C. W. Smith, and M. L. Entman. Time–dependent loss of Mac–1 from in–filtrating neutrophils in the reperfused myocardium. J. Immunol. 164:2752–2758, 2000.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, University of California, Davis, Davis, CA, 95616

    Scott I. Simon

  2. Montreal General Hospital, McGill University Hospital Centre, Montreal, Quebec, Canada

    Harry L. Goldsmith

Authors
  1. Scott I. Simon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Harry L. Goldsmith
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Simon, S.I., Goldsmith, H.L. Leukocyte Adhesion Dynamics in Shear Flow. Annals of Biomedical Engineering 30, 315–332 (2002). https://doi.org/10.1114/1.1467677

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1114/1.1467677

Search

Navigation