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. 1996 Mar 15;97(6):1525–1534. doi: 10.1172/JCI118575

Activated platelets signal chemokine synthesis by human monocytes.

A S Weyrich 1, M R Elstad 1, R P McEver 1, T M McIntyre 1, K L Moore 1, J H Morrissey 1, S M Prescott 1, G A Zimmerman 1
PMCID: PMC507213  PMID: 8617886

Abstract

Human blood monocytes adhere rapidly and for prolonged periods to activated platelets that display P-selectin, an adhesion protein that recognizes a specific ligand on leukocytes, P-selectin glycoprotein-1. We previously demonstrated that P-selectin regulates expression and secretion of cytokines by stimulated monocytes when it is presented in a purified, immobilized form or by transfected cells. Here we show that thrombin-activated platelets induce the expression and secretion of monocyte chemotactic protein-1 and IL-8 by monocytes. Enhanced monokine synthesis requires engagement of P-selectin glycoprotein-1 on the leukocyte by P-selectin on the platelet. Secretion of the chemokines is not, however, directly signaled by P-selectin; instead, tethering of the monocytes by P-selectin is required for their activation by RANTES (regulated upon activation normal T cell expressed presumed secreted), a platelet chemokine not previously known to induce immediate-early gene products in monocytes. Adhesion of monocytes to activated platelets results in nuclear translocation of p65 (RelA), a component of the NF-kappaB family of transcription factors that binds kappaB sequences in the regulatory regions of monocyte chemotactic protein-1, IL-8, and other immediate-early genes. However, expression of tissue factor, a coagulation protein that also has a kappaB sequence in the 5' regulatory region of its gene, is not induced in monocytes adherent to activated platelets. Thus, contact of monocytes with activated platelets differentially affects the expression of monocyte products. These experiments suggest that activated platelets regulate chemokine secretion by monocytes in inflammatory lesions in vivo and provide a model for the study of gene regulation in cell-cell interactions.

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Selected References

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  1. Bacon K. B., Premack B. A., Gardner P., Schall T. J. Activation of dual T cell signaling pathways by the chemokine RANTES. Science. 1995 Sep 22;269(5231):1727–1730. doi: 10.1126/science.7569902. [DOI] [PubMed] [Google Scholar]
  2. Baeuerle P. A., Henkel T. Function and activation of NF-kappa B in the immune system. Annu Rev Immunol. 1994;12:141–179. doi: 10.1146/annurev.iy.12.040194.001041. [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. Bevilacqua M. P., Pober J. S., Majeau G. R., Cotran R. S., Gimbrone M. A., Jr Interleukin 1 (IL-1) induces biosynthesis and cell surface expression of procoagulant activity in human vascular endothelial cells. J Exp Med. 1984 Aug 1;160(2):618–623. doi: 10.1084/jem.160.2.618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bischoff S. C., Krieger M., Brunner T., Rot A., von Tscharner V., Baggiolini M., Dahinden C. A. RANTES and related chemokines activate human basophil granulocytes through different G protein-coupled receptors. Eur J Immunol. 1993 Mar;23(3):761–767. doi: 10.1002/eji.1830230329. [DOI] [PubMed] [Google Scholar]
  6. Celi A., Pellegrini G., Lorenzet R., De Blasi A., Ready N., Furie B. C., Furie B. P-selectin induces the expression of tissue factor on monocytes. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8767–8771. doi: 10.1073/pnas.91.19.8767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Collins T. Endothelial nuclear factor-kappa B and the initiation of the atherosclerotic lesion. Lab Invest. 1993 May;68(5):499–508. [PubMed] [Google Scholar]
