Skip to main content
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1998 May 1;101(9):2017–2024. doi: 10.1172/JCI2688

The C-C chemokine receptor CCR3 participates in stimulation of eosinophil arrest on inflammatory endothelium in shear flow.

J Kitayama 1, C R Mackay 1, P D Ponath 1, T A Springer 1
PMCID: PMC508789  PMID: 9576767

Abstract

Chemokines are widely hypothesized to stimulate firm adhesion of leukocytes on endothelium in shear flow. Thus far, this has been demonstrated experimentally for exogenously added chemoattractants, but not for those released by endothelium. We found that human umbilical cord endothelial cells (HUVEC) stimulated with TNF-alpha and IFN-gamma secreted eosinophil chemoattractants into the culture supernatant. This material induced transendothelial chemotaxis, stimulated eosinophil binding to purified intercellular adhesion molecule 1, and augmented binding to purified vascular cell adhesion molecule 1 in a 3-min static assay. Chemotaxis and stimulation of adhesion were abrogated completely by the pretreatment of eosinophils with an mAb to the C-C chemokine receptor 3 (CCR3). Eosinophils accumulated efficiently on HUVEC stimulated with TNF-alpha and IFN-gamma in shear flow at 1.5 dyn/cm2. CCR3 mAb slightly but significantly reduced eosinophil arrest and accumulation, by preventing development of firm adhesion by some of the tethered eosinophils, so that they detached within 30 s after the initial tethering. In the presence of mAb to the alpha4 integrin subunit, the effect of CCR3 mAb was more prominent, and approximately half of eosinophil arrest and accumulation was abolished. Inhibition by CCR3 mAb in the presence of beta2 integrin mAb was similar to that in control eosinophils. This is the first evidence that endothelial cell-derived chemokines can activate firm adhesion through alpha4 and beta2 integrins even in the presence of shear flow.

Full Text

The Full Text of this article is available as a PDF (208.0 KB).

