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. 1995 Nov;69(5):2131–2138. doi: 10.1016/S0006-3495(95)80087-1

Selectin- and integrin-mediated T-lymphocyte rolling and arrest on TNF-alpha-activated endothelium: augmentation by erythrocytes.

R J Melder 1, L L Munn 1, S Yamada 1, C Ohkubo 1, R K Jain 1
PMCID: PMC1236447  PMID: 8580357

Abstract

The adhesive and hemodynamic forces that lead to lymphocyte rolling and arrest on activated endothelium and the biophysical role of various adhesion molecules and blood elements in this process are poorly understood. By quantifying their behaviour both in vivo and in vitro, we show here that erythrocytes facilitate selectin- and integrin-mediated rolling and binding of T-lymphocytes on tumor necrosis factor alpha-activated endothelium. The relative contribution of selectins and integrins to this process can be distinguished by using a simple mathematical expression of lymphocyte capture within the range of physiological shear stress. The need for selectin participation in lymphocyte capture increases with shear stress (> 1 dyn/cm2), and both beta 1 and beta 2 integrins act in synergy to produce adhesive drag on captured cells. These findings are potentially useful in developing strategies for intervening with T-cells in a variety of normal and pathological responses as well as for the delivery of genetically modified T-cells to their targets in vivo.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alon R., Hammer D. A., Springer T. A. Lifetime of the P-selectin-carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature. 1995 Apr 6;374(6522):539–542. doi: 10.1038/374539a0. [DOI] [PubMed] [Google Scholar]
  2. Berg E. L., McEvoy L. M., Berlin C., Bargatze R. F., Butcher E. C. L-selectin-mediated lymphocyte rolling on MAdCAM-1. Nature. 1993 Dec 16;366(6456):695–698. doi: 10.1038/366695a0. [DOI] [PubMed] [Google Scholar]
  3. Bevilacqua M. P. Endothelial-leukocyte adhesion molecules. Annu Rev Immunol. 1993;11:767–804. doi: 10.1146/annurev.iy.11.040193.004003. [DOI] [PubMed] [Google Scholar]
  4. Bevilacqua M. P., Pober J. S., Mendrick D. L., Cotran R. S., Gimbrone M. A., Jr Identification of an inducible endothelial-leukocyte adhesion molecule. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9238–9242. doi: 10.1073/pnas.84.24.9238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bevilacqua M. P., Stengelin S., Gimbrone M. A., Jr, Seed B. Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science. 1989 Mar 3;243(4895):1160–1165. doi: 10.1126/science.2466335. [DOI] [PubMed] [Google Scholar]
  6. Bjerknes M., Cheng H., Ottaway C. A. Dynamics of lymphocyte-endothelial interactions in vivo. Science. 1986 Jan 24;231(4736):402–405. doi: 10.1126/science.3941903. [DOI] [PubMed] [Google Scholar]
  7. Dembo M., Torney D. C., Saxman K., Hammer D. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc R Soc Lond B Biol Sci. 1988 Jun 22;234(1274):55–83. doi: 10.1098/rspb.1988.0038. [DOI] [PubMed] [Google Scholar]
  8. Geng J. G., Bevilacqua M. P., Moore K. L., McIntyre T. M., Prescott S. M., Kim J. M., Bliss G. A., Zimmerman G. A., McEver R. P. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature. 1990 Feb 22;343(6260):757–760. doi: 10.1038/343757a0. [DOI] [PubMed] [Google Scholar]
  9. Goldsmith H. L., Spain S. Margination of leukocytes in blood flow through small tubes. Microvasc Res. 1984 Mar;27(2):204–222. doi: 10.1016/0026-2862(84)90054-2. [DOI] [PubMed] [Google Scholar]