  8. Colotta F., Sciacca F. L., Sironi M., Luini W., Rabiet M. J., Mantovani A. Expression of monocyte chemotactic protein-1 by monocytes and endothelial cells exposed to thrombin. Am J Pathol. 1994 May;144(5):975–985. [PMC free article] [PubMed] [Google Scholar]
  9. Colucci M., Balconi G., Lorenzet R., Pietra A., Locati D., Donati M. B., Semeraro N. Cultured human endothelial cells generate tissue factor in response to endotoxin. J Clin Invest. 1983 Jun;71(6):1893–1896. doi: 10.1172/JCI110945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Diacovo T. G., deFougerolles A. R., Bainton D. F., Springer T. A. A functional integrin ligand on the surface of platelets: intercellular adhesion molecule-2. J Clin Invest. 1994 Sep;94(3):1243–1251. doi: 10.1172/JCI117442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Drake T. A., Ruf W., Morrissey J. H., Edgington T. S. Functional tissue factor is entirely cell surface expressed on lipopolysaccharide-stimulated human blood monocytes and a constitutively tissue factor-producing neoplastic cell line. J Cell Biol. 1989 Jul;109(1):389–395. doi: 10.1083/jcb.109.1.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Elstad M. R., La Pine T. R., Cowley F. S., McEver R. P., McIntyre T. M., Prescott S. M., Zimmerman G. A. P-selectin regulates platelet-activating factor synthesis and phagocytosis by monocytes. J Immunol. 1995 Aug 15;155(4):2109–2122. [PubMed] [Google Scholar]
  14. Elstad M. R., McIntyre T. M., Prescott S. M., Zimmerman G. A. The interaction of leukocytes with platelets in blood coagulation. Curr Opin Hematol. 1995 Jan;2(1):47–54. doi: 10.1097/00062752-199502010-00007. [DOI] [PubMed] [Google Scholar]
  15. Elstad M. R., Prescott S. M., McIntyre T. M., Zimmerman G. A. Synthesis and release of platelet-activating factor by stimulated human mononuclear phagocytes. J Immunol. 1988 Mar 1;140(5):1618–1624. [PubMed] [Google Scholar]
  16. Faucette K. J., Parker C. J., McCluskey T., Bernshaw N. J., Rodgers G. M. Induction of tissue factor activity in endothelial cells and monocytes by a modified form of albumin present in normal human plasma. Blood. 1992 Jun 1;79(11):2888–2895. [PubMed] [Google Scholar]
  17. Foxall C., Watson S. R., Dowbenko D., Fennie C., Lasky L. A., Kiso M., Hasegawa A., Asa D., Brandley B. K. The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis(x) oligosaccharide. J Cell Biol. 1992 May;117(4):895–902. doi: 10.1083/jcb.117.4.895. [DOI] [PMC free article] [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. George J. N., Pickett E. B., Saucerman S., McEver R. P., Kunicki T. J., Kieffer N., Newman P. J. Platelet surface glycoproteins. Studies on resting and activated platelets and platelet membrane microparticles in normal subjects, and observations in patients during adult respiratory distress syndrome and cardiac surgery. J Clin Invest. 1986 Aug;78(2):340–348. doi: 10.1172/JCI112582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gregory S. A., Kornbluth R. S., Helin H., Remold H. G., Edgington T. S. Monocyte procoagulant inducing factor: a lymphokine involved in the T cell-instructed monocyte procoagulant response to antigen. J Immunol. 1986 Nov 15;137(10):3231–3239. [PubMed] [Google Scholar]
  21. Hamburger S. A., McEver R. P. GMP-140 mediates adhesion of stimulated platelets to neutrophils. Blood. 1990 Feb 1;75(3):550–554. [PubMed] [Google Scholar]
