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. 1995 Jul;96(1):171–182. doi: 10.1172/JCI118018

Activation of polymorphonuclear leukocytes reduces their adhesion to P-selectin and causes redistribution of ligands for P-selectin on their surfaces.

D E Lorant 1, R P McEver 1, T M McIntyre 1, K L Moore 1, S M Prescott 1, G A Zimmerman 1
PMCID: PMC185186  PMID: 7542276

Abstract

In acute inflammatory responses, selectins mediate initial rolling of neutrophils (PMNs) along the endothelial surface. This is followed by tight adhesion that requires activation-dependent up-regulation of CD11/CD18 integrins on PMNs. For emigration to occur, the initial bonds that are established at the endothelial surface must be disengaged. We show that activation of PMNs results in their detachment from P-selectin, a glycoprotein expressed at the surface of inflamed endothelium that mediates initial tethering of PMNs. Loosening of the bond occurs when PMNs are activated by platelet-activating factor, which is coexpressed with P-selectin, or by other signaling molecules. The time course of reduced adhesion to P-selectin, when compared to up-regulation of CD11/CD18 integrins, suggests that "bond trading" may occur as activated PMNs transmigrate in vivo. Activation of PMNs did not alter binding of fluid-phase P-selectin, indicating that the ligand(s) for P-selectin is not shed or internalized. Using microspheres coated with P-selectin, we found that ligands for P-selectin were randomly distributed over the surfaces of rounded, unactivated PMNs. An antibody against P-selectin glycoprotein ligand-1 (PSGL-1) completely inhibited binding of P-selectin-coated beads suggesting that P-selectin glycoprotein ligand-1 is the critical binding site in this assay. In contrast to the dispersed pattern on unactivated PMNs, the ligands for P-selectin were localized on the uropods of activated, polarized cells. Pretreating PMNs with cytochalasin D before activation prevented the change in cell shape, the redistribution of binding sites for P-selectin-coated beads, and the decrease in cellular adhesiveness for P-selectin. These experiments indicate that the distribution of ligands for P-selectin is influenced by cellular activation and by cytoskeletal interactions, and that redistribution of these ligands may influence adhesive interactions. Activation of PMNs may cause loosening or disengagement of bonds between P-selectin and its ligands, facilitating transendothelial migration.

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Selected References

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

  1. Abbassi O., Kishimoto T. K., McIntire L. V., Anderson D. C., Smith C. W. E-selectin supports neutrophil rolling in vitro under conditions of flow. J Clin Invest. 1993 Dec;92(6):2719–2730. doi: 10.1172/JCI116889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adams D. H., Shaw S. Leucocyte-endothelial interactions and regulation of leucocyte migration. Lancet. 1994 Apr 2;343(8901):831–836. doi: 10.1016/s0140-6736(94)92029-x. [DOI] [PubMed] [Google Scholar]
  3. Anderson D. C., Hughes B. J., Smith C. W. Abnormal mobility of neonatal polymorphonuclear leukocytes. Relationship to impaired redistribution of surface adhesion sites by chemotactic factor or colchicine. J Clin Invest. 1981 Oct;68(4):863–874. doi: 10.1172/JCI110341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beatty P. G., Ledbetter J. A., Martin P. J., Price T. H., Hansen J. A. Definition of a common leukocyte cell-surface antigen (Lp95-150) associated with diverse cell-mediated immune functions. J Immunol. 1983 Dec;131(6):2913–2918. [PubMed] [Google Scholar]
  5. 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]
  6. Bohnsack J. F., Akiyama S. K., Damsky C. H., Knape W. A., Zimmerman G. A. Human neutrophil adherence to laminin in vitro. Evidence for a distinct neutrophil integrin receptor for laminin. J Exp Med. 1990 Apr 1;171(4):1221–1237. doi: 10.1084/jem.171.4.1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Buttrum S. M., Hatton R., Nash G. B. Selectin-mediated rolling of neutrophils on immobilized platelets. Blood. 1993 Aug 15;82(4):1165–1174. [PubMed] [Google Scholar]