  10. Hakkert B. C., Kuijpers T. W., Leeuwenberg J. F., van Mourik J. A., Roos D. Neutrophil and monocyte adherence to and migration across monolayers of cytokine-activated endothelial cells: the contribution of CD18, ELAM-1, and VLA-4. Blood. 1991 Nov 15;78(10):2721–2726. [PubMed] [Google Scholar]
  11. Hammer D. A., Apte S. M. Simulation of cell rolling and adhesion on surfaces in shear flow: general results and analysis of selectin-mediated neutrophil adhesion. Biophys J. 1992 Jul;63(1):35–57. doi: 10.1016/S0006-3495(92)81577-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hammer D. A., Lauffenburger D. A. A dynamical model for receptor-mediated cell adhesion to surfaces. Biophys J. 1987 Sep;52(3):475–487. doi: 10.1016/S0006-3495(87)83236-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hession C., Moy P., Tizard R., Chisholm P., Williams C., Wysk M., Burkly L., Miyake K., Kincade P., Lobb R. Cloning of murine and rat vascular cell adhesion molecule-1. Biochem Biophys Res Commun. 1992 Feb 28;183(1):163–169. doi: 10.1016/0006-291x(92)91623-x. [DOI] [PubMed] [Google Scholar]
  14. Jones D. A., McIntire L. V., Smith C. W., Picker L. J. A two-step adhesion cascade for T cell/endothelial cell interactions under flow conditions. J Clin Invest. 1994 Dec;94(6):2443–2450. doi: 10.1172/JCI117612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kansas G. S., Ley K., Munro J. M., Tedder T. F. Regulation of leukocyte rolling and adhesion to high endothelial venules through the cytoplasmic domain of L-selectin. J Exp Med. 1993 Mar 1;177(3):833–838. doi: 10.1084/jem.177.3.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Larsen E., Celi A., Gilbert G. E., Furie B. C., Erban J. K., Bonfanti R., Wagner D. D., Furie B. PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes. Cell. 1989 Oct 20;59(2):305–312. doi: 10.1016/0092-8674(89)90292-4. [DOI] [PubMed] [Google Scholar]
  17. Lawrence M. B., McIntire L. V., Eskin S. G. Effect of flow on polymorphonuclear leukocyte/endothelial cell adhesion. Blood. 1987 Nov;70(5):1284–1290. [PubMed] [Google Scholar]
  18. Lawrence M. B., Smith C. W., Eskin S. G., McIntire L. V. Effect of venous shear stress on CD18-mediated neutrophil adhesion to cultured endothelium. Blood. 1990 Jan 1;75(1):227–237. [PubMed] [Google Scholar]
  19. Lawrence M. B., Springer T. A. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell. 1991 May 31;65(5):859–873. doi: 10.1016/0092-8674(91)90393-d. [DOI] [PubMed] [Google Scholar]
  20. Leunig M., Yuan F., Menger M. D., Boucher Y., Goetz A. E., Messmer K., Jain R. K. Angiogenesis, microvascular architecture, microhemodynamics, and interstitial fluid pressure during early growth of human adenocarcinoma LS174T in SCID mice. Cancer Res. 1992 Dec 1;52(23):6553–6560. [PubMed] [Google Scholar]
  21. Ley K., Gaehtgens P., Fennie C., Singer M. S., Lasky L. A., Rosen S. D. Lectin-like cell adhesion molecule 1 mediates leukocyte rolling in mesenteric venules in vivo. Blood. 1991 Jun 15;77(12):2553–2555. [PubMed] [Google Scholar]
  22. Luscinskas F. W., Ding H., Lichtman A. H. P-selectin and vascular cell adhesion molecule 1 mediate rolling and arrest, respectively, of CD4+ T lymphocytes on tumor necrosis factor alpha-activated vascular endothelium under flow. J Exp Med. 1995 Mar 1;181(3):1179–1186. doi: 10.1084/jem.181.3.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moore K. L., Eaton S. F., Lyons D. E., Lichenstein H. S., Cummings R. D., McEver R. P. The P-selectin glycoprotein ligand from human neutrophils displays sialylated, fucosylated, O-linked poly-N-acetyllactosamine. J Biol Chem. 1994 Sep 16;269(37):23318–23327. [PubMed] [Google Scholar]