  22. Hansen S. K., Baeuerle P. A., Blasi F. Purification, reconstitution, and I kappa B association of the c-Rel-p65 (RelA) complex, a strong activator of transcription. Mol Cell Biol. 1994 Apr;14(4):2593–2603. doi: 10.1128/mcb.14.4.2593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hattori R., Hamilton K. K., Fugate R. D., McEver R. P., Sims P. J. Stimulated secretion of endothelial von Willebrand factor is accompanied by rapid redistribution to the cell surface of the intracellular granule membrane protein GMP-140. J Biol Chem. 1989 May 15;264(14):7768–7771. [PubMed] [Google Scholar]
  24. Hsu-Lin S., Berman C. L., Furie B. C., August D., Furie B. A platelet membrane protein expressed during platelet activation and secretion. Studies using a monoclonal antibody specific for thrombin-activated platelets. J Biol Chem. 1984 Jul 25;259(14):9121–9126. [PubMed] [Google Scholar]
  25. Juliano R. L., Haskill S. Signal transduction from the extracellular matrix. J Cell Biol. 1993 Feb;120(3):577–585. doi: 10.1083/jcb.120.3.577. [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. Kieffer N., Phillips D. R. Platelet membrane glycoproteins: functions in cellular interactions. Annu Rev Cell Biol. 1990;6:329–357. doi: 10.1146/annurev.cb.06.110190.001553. [DOI] [PubMed] [Google Scholar]
  28. Kravchenko V. V., Pan Z., Han J., Herbert J. M., Ulevitch R. J., Ye R. D. Platelet-activating factor induces NF-kappa B activation through a G protein-coupled pathway. J Biol Chem. 1995 Jun 23;270(25):14928–14934. doi: 10.1074/jbc.270.25.14928. [DOI] [PubMed] [Google Scholar]
  29. Kunsch C., Rosen C. A. NF-kappa B subunit-specific regulation of the interleukin-8 promoter. Mol Cell Biol. 1993 Oct;13(10):6137–6146. doi: 10.1128/mcb.13.10.6137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lalmanach-Girard A. C., Chiles T. C., Parker D. C., Rothstein T. L. T cell-dependent induction of NF-kappa B in B cells. J Exp Med. 1993 Apr 1;177(4):1215–1219. doi: 10.1084/jem.177.4.1215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Lehr H. A., Frei B., Arfors K. E. Vitamin C prevents cigarette smoke-induced leukocyte aggregation and adhesion to endothelium in vivo. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7688–7692. doi: 10.1073/pnas.91.16.7688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lehr H. A., Olofsson A. M., Carew T. E., Vajkoczy P., von Andrian U. H., Hübner C., Berndt M. C., Steinberg D., Messmer K., Arfors K. E. P-selectin mediates the interaction of circulating leukocytes with platelets and microvascular endothelium in response to oxidized lipoprotein in vivo. Lab Invest. 1994 Sep;71(3):380–386. [PubMed] [Google Scholar]
  34. Levine S. P., Knieriem L. K., Rager M. A. Platelet factor 4 and the platelet secreted proteoglycan: immunologic characterization by crossed immunoelectrophoresis. Blood. 1990 Feb 15;75(4):902–910. [PubMed] [Google Scholar]
  35. Lorant D. E., McEver R. P., McIntyre T. M., Moore K. L., Prescott S. M., Zimmerman G. A. Activation of polymorphonuclear leukocytes reduces their adhesion to P-selectin and causes redistribution of ligands for P-selectin on their surfaces. J Clin Invest. 1995 Jul;96(1):171–182. doi: 10.1172/JCI118018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. McEver R. P., Martin M. N. A monoclonal antibody to a membrane glycoprotein binds only to activated platelets. J Biol Chem. 1984 Aug 10;259(15):9799–9804. [PubMed] [Google Scholar]
  39. McEver R. P., Moore K. L., Cummings R. D. Leukocyte trafficking mediated by selectin-carbohydrate interactions. J Biol Chem. 1995 May 12;270(19):11025–11028. doi: 10.1074/jbc.270.19.11025. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. 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]