Selected References

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

  1. Alon R., Kassner P. D., Carr M. W., Finger E. B., Hemler M. E., Springer T. A. The integrin VLA-4 supports tethering and rolling in flow on VCAM-1. J Cell Biol. 1995 Mar;128(6):1243–1253. doi: 10.1083/jcb.128.6.1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baggiolini M., Dahinden C. A. CC chemokines in allergic inflammation. Immunol Today. 1994 Mar;15(3):127–133. doi: 10.1016/0167-5699(94)90156-2. [DOI] [PubMed] [Google Scholar]
  3. Baggiolini M., Dewald B., Moser B. Interleukin-8 and related chemotactic cytokines--CXC and CC chemokines. Adv Immunol. 1994;55:97–179. [PubMed] [Google Scholar]
  4. Baggiolini M., Walz A., Kunkel S. L. Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils. J Clin Invest. 1989 Oct;84(4):1045–1049. doi: 10.1172/JCI114265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berlin C., Bargatze R. F., Campbell J. J., von Andrian U. H., Szabo M. C., Hasslen S. R., Nelson R. D., Berg E. L., Erlandsen S. L., Butcher E. C. alpha 4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell. 1995 Feb 10;80(3):413–422. doi: 10.1016/0092-8674(95)90491-3. [DOI] [PubMed] [Google Scholar]
  6. Bochner B. S., Luscinskas F. W., Gimbrone M. A., Jr, Newman W., Sterbinsky S. A., Derse-Anthony C. P., Klunk D., Schleimer R. P. Adhesion of human basophils, eosinophils, and neutrophils to interleukin 1-activated human vascular endothelial cells: contributions of endothelial cell adhesion molecules. J Exp Med. 1991 Jun 1;173(6):1553–1557. doi: 10.1084/jem.173.6.1553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bousquet J., Chanez P., Lacoste J. Y., Barnéon G., Ghavanian N., Enander I., Venge P., Ahlstedt S., Simony-Lafontaine J., Godard P. Eosinophilic inflammation in asthma. N Engl J Med. 1990 Oct 11;323(15):1033–1039. doi: 10.1056/NEJM199010113231505. [DOI] [PubMed] [Google Scholar]
  8. Butcher E. C. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell. 1991 Dec 20;67(6):1033–1036. doi: 10.1016/0092-8674(91)90279-8. [DOI] [PubMed] [Google Scholar]
  9. Camussi G., Bussolino F., Salvidio G., Baglioni C. Tumor necrosis factor/cachectin stimulates peritoneal macrophages, polymorphonuclear neutrophils, and vascular endothelial cells to synthesize and release platelet-activating factor. J Exp Med. 1987 Nov 1;166(5):1390–1404. doi: 10.1084/jem.166.5.1390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dahinden C. A., Geiser T., Brunner T., von Tscharner V., Caput D., Ferrara P., Minty A., Baggiolini M. Monocyte chemotactic protein 3 is a most effective basophil- and eosinophil-activating chemokine. J Exp Med. 1994 Feb 1;179(2):751–756. doi: 10.1084/jem.179.2.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Daugherty B. L., Siciliano S. J., DeMartino J. A., Malkowitz L., Sirotina A., Springer M. S. Cloning, expression, and characterization of the human eosinophil eotaxin receptor. J Exp Med. 1996 May 1;183(5):2349–2354. doi: 10.1084/jem.183.5.2349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Detmers P. A., Powell D. E., Walz A., Clark-Lewis I., Baggiolini M., Cohn Z. A. Differential effects of neutrophil-activating peptide 1/IL-8 and its homologues on leukocyte adhesion and phagocytosis. J Immunol. 1991 Dec 15;147(12):4211–4217. [PubMed] [Google Scholar]
  13. Dobrina A., Menegazzi R., Carlos T. M., Nardon E., Cramer R., Zacchi T., Harlan J. M., Patriarca P. Mechanisms of eosinophil adherence to cultured vascular endothelial cells. Eosinophils bind to the cytokine-induced ligand vascular cell adhesion molecule-1 via the very late activation antigen-4 integrin receptor. J Clin Invest. 1991 Jul;88(1):20–26. doi: 10.1172/JCI115278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ebisawa M., Yamada T., Bickel C., Klunk D., Schleimer R. P. Eosinophil transendothelial migration induced by cytokines. III. Effect of the chemokine RANTES. J Immunol. 1994 Sep 1;153(5):2153–2160. [PubMed] [Google Scholar]
  15. Elsner J., Höchstetter R., Kimmig D., Kapp A. Human eotaxin represents a potent activator of the respiratory burst of human eosinophils. Eur J Immunol. 1996 Aug;26(8):1919–1925. doi: 10.1002/eji.1830260837. [DOI] [PubMed] [Google Scholar]