  24. Munn L. L., Melder R. J., Jain R. K. Analysis of cell flux in the parallel plate flow chamber: implications for cell capture studies. Biophys J. 1994 Aug;67(2):889–895. doi: 10.1016/S0006-3495(94)80550-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nobis U., Pries A. R., Cokelet G. R., Gaehtgens P. Radial distribution of white cells during blood flow in small tubes. Microvasc Res. 1985 May;29(3):295–304. doi: 10.1016/0026-2862(85)90020-2. [DOI] [PubMed] [Google Scholar]
  26. Schmid-Schoenbein G. W., Fung Y. C., Zweifach B. W. Vascular endothelium-leukocyte interaction; sticking shear force in venules. Circ Res. 1975 Jan;36(1):173–184. doi: 10.1161/01.res.36.1.173. [DOI] [PubMed] [Google Scholar]
  27. Schmid-Schönbein G. W. Leukocyte kinetics in the microcirculation. Biorheology. 1987;24(2):139–151. doi: 10.3233/bir-1987-24207. [DOI] [PubMed] [Google Scholar]
  28. Schmid-Schönbein G. W., Sung K. L., Tözeren H., Skalak R., Chien S. Passive mechanical properties of human leukocytes. Biophys J. 1981 Oct;36(1):243–256. doi: 10.1016/S0006-3495(81)84726-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schmid-Schönbein G. W., Usami S., Skalak R., Chien S. The interaction of leukocytes and erythrocytes in capillary and postcapillary vessels. Microvasc Res. 1980 Jan;19(1):45–70. doi: 10.1016/0026-2862(80)90083-7. [DOI] [PubMed] [Google Scholar]
  30. Springer T. A. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. doi: 10.1038/346425a0. [DOI] [PubMed] [Google Scholar]
  31. Tamatani T., Kotani M., Tanaka T., Miyasaka M. Molecular mechanisms underlying lymphocyte recirculation. II. Differential regulation of LFA-1 in the interaction between lymphocytes and high endothelial cells. Eur J Immunol. 1991 Mar;21(3):855–858. doi: 10.1002/eji.1830210351. [DOI] [PubMed] [Google Scholar]
  32. Tamatani T., Kuida K., Watanabe T., Koike S., Miyasaka M. Molecular mechanisms underlying lymphocyte recirculation. III. Characterization of the LECAM-1 (L-selectin)-dependent adhesion pathway in rats. J Immunol. 1993 Mar 1;150(5):1735–1745. [PubMed] [Google Scholar]
  33. Weston S. A., Parish C. R. Calcein: a novel marker for lymphocytes which enter lymph nodes. Cytometry. 1992;13(7):739–749. doi: 10.1002/cyto.990130710. [DOI] [PubMed] [Google Scholar]
  34. Weston S. A., Parish C. R. New fluorescent dyes for lymphocyte migration studies. Analysis by flow cytometry and fluorescence microscopy. J Immunol Methods. 1990 Oct 4;133(1):87–97. doi: 10.1016/0022-1759(90)90322-m. [DOI] [PubMed] [Google Scholar]
  35. Yan H. C., Delisser H. M., Pilewski J. M., Barone K. M., Szklut P. J., Chang X. J., Ahern T. J., Langer-Safer P., Albelda S. M. Leukocyte recruitment into human skin transplanted onto severe combined immunodeficient mice induced by TNF-alpha is dependent on E-selectin. J Immunol. 1994 Mar 15;152(6):3053–3063. [PubMed] [Google Scholar]
  36. von Andrian U. H., Chambers J. D., McEvoy L. M., Bargatze R. F., Arfors K. E., Butcher E. C. Two-step model of leukocyte-endothelial cell interaction in inflammation: distinct roles for LECAM-1 and the leukocyte beta 2 integrins in vivo. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7538–7542. doi: 10.1073/pnas.88.17.7538. [DOI] [PMC free article] [PubMed] [Google Scholar]

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