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. 1998 Jun;94(2):221–227. doi: 10.1046/j.1365-2567.1998.00473.x

The effects of monocytes on the transendothelial migration of T lymphocytes.

E A Lidington 1, A M McCormack 1, M H Yacoub 1, M L Rose 1
PMCID: PMC1364208  PMID: 9741344

Abstract

In vivo cell-mediated immune reactions are characterized by mixtures of monocytes and T cells. The purpose of this study was to investigate the role of monocytes on T-cell migration and induction of endothelial adhesion molecules. The in vitro model consisted of adding peripheral blood mononuclear cells (PBMC), T cells or mixtures of monocytes and T cells, to endothelial cells on a porous membrane and using flow cytometry to distinguish between the monocyte and lymphocyte components. PBMC and PBMC supernatants were highly potent at upregulating intercellular adhesion molecule-1 (ICAM-1) and inducing expression of vascular cell adhesion molecule-1 (VCAM-1) and E-selectin. Induction by supernatants was inhibited by antibodies to tumour necrosis factor-alpha (TNF-alpha) and interleukin-1 (IL)-1 beta. Using monocyte-enriched populations, as few as one monocyte to 100 endothelial cells was sufficient to upregulate adhesion molecules. Fixed monocytes also induced adhesion molecules and expressed surface-bound cytokines. In contrast, highly purified unstimulated T cells were not found to induce adhesion molecules at 4, 6, 24 or 48 hr of coculture. Purified T cells showed low-level migration through resting (VCAM-1 negative) endothelium, which was approximately doubled by addition of small numbers of monocytes or TNF-alpha. In conclusion, monocytes, via cell surface or released cytokines play an essential role in allowing large-scale recruitment of T cells to inflammatory sites in vivo.