  42. 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]
  43. Morrissey J. H., Revak D., Tejada P., Fair D. S., Edgington T. S. Resolution of monomeric and heterodimeric forms of tissue factor, the high-affinity cellular receptor for factor VII. Thromb Res. 1988 May 15;50(4):481–493. doi: 10.1016/0049-3848(88)90197-1. [DOI] [PubMed] [Google Scholar]
  44. Munro J. M., Cotran R. S. The pathogenesis of atherosclerosis: atherogenesis and inflammation. Lab Invest. 1988 Mar;58(3):249–261. [PubMed] [Google Scholar]
  45. Murphy P. M. The molecular biology of leukocyte chemoattractant receptors. Annu Rev Immunol. 1994;12:593–633. doi: 10.1146/annurev.iy.12.040194.003113. [DOI] [PubMed] [Google Scholar]
  46. Nagata K., Tsuji T., Hanai N., Irimura T. Role of O-linked carbohydrate chains on leukocyte cell membranes in platelet-induced leukocyte activation. J Biol Chem. 1994 Sep 16;269(37):23290–23295. [PubMed] [Google Scholar]
  47. Nagata K., Tsuji T., Todoroki N., Katagiri Y., Tanoue K., Yamazaki H., Hanai N., Irimura T. Activated platelets induce superoxide anion release by monocytes and neutrophils through P-selectin (CD62). J Immunol. 1993 Sep 15;151(6):3267–3273. [PubMed] [Google Scholar]
  48. Nawroth P. P., Stern D. M. Modulation of endothelial cell hemostatic properties by tumor necrosis factor. J Exp Med. 1986 Mar 1;163(3):740–745. doi: 10.1084/jem.163.3.740. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. 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]
  50. Oeth P. A., Parry G. C., Kunsch C., Nantermet P., Rosen C. A., Mackman N. Lipopolysaccharide induction of tissue factor gene expression in monocytic cells is mediated by binding of c-Rel/p65 heterodimers to a kappa B-like site. Mol Cell Biol. 1994 Jun;14(6):3772–3781. doi: 10.1128/mcb.14.6.3772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Packham M. A. Role of platelets in thrombosis and hemostasis. Can J Physiol Pharmacol. 1994 Mar;72(3):278–284. doi: 10.1139/y94-043. [DOI] [PubMed] [Google Scholar]
  52. Palabrica T., Lobb R., Furie B. C., Aronovitz M., Benjamin C., Hsu Y. M., Sajer S. A., Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature. 1992 Oct 29;359(6398):848–851. doi: 10.1038/359848a0. [DOI] [PubMed] [Google Scholar]
  53. Parry G. C., Mackman N. A set of inducible genes expressed by activated human monocytic and endothelial cells contain kappa B-like sites that specifically bind c-Rel-p65 heterodimers. J Biol Chem. 1994 Aug 19;269(33):20823–20825. [PubMed] [Google Scholar]
  54. Prescott S. M., Seeger A. R., Zimmerman G. A., McIntyre T. M., Maraganore J. M. Hirudin-based peptides block the inflammatory effects of thrombin on endothelial cells. J Biol Chem. 1990 Jun 15;265(17):9614–9616. [PubMed] [Google Scholar]
  55. Rinder H. M., Snyder E. L., Bonan J. L., Napychank P. A., Malkus H., Smith B. R. Activation in stored platelet concentrates: correlation between membrane expression of P-selectin, glycoprotein IIb/IIIa, and beta-thromboglobulin release. Transfusion. 1993 Jan;33(1):25–29. doi: 10.1046/j.1537-2995.1993.33193142305.x. [DOI] [PubMed] [Google Scholar]
  56. 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]
  57. Rosales C., Juliano R. L. Signal transduction by cell adhesion receptors in leukocytes. J Leukoc Biol. 1995 Feb;57(2):189–198. doi: 10.1002/jlb.57.2.189. [DOI] [PubMed] [Google Scholar]