  8. Carveth H. J., Bohnsack J. F., McIntyre T. M., Baggiolini M., Prescott S. M., Zimmerman G. A. Neutrophil activating factor (NAF) induces polymorphonuclear leukocyte adherence to endothelial cells and to subendothelial matrix proteins. Biochem Biophys Res Commun. 1989 Jul 14;162(1):387–393. doi: 10.1016/0006-291x(89)92009-3. [DOI] [PubMed] [Google Scholar]
  9. Cooper J. A. Effects of cytochalasin and phalloidin on actin. J Cell Biol. 1987 Oct;105(4):1473–1478. doi: 10.1083/jcb.105.4.1473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cross A. S., Wright D. G. Mobilization of sialidase from intracellular stores to the surface of human neutrophils and its role in stimulated adhesion responses of these cells. J Clin Invest. 1991 Dec;88(6):2067–2076. doi: 10.1172/JCI115536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Davis B. H., Walter R. J., Pearson C. B., Becker E. L., Oliver J. M. Membrane activity and topography of F-Met-Leu-Phe-Treated polymorphonuclear leukocytes. Acute and sustained responses to chemotactic peptide. Am J Pathol. 1982 Aug;108(2):206–216. [PMC free article] [PubMed] [Google Scholar]
  12. Diamond M. S., Springer T. A. The dynamic regulation of integrin adhesiveness. Curr Biol. 1994 Jun 1;4(6):506–517. doi: 10.1016/s0960-9822(00)00111-1. [DOI] [PubMed] [Google Scholar]
  13. Disdier M., Morrissey J. H., Fugate R. D., Bainton D. F., McEver R. P. Cytoplasmic domain of P-selectin (CD62) contains the signal for sorting into the regulated secretory pathway. Mol Biol Cell. 1992 Mar;3(3):309–321. doi: 10.1091/mbc.3.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dobrina A., Carlos T. M., Schwartz B. R., Beatty P. G., Ochs H. D., Harlan J. M. Phorbol ester causes down-regulation of CD11/CD18-independent neutrophil adherence to endothelium. Immunology. 1990 Mar;69(3):429–434. [PMC free article] [PubMed] [Google Scholar]
  15. Dransfield I., Cabañas C., Craig A., Hogg N. Divalent cation regulation of the function of the leukocyte integrin LFA-1. J Cell Biol. 1992 Jan;116(1):219–226. doi: 10.1083/jcb.116.1.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Elemer G. S., Edgington T. S. Microfilament reorganization is associated with functional activation of alpha M beta 2 on monocytic cells. J Biol Chem. 1994 Feb 4;269(5):3159–3166. [PubMed] [Google Scholar]
  17. Francis J. W., Todd R. F., 3rd, Boxer L. A., Petty H. R. Sequential expression of cell surface C3bi receptors during neutrophil locomotion. J Cell Physiol. 1989 Sep;140(3):519–523. doi: 10.1002/jcp.1041400317. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Gimbrone M. A., Jr, Obin M. S., Brock A. F., Luis E. A., Hass P. E., Hébert C. A., Yip Y. K., Leung D. W., Lowe D. G., Kohr W. J. Endothelial interleukin-8: a novel inhibitor of leukocyte-endothelial interactions. Science. 1989 Dec 22;246(4937):1601–1603. doi: 10.1126/science.2688092. [DOI] [PubMed] [Google Scholar]
  20. Granger D. N., Kubes P. The microcirculation and inflammation: modulation of leukocyte-endothelial cell adhesion. J Leukoc Biol. 1994 May;55(5):662–675. [PubMed] [Google Scholar]
  21. Griffin J. D., Spertini O., Ernst T. J., Belvin M. P., Levine H. B., Kanakura Y., Tedder T. F. Granulocyte-macrophage colony-stimulating factor and other cytokines regulate surface expression of the leukocyte adhesion molecule-1 on human neutrophils, monocytes, and their precursors. J Immunol. 1990 Jul 15;145(2):576–584. [PubMed] [Google Scholar]
  22. Hechtman D. H., Cybulsky M. I., Fuchs H. J., Baker J. B., Gimbrone M. A., Jr Intravascular IL-8. Inhibitor of polymorphonuclear leukocyte accumulation at sites of acute inflammation. J Immunol. 1991 Aug 1;147(3):883–892. [PubMed] [Google Scholar]
  23. Howard T. H., Casella J., Lin S. Correlation of the biologic effects and binding of cytochalasins to human polymorphonuclear leukocytes. Blood. 1981 Mar;57(3):399–405. [PubMed] [Google Scholar]
  24. Huber A. R., Kunkel S. L., Todd R. F., 3rd, Weiss S. J. Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science. 1991 Oct 4;254(5028):99–102. doi: 10.1126/science.1718038. [DOI] [PubMed] [Google Scholar]