  16. Forssmann U., Uguccioni M., Loetscher P., Dahinden C. A., Langen H., Thelen M., Baggiolini M. Eotaxin-2, a novel CC chemokine that is selective for the chemokine receptor CCR3, and acts like eotaxin on human eosinophil and basophil leukocytes. J Exp Med. 1997 Jun 16;185(12):2171–2176. doi: 10.1084/jem.185.12.2171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gimbrone M. A., Jr Culture of vascular endothelium. Prog Hemost Thromb. 1976;3:1–28. [PubMed] [Google Scholar]
  18. Gleich G. J., Adolphson C. R. The eosinophilic leukocyte: structure and function. Adv Immunol. 1986;39:177–253. doi: 10.1016/s0065-2776(08)60351-x. [DOI] [PubMed] [Google Scholar]
  19. Gopalan P. K., Smith C. W., Lu H., Berg E. L., McIntire L. V., Simon S. I. Neutrophil CD18-dependent arrest on intercellular adhesion molecule 1 (ICAM-1) in shear flow can be activated through L-selectin. J Immunol. 1997 Jan 1;158(1):367–375. [PubMed] [Google Scholar]
  20. Hansel T. T., Pound J. D., Pilling D., Kitas G. D., Salmon M., Gentle T. A., Lee S. S., Thompson R. A. Purification of human blood eosinophils by negative selection using immunomagnetic beads. J Immunol Methods. 1989 Aug 15;122(1):97–103. doi: 10.1016/0022-1759(89)90339-6. [DOI] [PubMed] [Google Scholar]
  21. Heath H., Qin S., Rao P., Wu L., LaRosa G., Kassam N., Ponath P. D., Mackay C. R. Chemokine receptor usage by human eosinophils. The importance of CCR3 demonstrated using an antagonistic monoclonal antibody. J Clin Invest. 1997 Jan 15;99(2):178–184. doi: 10.1172/JCI119145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Henriques G. M., Miotla J. M., Cordeiro S. B., Wolitzky B. A., Woolley S. T., Hellewell P. G. Selectins mediate eosinophil recruitment in vivo: a comparison with their role in neutrophil influx. Blood. 1996 Jun 15;87(12):5297–5304. [PubMed] [Google Scholar]
  23. Honda S., Campbell J. J., Andrew D. P., Engelhardt B., Butcher B. A., Warnock R. A., Ye R. D., Butcher E. C. Ligand-induced adhesion to activated endothelium and to vascular cell adhesion molecule-1 in lymphocytes transfected with the N-formyl peptide receptor. J Immunol. 1994 Apr 15;152(8):4026–4035. [PubMed] [Google Scholar]
  24. Honda Z., Nakamura M., Miki I., Minami M., Watanabe T., Seyama Y., Okado H., Toh H., Ito K., Miyamoto T. Cloning by functional expression of platelet-activating factor receptor from guinea-pig lung. Nature. 1991 Jan 24;349(6307):342–346. doi: 10.1038/349342a0. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Kameyoshi Y., Dörschner A., Mallet A. I., Christophers E., Schröder J. M. Cytokine RANTES released by thrombin-stimulated platelets is a potent attractant for human eosinophils. J Exp Med. 1992 Aug 1;176(2):587–592. doi: 10.1084/jem.176.2.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kimani G., Tonnesen M. G., Henson P. M. Stimulation of eosinophil adherence to human vascular endothelial cells in vitro by platelet-activating factor. J Immunol. 1988 May 1;140(9):3161–3166. [PubMed] [Google Scholar]
  28. Kita H., Gleich G. J. Chemokines active on eosinophils: potential roles in allergic inflammation. J Exp Med. 1996 Jun 1;183(6):2421–2426. doi: 10.1084/jem.183.6.2421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kitayama J., Carr M. W., Roth S. J., Buccola J., Springer T. A. Contrasting responses to multiple chemotactic stimuli in transendothelial migration: heterologous desensitization in neutrophils and augmentation of migration in eosinophils. J Immunol. 1997 Mar 1;158(5):2340–2349. [PubMed] [Google Scholar]
  30. Kuijpers T. W., Hakkert B. C., Hoogerwerf M., Leeuwenberg J. F., Roos D. Role of endothelial leukocyte adhesion molecule-1 and platelet-activating factor in neutrophil adherence to IL-1-prestimulated endothelial cells. Endothelial leukocyte adhesion molecule-1-mediated CD18 activation. J Immunol. 1991 Aug 15;147(4):1369–1376. [PubMed] [Google Scholar]
  31. Kuijpers T. W., Hoogerwerf M., van der Laan L. J., Nagel G., van der Schoot C. E., Grunert F., Roos D. CD66 nonspecific cross-reacting antigens are involved in neutrophil adherence to cytokine-activated endothelial cells. J Cell Biol. 1992 Jul;118(2):457–466. doi: 10.1083/jcb.118.2.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Lawrence M. B., Springer T. A. Neutrophils roll on E-selectin. J Immunol. 1993 Dec 1;151(11):6338–6346. [PubMed] [Google Scholar]