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Selected References

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  1. Bevilacqua M. P., Pober J. S., Wheeler M. E., Cotran R. S., Gimbrone M. A., Jr Interleukin 1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes, and related leukocyte cell lines. J Clin Invest. 1985 Nov;76(5):2003–2011. doi: 10.1172/JCI112200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blue M. L., Conrad P., Webb D. L., Sarr T., Macaro M. Interacting monocytes and synoviocytes induce adhesion molecules by a cytokine-regulated process. Lymphokine Cytokine Res. 1993 Aug;12(4):213–218. [PubMed] [Google Scholar]
  3. Briscoe D. M., Cotran R. S., Pober J. S. Effects of tumor necrosis factor, lipopolysaccharide, and IL-4 on the expression of vascular cell adhesion molecule-1 in vivo. Correlation with CD3+ T cell infiltration. J Immunol. 1992 Nov 1;149(9):2954–2960. [PubMed] [Google Scholar]
  4. Campanero M. R., Sánchez-Mateos P., del Pozo M. A., Sánchez-Madrid F. ICAM-3 regulates lymphocyte morphology and integrin-mediated T cell interaction with endothelial cell and extracellular matrix ligands. J Cell Biol. 1994 Nov;127(3):867–878. doi: 10.1083/jcb.127.3.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cuturi M. C., Murphy M., Costa-Giomi M. P., Weinmann R., Perussia B., Trinchieri G. Independent regulation of tumor necrosis factor and lymphotoxin production by human peripheral blood lymphocytes. J Exp Med. 1987 Jun 1;165(6):1581–1594. doi: 10.1084/jem.165.6.1581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Damle N. K., Eberhardt C., Van der Vieren M. Direct interaction with primed CD4+ CD45R0+ memory T lymphocytes induces expression of endothelial leukocyte adhesion molecule-1 and vascular cell adhesion molecule-1 on the surface of vascular endothelial cells. Eur J Immunol. 1991 Dec;21(12):2915–2923. doi: 10.1002/eji.1830211204. [DOI] [PubMed] [Google Scholar]
  7. Doukas J., Pober J. S. Lymphocyte-mediated activation of cultured endothelial cells (EC). CD4+ T cells inhibit EC class II MHC expression despite secreting IFN-gamma and increasing EC class I MHC and intercellular adhesion molecule-1 expression. J Immunol. 1990 Aug 15;145(4):1088–1098. [PubMed] [Google Scholar]
  8. Fan J., Shimokama T., Haraoka S., Tokunaga O., Watanabe T. Monocyte-endothelial cell interactions in vitro, with reference to the influence of interleukin-1 and tumor necrosis factor. Biol Cell. 1993;79(1):17–26. doi: 10.1016/0248-4900(93)90258-g. [DOI] [PubMed] [Google Scholar]
  9. Fischer H., Dohlsten M., Andersson U., Hedlund G., Ericsson P., Hansson J., Sjögren H. O. Production of TNF-alpha and TNF-beta by staphylococcal enterotoxin A activated human T cells. J Immunol. 1990 Jun 15;144(12):4663–4669. [PubMed] [Google Scholar]
  10. Ikuta S., Kirby J. A., Shenton B. K., Givan A. L., Lennard T. W. Human endothelial cells: effect of TNF-alpha on peripheral blood mononuclear cell adhesion. Immunology. 1991 May;73(1):71–76. [PMC free article] [PubMed] [Google Scholar]
  11. Kriegler M., Perez C., DeFay K., Albert I., Lu S. D. A novel form of TNF/cachectin is a cell surface cytotoxic transmembrane protein: ramifications for the complex physiology of TNF. Cell. 1988 Apr 8;53(1):45–53. doi: 10.1016/0092-8674(88)90486-2. [DOI] [PubMed] [Google Scholar]
  12. Lidington E., Nohammer C., Dominguez M., Ferry B., Rose M. L. Inhibition of the transendothelial migration of human lymphocytes but not monocytes by phosphodiesterase inhibitors. Clin Exp Immunol. 1996 Apr;104(1):66–71. doi: 10.1046/j.1365-2249.1996.d01-660.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lorré K., Fransen L., Ceuppens J. L. Interleukin-2 induces tumor necrosis factor-alpha production by activated human T cells via a cyclosporin-sensitive pathway. Eur Cytokine Netw. 1992 May-Jun;3(3):321–330. [PubMed] [Google Scholar]
  14. Lou J., Dayer J. M., Grau G. E., Burger D. Direct cell/cell contact with stimulated T lymphocytes induces the expression of cell adhesion molecules and cytokines by human brain microvascular endothelial cells. Eur J Immunol. 1996 Dec;26(12):3107–3113. doi: 10.1002/eji.1830261242. [DOI] [PubMed] [Google Scholar]
  15. Meerschaert J., Furie M. B. Monocytes use either CD11/CD18 or VLA-4 to migrate across human endothelium in vitro. J Immunol. 1994 Feb 15;152(4):1915–1926. [PubMed] [Google Scholar]
  16. Miller M. D., Krangel M. S. Biology and biochemistry of the chemokines: a family of chemotactic and inflammatory cytokines. Crit Rev Immunol. 1992;12(1-2):17–46. [PubMed] [Google Scholar]
  17. Noble K. E., Panayiotidis P., Collins P. W., Hoffbrand A. V., Yong K. L. Monocytes induce E-selectin gene expression in endothelial cells: role of CD11/CD18 and extracellular matrix proteins. Eur J Immunol. 1996 Dec;26(12):2944–2951. doi: 10.1002/eji.1830261221. [DOI] [PubMed] [Google Scholar]
  18. Pryce G., Santos W., Male D. An assay for the analysis of lymphocyte migration across cerebral endothelium in vitro. J Immunol Methods. 1994 Jan 3;167(1-2):55–63. doi: 10.1016/0022-1759(94)90074-4. [DOI] [PubMed] [Google Scholar]
  19. Pugin J., Ulevitch R. J., Tobias P. S. A critical role for monocytes and CD14 in endotoxin-induced endothelial cell activation. J Exp Med. 1993 Dec 1;178(6):2193–2200. doi: 10.1084/jem.178.6.2193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rainger G. E., Wautier M. P., Nash G. B., Wautier J. L. Prolonged E-selectin induction by monocytes potentiates the adhesion of flowing neutrophils to cultured endothelial cells. Br J Haematol. 1996 Jan;92(1):192–199. doi: 10.1046/j.1365-2141.1996.00308.x. [DOI] [PubMed] [Google Scholar]
  21. Sepp N. T., Gille J., Li L. J., Caughman S. W., Lawley T. J., Swerlick R. A. A factor in human plasma permits persistent expression of E-selectin by human endothelial cells. J Invest Dermatol. 1994 Apr;102(4):445–450. doi: 10.1111/1523-1747.ep12373008. [DOI] [PubMed] [Google Scholar]
  22. Singer I. I., Scott S., Chin J., Bayne E. K., Limjuco G., Weidner J., Miller D. K., Chapman K., Kostura M. J. The interleukin-1 beta-converting enzyme (ICE) is localized on the external cell surface membranes and in the cytoplasmic ground substance of human monocytes by immuno-electron microscopy. J Exp Med. 1995 Nov 1;182(5):1447–1459. doi: 10.1084/jem.182.5.1447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Sunderkötter C., Steinbrink K., Henseleit U., Bosse R., Schwarz A., Vestweber D., Sorg C. Activated T cells induce expression of E-selectin in vitro and in an antigen-dependent manner in vivo. Eur J Immunol. 1996 Jul;26(7):1571–1579. doi: 10.1002/eji.1830260725. [DOI] [PubMed] [Google Scholar]
  25. Turunen J. P., Mattila P., Renkonen R. cAMP mediates IL-1-induced lymphocyte penetration through endothelial monolayers. J Immunol. 1990 Dec 15;145(12):4192–4197. [PubMed] [Google Scholar]
  26. Varki A. P. The times they are still a'changing: keeping up with the times. J Clin Invest. 1996 Jan 1;97(1):1–1. doi: 10.1172/JCI118375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Vilcek J., Lee T. H. Tumor necrosis factor. New insights into the molecular mechanisms of its multiple actions. J Biol Chem. 1991 Apr 25;266(12):7313–7316. [PubMed] [Google Scholar]
  28. Weill D., Wautier J. L., Dosquet C., Wautier M. P., Carreno M. P., Boval B. Monocyte modulation of endothelial leukocyte adhesion molecules. J Lab Clin Med. 1995 Jun;125(6):768–774. [PubMed] [Google Scholar]
  29. Zocchi M. R., Ferrero E., Leone B. E., Rovere P., Bianchi E., Toninelli E., Pardi R. CD31/PECAM-1-driven chemokine-independent transmigration of human T lymphocytes. Eur J Immunol. 1996 Apr;26(4):759–767. doi: 10.1002/eji.1830260406. [DOI] [PubMed] [Google Scholar]
  30. von Fliedner V., Miescher S., Gérain J., Gallati H., Barras C., Heumann D., Cerottini J. C. Production of tumor necrosis factor-alpha by naive or memory T lymphocytes activated via CD28. Cell Immunol. 1992 Jan;139(1):198–207. doi: 10.1016/0008-8749(92)90112-3. [DOI] [PubMed] [Google Scholar]

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