  25. Hughes B. J., Hollers J. C., Crockett-Torabi E., Smith C. W. Recruitment of CD11b/CD18 to the neutrophil surface and adherence-dependent cell locomotion. J Clin Invest. 1992 Nov;90(5):1687–1696. doi: 10.1172/JCI116041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hynes R. O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992 Apr 3;69(1):11–25. doi: 10.1016/0092-8674(92)90115-s. [DOI] [PubMed] [Google Scholar]
  27. Johnston G. I., Kurosky A., McEver R. P. Structural and biosynthetic studies of the granule membrane protein, GMP-140, from human platelets and endothelial cells. J Biol Chem. 1989 Jan 25;264(3):1816–1823. [PubMed] [Google Scholar]
  28. Jones D. A., Abbassi O., McIntire L. V., McEver R. P., Smith C. W. P-selectin mediates neutrophil rolling on histamine-stimulated endothelial cells. Biophys J. 1993 Oct;65(4):1560–1569. doi: 10.1016/S0006-3495(93)81195-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kahn J., Ingraham R. H., Shirley F., Migaki G. I., Kishimoto T. K. Membrane proximal cleavage of L-selectin: identification of the cleavage site and a 6-kD transmembrane peptide fragment of L-selectin. J Cell Biol. 1994 Apr;125(2):461–470. doi: 10.1083/jcb.125.2.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kishimoto T. K., Jutila M. A., Butcher E. C. Identification of a human peripheral lymph node homing receptor: a rapidly down-regulated adhesion molecule. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2244–2248. doi: 10.1073/pnas.87.6.2244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kuijpers T. W., Hakkert B. C., Hart M. H., Roos D. Neutrophil migration across monolayers of cytokine-prestimulated endothelial cells: a role for platelet-activating factor and IL-8. J Cell Biol. 1992 May;117(3):565–572. doi: 10.1083/jcb.117.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lasky L. A. A 'roll' in acute inflammation. Curr Biol. 1993 Oct 1;3(10):680–682. doi: 10.1016/0960-9822(93)90067-x. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Lawrence M. B., Springer T. A. Neutrophils roll on E-selectin. J Immunol. 1993 Dec 1;151(11):6338–6346. [PubMed] [Google Scholar]
  35. Lenter M., Levinovitz A., Isenmann S., Vestweber D. Monospecific and common glycoprotein ligands for E- and P-selectin on myeloid cells. J Cell Biol. 1994 Apr;125(2):471–481. doi: 10.1083/jcb.125.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ley K., Baker J. B., Cybulsky M. I., Gimbrone M. A., Jr, Luscinskas F. W. Intravenous interleukin-8 inhibits granulocyte emigration from rabbit mesenteric venules without altering L-selectin expression or leukocyte rolling. J Immunol. 1993 Dec 1;151(11):6347–6357. [PubMed] [Google Scholar]
  37. 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]
  38. Ley K., Lundgren E., Berger E., Arfors K. E. Shear-dependent inhibition of granulocyte adhesion to cultured endothelium by dextran sulfate. Blood. 1989 Apr;73(5):1324–1330. [PubMed] [Google Scholar]
  39. Ley K., Tedder T. F., Kansas G. S. L-selectin can mediate leukocyte rolling in untreated mesenteric venules in vivo independent of E- or P-selectin. Blood. 1993 Sep 1;82(5):1632–1638. [PubMed] [Google Scholar]
  40. Lo S. K., Detmers P. A., Levin S. M., Wright S. D. Transient adhesion of neutrophils to endothelium. J Exp Med. 1989 May 1;169(5):1779–1793. doi: 10.1084/jem.169.5.1779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Lorant D. E., Patel K. D., McIntyre T. M., McEver R. P., Prescott S. M., Zimmerman G. A. Coexpression of GMP-140 and PAF by endothelium stimulated by histamine or thrombin: a juxtacrine system for adhesion and activation of neutrophils. J Cell Biol. 1991 Oct;115(1):223–234. doi: 10.1083/jcb.115.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lorant D. E., Topham M. K., Whatley R. E., McEver R. P., McIntyre T. M., Prescott S. M., Zimmerman G. A. Inflammatory roles of P-selectin. J Clin Invest. 1993 Aug;92(2):559–570. doi: 10.1172/JCI116623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Luscinskas F. W., Kiely J. M., Ding H., Obin M. S., Hébert C. A., Baker J. B., Gimbrone M. A., Jr In vitro inhibitory effect of IL-8 and other chemoattractants on neutrophil-endothelial adhesive interactions. J Immunol. 1992 Sep 15;149(6):2163–2171. [PubMed] [Google Scholar]