  58. Rothberger H., Zimmerman T. S., Spiegelberg H. L., Vaughan J. H. Leukocyte procoagulant activity: enhancement of production in vitro by IgG and antigen-antibody complexes. J Clin Invest. 1977 Mar;59(3):549–557. doi: 10.1172/JCI108670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Ruf A., Patscheke H. Platelet-induced neutrophil activation: platelet-expressed fibrinogen induces the oxidative burst in neutrophils by an interaction with CD11C/CD18. Br J Haematol. 1995 Aug;90(4):791–796. doi: 10.1111/j.1365-2141.1995.tb05197.x. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. Schall T. J., Bacon K., Toy K. J., Goeddel D. V. Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature. 1990 Oct 18;347(6294):669–671. doi: 10.1038/347669a0. [DOI] [PubMed] [Google Scholar]
  62. Schall T. J., Jongstra J., Dyer B. J., Jorgensen J., Clayberger C., Davis M. M., Krensky A. M. A human T cell-specific molecule is a member of a new gene family. J Immunol. 1988 Aug 1;141(3):1018–1025. [PubMed] [Google Scholar]
  63. Siebenlist U., Franzoso G., Brown K. Structure, regulation and function of NF-kappa B. Annu Rev Cell Biol. 1994;10:405–455. doi: 10.1146/annurev.cb.10.110194.002201. [DOI] [PubMed] [Google Scholar]
  64. Stein B., Baldwin A. S., Jr Distinct mechanisms for regulation of the interleukin-8 gene involve synergism and cooperativity between C/EBP and NF-kappa B. Mol Cell Biol. 1993 Nov;13(11):7191–7198. doi: 10.1128/mcb.13.11.7191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Touqui L., Hatmi M., Vargaftig B. B. Human platelets stimulated by thrombin produce platelet-activating factor (1-O-alkyl-2-acetyl-sn-glycero-3-phosphocholine) when the degrading enzyme acetyl hydrolase is blocked. Biochem J. 1985 Aug 1;229(3):811–816. doi: 10.1042/bj2290811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Ueda A., Okuda K., Ohno S., Shirai A., Igarashi T., Matsunaga K., Fukushima J., Kawamoto S., Ishigatsubo Y., Okubo T. NF-kappa B and Sp1 regulate transcription of the human monocyte chemoattractant protein-1 gene. J Immunol. 1994 Sep 1;153(5):2052–2063. [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. Varki A. Selectin ligands. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7390–7397. doi: 10.1073/pnas.91.16.7390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Wang J. M., McVicar D. W., Oppenheim J. J., Kelvin D. J. Identification of RANTES receptors on human monocytic cells: competition for binding and desensitization by homologous chemotactic cytokines. J Exp Med. 1993 Mar 1;177(3):699–705. doi: 10.1084/jem.177.3.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Wester J., Sixma J. J., Geuze J. J., Heijnen H. F. Morphology of the hemostatic plug in human skin wounds: transformation of the plug. Lab Invest. 1979 Aug;41(2):182–192. [PubMed] [Google Scholar]
  71. Weyrich A. S., McIntyre T. M., McEver R. P., Prescott S. M., Zimmerman G. A. Monocyte tethering by P-selectin regulates monocyte chemotactic protein-1 and tumor necrosis factor-alpha secretion. Signal integration and NF-kappa B translocation. J Clin Invest. 1995 May;95(5):2297–2303. doi: 10.1172/JCI117921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Wiedermann C. J., Kowald E., Reinisch N., Kaehler C. M., von Luettichau I., Pattison J. M., Huie P., Sibley R. K., Nelson P. J., Krensky A. M. Monocyte haptotaxis induced by the RANTES chemokine. Curr Biol. 1993 Nov 1;3(11):735–739. doi: 10.1016/0960-9822(93)90020-o. [DOI] [PubMed] [Google Scholar]
  73. Yeo E. L., Sheppard J. A., Feuerstein I. A. Role of P-selectin and leukocyte activation in polymorphonuclear cell adhesion to surface adherent activated platelets under physiologic shear conditions (an injury vessel wall model). Blood. 1994 May 1;83(9):2498–2507. [PubMed] [Google Scholar]
  74. 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]
  75. 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]

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