  34. Lo S. K., Lee S., Ramos R. A., Lobb R., Rosa M., Chi-Rosso G., Wright S. D. Endothelial-leukocyte adhesion molecule 1 stimulates the adhesive activity of leukocyte integrin CR3 (CD11b/CD18, Mac-1, alpha m beta 2) on human neutrophils. J Exp Med. 1991 Jun 1;173(6):1493–1500. doi: 10.1084/jem.173.6.1493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. Luscinskas F. W., Kansas G. S., Ding H., Pizcueta P., Schleiffenbaum B. E., Tedder T. F., Gimbrone M. A., Jr Monocyte rolling, arrest and spreading on IL-4-activated vascular endothelium under flow is mediated via sequential action of L-selectin, beta 1-integrins, and beta 2-integrins. J Cell Biol. 1994 Jun;125(6):1417–1427. doi: 10.1083/jcb.125.6.1417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Macconi D., Foppolo M., Paris S., Noris M., Aiello S., Remuzzi G., Remuzzi A. PAF mediates neutrophil adhesion to thrombin or TNF-stimulated endothelial cells under shear stress. Am J Physiol. 1995 Jul;269(1 Pt 1):C42–C47. doi: 10.1152/ajpcell.1995.269.1.C42. [DOI] [PubMed] [Google Scholar]
  39. Mackay C. R. Chemokine receptors and T cell chemotaxis. J Exp Med. 1996 Sep 1;184(3):799–802. doi: 10.1084/jem.184.3.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Marfaing-Koka A., Devergne O., Gorgone G., Portier A., Schall T. J., Galanaud P., Emilie D. Regulation of the production of the RANTES chemokine by endothelial cells. Synergistic induction by IFN-gamma plus TNF-alpha and inhibition by IL-4 and IL-13. J Immunol. 1995 Feb 15;154(4):1870–1878. [PubMed] [Google Scholar]
  41. Marlin S. D., Staunton D. E., Springer T. A., Stratowa C., Sommergruber W., Merluzzi V. J. A soluble form of intercellular adhesion molecule-1 inhibits rhinovirus infection. Nature. 1990 Mar 1;344(6261):70–72. doi: 10.1038/344070a0. [DOI] [PubMed] [Google Scholar]
  42. McLellan A. D., Sorg R. V., Williams L. A., Hart D. N. Human dendritic cells activate T lymphocytes via a CD40: CD40 ligand-dependent pathway. Eur J Immunol. 1996 Jun;26(6):1204–1210. doi: 10.1002/eji.1830260603. [DOI] [PubMed] [Google Scholar]
  43. Noso N., Proost P., Van Damme J., Schröder J. M. Human monocyte chemotactic proteins-2 and 3 (MCP-2 and MCP-3) attract human eosinophils and desensitize the chemotactic responses towards RANTES. Biochem Biophys Res Commun. 1994 May 16;200(3):1470–1476. doi: 10.1006/bbrc.1994.1616. [DOI] [PubMed] [Google Scholar]
  44. Pepinsky B., Hession C., Chen L. L., Moy P., Burkly L., Jakubowski A., Chow E. P., Benjamin C., Chi-Rosso G., Luhowskyj S. Structure/function studies on vascular cell adhesion molecule-1. J Biol Chem. 1992 Sep 5;267(25):17820–17826. [PubMed] [Google Scholar]
  45. Ponath P. D., Qin S., Post T. W., Wang J., Wu L., Gerard N. P., Newman W., Gerard C., Mackay C. R. Molecular cloning and characterization of a human eotaxin receptor expressed selectively on eosinophils. J Exp Med. 1996 Jun 1;183(6):2437–2448. doi: 10.1084/jem.183.6.2437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Ponath P. D., Qin S., Ringler D. J., Clark-Lewis I., Wang J., Kassam N., Smith H., Shi X., Gonzalo J. A., Newman W. Cloning of the human eosinophil chemoattractant, eotaxin. Expression, receptor binding, and functional properties suggest a mechanism for the selective recruitment of eosinophils. J Clin Invest. 1996 Feb 1;97(3):604–612. doi: 10.1172/JCI118456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Pons F., Rossi A. G., Norman K. E., Williams T. J., Nourshargh S. Role of platelet-activating factor (PAF) in platelet accumulation in rabbit skin: effect of the novel long-acting PAF antagonist, UK-74,505. Br J Pharmacol. 1993 May;109(1):234–242. doi: 10.1111/j.1476-5381.1993.tb13559.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. 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]
  49. Rot A., Krieger M., Brunner T., Bischoff S. C., Schall T. J., Dahinden C. A. RANTES and macrophage inflammatory protein 1 alpha induce the migration and activation of normal human eosinophil granulocytes. J Exp Med. 1992 Dec 1;176(6):1489–1495. doi: 10.1084/jem.176.6.1489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Roth S. J., Carr M. W., Rose S. S., Springer T. A. Characterization of transendothelial chemotaxis of T lymphocytes. J Immunol Methods. 1995 Dec 15;188(1):97–116. doi: 10.1016/0022-1759(95)00208-1. [DOI] [PubMed] [Google Scholar]