  44. Marks P. W., Hendey B., Maxfield F. R. Attachment to fibronectin or vitronectin makes human neutrophil migration sensitive to alterations in cytosolic free calcium concentration. J Cell Biol. 1991 Jan;112(1):149–158. doi: 10.1083/jcb.112.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Maruyama S., Kubagawa H., Cooper M. D. Activation of human B cells and inhibition of their terminal differentiation by monoclonal anti-mu antibodies. J Immunol. 1985 Jul;135(1):192–199. [PubMed] [Google Scholar]
  46. Maxfield F. R. Regulation of leukocyte locomotion by Ca2+. Trends Cell Biol. 1993 Nov;3(11):386–391. doi: 10.1016/0962-8924(93)90088-i. [DOI] [PubMed] [Google Scholar]
  47. Mayadas T. N., Johnson R. C., Rayburn H., Hynes R. O., Wagner D. D. Leukocyte rolling and extravasation are severely compromised in P selectin-deficient mice. Cell. 1993 Aug 13;74(3):541–554. doi: 10.1016/0092-8674(93)80055-j. [DOI] [PubMed] [Google Scholar]
  48. McEver R. P. Leukocyte-endothelial cell interactions. Curr Opin Cell Biol. 1992 Oct;4(5):840–849. doi: 10.1016/0955-0674(92)90109-p. [DOI] [PubMed] [Google Scholar]
  49. McEver R. P. Selectins. Curr Opin Immunol. 1994 Feb;6(1):75–84. doi: 10.1016/0952-7915(94)90037-x. [DOI] [PubMed] [Google Scholar]
  50. 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]
  51. Moore K. L., Patel K. D., Bruehl R. E., Li F., Johnson D. A., Lichenstein H. S., Cummings R. D., Bainton D. F., McEver R. P. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J Cell Biol. 1995 Feb;128(4):661–671. doi: 10.1083/jcb.128.4.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Moore K. L., Stults N. L., Diaz S., Smith D. F., Cummings R. D., Varki A., McEver R. P. Identification of a specific glycoprotein ligand for P-selectin (CD62) on myeloid cells. J Cell Biol. 1992 Jul;118(2):445–456. doi: 10.1083/jcb.118.2.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Moore K. L., Varki A., McEver R. P. GMP-140 binds to a glycoprotein receptor on human neutrophils: evidence for a lectin-like interaction. J Cell Biol. 1991 Feb;112(3):491–499. doi: 10.1083/jcb.112.3.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Muller W. A., Weigl S. A., Deng X., Phillips D. M. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med. 1993 Aug 1;178(2):449–460. doi: 10.1084/jem.178.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Norgard K. E., Moore K. L., Diaz S., Stults N. L., Ushiyama S., McEver R. P., Cummings R. D., Varki A. Characterization of a specific ligand for P-selectin on myeloid cells. A minor glycoprotein with sialylated O-linked oligosaccharides. J Biol Chem. 1993 Jun 15;268(17):12764–12774. [PubMed] [Google Scholar]
  56. Patel K. D., Lorant E., Jones D. A., Prescott M., McIntyre T. M., Zimmerman G. A. Juxtacrine interactions of endothelial cells with leukocytes: tethering and signaling molecules. Behring Inst Mitt. 1993 Aug;(92):144–164. [PubMed] [Google Scholar]
  57. Picker L. J., Warnock R. A., Burns A. R., Doerschuk C. M., Berg E. L., Butcher E. C. The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140. Cell. 1991 Sep 6;66(5):921–933. doi: 10.1016/0092-8674(91)90438-5. [DOI] [PubMed] [Google Scholar]
  58. Prescott S. M., Zimmerman G. A., McIntyre T. M. Human endothelial cells in culture produce platelet-activating factor (1-alkyl-2-acetyl-sn-glycero-3-phosphocholine) when stimulated with thrombin. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3534–3538. doi: 10.1073/pnas.81.11.3534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Pytowski B., Maxfield F. R., Michl J. Fc and C3bi receptors and the differentiation antigen BH2-Ag are randomly distributed in the plasma membrane of locomoting neutrophils. J Cell Biol. 1990 Mar;110(3):661–668. doi: 10.1083/jcb.110.3.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Rinder H. M., Tracey J. L., Rinder C. S., Leitenberg D., Smith B. R. Neutrophil but not monocyte activation inhibits P-selectin-mediated platelet adhesion. Thromb Haemost. 1994 Nov;72(5):750–756. [PubMed] [Google Scholar]
  61. Rot A. Endothelial cell binding of NAP-1/IL-8: role in neutrophil emigration. Immunol Today. 1992 Aug;13(8):291–294. doi: 10.1016/0167-5699(92)90039-A. [DOI] [PubMed] [Google Scholar]
  62. Sako D., Chang X. J., Barone K. M., Vachino G., White H. M., Shaw G., Veldman G. M., Bean K. M., Ahern T. J., Furie B. Expression cloning of a functional glycoprotein ligand for P-selectin. Cell. 1993 Dec 17;75(6):1179–1186. doi: 10.1016/0092-8674(93)90327-m. [DOI] [PubMed] [Google Scholar]
  63. Sha'afi R. I., Shefcyk J., Yassin R., Molski T. F., Volpi M., Naccache P. H., White J. R., Feinstein M. B., Becker E. L. Is a rise in intracellular concentration of free calcium necessary or sufficient for stimulated cytoskeletal-associated actin? J Cell Biol. 1986 Apr;102(4):1459–1463. doi: 10.1083/jcb.102.4.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Smith C. W., Hollers J. C. Motility and adhesiveness in human neutrophils. Redistribution of chemotactic factor-induced adhesion sites. J Clin Invest. 1980 Apr;65(4):804–812. doi: 10.1172/JCI109731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Spertini O., Kansas G. S., Munro J. M., Griffin J. D., Tedder T. F. Regulation of leukocyte migration by activation of the leukocyte adhesion molecule-1 (LAM-1) selectin. Nature. 1991 Feb 21;349(6311):691–694. doi: 10.1038/349691a0. [DOI] [PubMed] [Google Scholar]
  66. Spertini O., Luscinskas F. W., Kansas G. S., Munro J. M., Griffin J. D., Gimbrone M. A., Jr, Tedder T. F. Leukocyte adhesion molecule-1 (LAM-1, L-selectin) interacts with an inducible endothelial cell ligand to support leukocyte adhesion. J Immunol. 1991 Oct 15;147(8):2565–2573. [PubMed] [Google Scholar]
  67. Ushiyama S., Laue T. M., Moore K. L., Erickson H. P., McEver R. P. Structural and functional characterization of monomeric soluble P-selectin and comparison with membrane P-selectin. J Biol Chem. 1993 Jul 15;268(20):15229–15237. [PubMed] [Google Scholar]
  68. Westlin W. F., Kiely J. M., Gimbrone M. A., Jr Interleukin-8 induces changes in human neutrophil actin conformation and distribution: relationship to inhibition of adhesion to cytokine-activated endothelium. J Leukoc Biol. 1992 Jul;52(1):43–51. doi: 10.1002/jlb.52.1.43. [DOI] [PubMed] [Google Scholar]
  69. Ye R. D., Prossnitz E. R., Zou A. H., Cochrane C. G. Characterization of a human cDNA that encodes a functional receptor for platelet activating factor. Biochem Biophys Res Commun. 1991 Oct 15;180(1):105–111. doi: 10.1016/s0006-291x(05)81261-6. [DOI] [PubMed] [Google Scholar]
  70. Zheng J., Buxbaum R. E., Heidemann S. R. Measurements of growth cone adhesion to culture surfaces by micromanipulation. J Cell Biol. 1994 Dec;127(6 Pt 2):2049–2060. doi: 10.1083/jcb.127.6.2049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Zimmerman G. A., Lorant D. E., McIntyre T. M., Prescott S. M. Juxtacrine intercellular signaling: another way to do it. Am J Respir Cell Mol Biol. 1993 Dec;9(6):573–577. doi: 10.1165/ajrcmb/9.6.573. [DOI] [PubMed] [Google Scholar]
  72. Zimmerman G. A., McIntyre T. M., Mehra M., Prescott S. M. Endothelial cell-associated platelet-activating factor: a novel mechanism for signaling intercellular adhesion. J Cell Biol. 1990 Feb;110(2):529–540. doi: 10.1083/jcb.110.2.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Zimmerman G. A., McIntyre T. M., Prescott S. M. Thrombin stimulates the adherence of neutrophils to human endothelial cells in vitro. J Clin Invest. 1985 Dec;76(6):2235–2246. doi: 10.1172/JCI112232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Zimmerman G. A., Prescott S. M., McIntyre T. M. Endothelial cell interactions with granulocytes: tethering and signaling molecules. Immunol Today. 1992 Mar;13(3):93–100. doi: 10.1016/0167-5699(92)90149-2. [DOI] [PubMed] [Google Scholar]
  75. von Andrian U. H., Chambers J. D., Berg E. L., Michie S. A., Brown D. A., Karolak D., Ramezani L., Berger E. M., Arfors K. E., Butcher E. C. L-selectin mediates neutrophil rolling in inflamed venules through sialyl LewisX-dependent and -independent recognition pathways. Blood. 1993 Jul 1;82(1):182–191. [PubMed] [Google Scholar]
  76. 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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