  51. Rothenberg M. E., Luster A. D., Leder P. Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8960–8964. doi: 10.1073/pnas.92.19.8960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Sanchez-Madrid F., Nagy J. A., Robbins E., Simon P., Springer T. A. A human leukocyte differentiation antigen family with distinct alpha-subunits and a common beta-subunit: the lymphocyte function-associated antigen (LFA-1), the C3bi complement receptor (OKM1/Mac-1), and the p150,95 molecule. J Exp Med. 1983 Dec 1;158(6):1785–1803. doi: 10.1084/jem.158.6.1785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Sanz M. J., Weg V. B., Walsh D. T., Williams T. J., Nourshargh S. Differential effects of the PAF receptor antagonist UK-74,505 on neutrophil and eosinophil accumulation in guinea-pig skin. Br J Pharmacol. 1994 Oct;113(2):513–521. doi: 10.1111/j.1476-5381.1994.tb17019.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Simon S. I., Burns A. R., Taylor A. D., Gopalan P. K., Lynam E. B., Sklar L. A., Smith C. W. L-selectin (CD62L) cross-linking signals neutrophil adhesive functions via the Mac-1 (CD11b/CD18) beta 2-integrin. J Immunol. 1995 Aug 1;155(3):1502–1514. [PubMed] [Google Scholar]
  55. Springer T. A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994 Jan 28;76(2):301–314. doi: 10.1016/0092-8674(94)90337-9. [DOI] [PubMed] [Google Scholar]
  56. Sriramarao P., Norton C. R., Borgstrom P., DiScipio R. G., Wolitzky B. A., Broide D. H. E-selectin preferentially supports neutrophil but not eosinophil rolling under conditions of flow in vitro and in vivo. J Immunol. 1996 Nov 15;157(10):4672–4680. [PubMed] [Google Scholar]
  57. Tanaka Y., Adams D. H., Hubscher S., Hirano H., Siebenlist U., Shaw S. T-cell adhesion induced by proteoglycan-immobilized cytokine MIP-1 beta. Nature. 1993 Jan 7;361(6407):79–82. doi: 10.1038/361079a0. [DOI] [PubMed] [Google Scholar]
  58. Tenscher K., Metzner B., Schöpf E., Norgauer J., Czech W. Recombinant human eotaxin induces oxygen radical production, Ca(2+)-mobilization, actin reorganization, and CD11b upregulation in human eosinophils via a pertussis toxin-sensitive heterotrimeric guanine nucleotide-binding protein. Blood. 1996 Oct 15;88(8):3195–3199. [PubMed] [Google Scholar]
  59. Uguccioni M., Loetscher P., Forssmann U., Dewald B., Li H., Lima S. H., Li Y., Kreider B., Garotta G., Thelen M. Monocyte chemotactic protein 4 (MCP-4), a novel structural and functional analogue of MCP-3 and eotaxin. J Exp Med. 1996 May 1;183(5):2379–2384. doi: 10.1084/jem.183.5.2379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Walsh G. M., Mermod J. J., Hartnell A., Kay A. B., Wardlaw A. J. Human eosinophil, but not neutrophil, adherence to IL-1-stimulated human umbilical vascular endothelial cells is alpha 4 beta 1 (very late antigen-4) dependent. J Immunol. 1991 May 15;146(10):3419–3423. [PubMed] [Google Scholar]
  61. Walsh G. M., Symon F. A., Lazarovils A. L., Wardlaw A. J. Integrin alpha 4 beta 7 mediates human eosinophil interaction with MAdCAM-1, VCAM-1 and fibronectin. Immunology. 1996 Sep;89(1):112–119. doi: 10.1046/j.1365-2567.1996.d01-713.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Weber C., Kitayama J., Springer T. A. Differential regulation of beta 1 and beta 2 integrin avidity by chemoattractants in eosinophils. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10939–10944. doi: 10.1073/pnas.93.20.10939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Weller P. F., Rand T. H., Goelz S. E., Chi-Rosso G., Lobb R. R. Human eosinophil adherence to vascular endothelium mediated by binding to vascular cell adhesion molecule 1 and endothelial leukocyte adhesion molecule 1. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7430–7433. doi: 10.1073/pnas.88.16.7430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. 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]
  65. Wu L., Ruffing N., Shi X., Newman W., Soler D., Mackay C. R., Qin S. Discrete steps in binding and signaling of interleukin-8 with its receptor. J Biol Chem. 1996 Dec 6;271(49):31202–31209. doi: 10.1074/jbc.271.49.31202. [DOI] [PubMed] [Google Scholar]
  66. 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]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES