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. 1997 Jun;150(6):2113–2123.

Expression of functional VCAM-1 by cultured nasal polyp-derived microvascular endothelium.

F L Jahnsen 1, P Brandtzaeg 1, R Haye 1, G Haraldsen 1
PMCID: PMC1858320  PMID: 9176402

Abstract

Induction of endothelial vascular cell adhesion molecule-1 (VCAM-1) by interleukin (IL)-4 is believed to exert a major impact on the extravasation of leukocyte subsets in allergic disease. This notion has recently been challenged because cultured microvascular endothelial cells (ECs) derived from various organs are unable to express VCAM-1 after exposure to IL-4. In this study, we have established a method for isolation and culture of nasal polyp-derived microvascular ECs and report their cytokine-regulated VCAM-1 expression. With a combination of cell enzyme-linked immunosorbent assay, flow cytometry, and reverse transcription polymerase chain reaction, such expression was shown to be induced in a dose- and time-dependent manner not only by IL-1 beta and tumor necrosis factor-alpha but also by IL-4 and IL-13. Therefore, the response of nasal microvascular ECs did not harmonize with that of counterparts from several other tissues. IL-4 or IL-13 combined with submaximal concentrations of IL-1 beta or tumor necrosis factor-alpha increased VCAM-1 expression in a synergistic manner. VCAM-1 was functional as shown by antibody-mediated inhibition of leukocyte adhesion. Taken together, our results supported the notion that selective VCAM-1 induction by IL-4 and IL-13 plays an important role for the preferential recruitment of eosinophils and T lymphocytes seen in human airways affected by allergy.

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Selected References

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

  1. 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]
  2. Bochner B. S., Klunk D. A., Sterbinsky S. A., Coffman R. L., Schleimer R. P. IL-13 selectively induces vascular cell adhesion molecule-1 expression in human endothelial cells. J Immunol. 1995 Jan 15;154(2):799–803. [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. Carlos T. M., Schwartz B. R., Kovach N. L., Yee E., Rosa M., Osborn L., Chi-Rosso G., Newman B., Lobb R., Rosso M. Vascular cell adhesion molecule-1 mediates lymphocyte adherence to cytokine-activated cultured human endothelial cells. Blood. 1990 Sep 1;76(5):965–970. [PubMed] [Google Scholar]
  5. Corrigan C. J. Allergy of the respiratory tract. Curr Opin Immunol. 1992 Dec;4(6):798–804. doi: 10.1016/0952-7915(92)90065-m. [DOI] [PubMed] [Google Scholar]
  6. Davison P. M., Karasek M. A. Human dermal microvascular endothelial cells in vitro: effect of cyclic AMP on cellular morphology and proliferation rate. J Cell Physiol. 1981 Feb;106(2):253–258. doi: 10.1002/jcp.1041060211. [DOI] [PubMed] [Google Scholar]
  7. De Clerck L. S., Bridts C. H., Mertens A. M., Moens M. M., Stevens W. J. Use of fluorescent dyes in the determination of adherence of human leucocytes to endothelial cells and the effect of fluorochromes on cellular function. J Immunol Methods. 1994 Jun 3;172(1):115–124. doi: 10.1016/0022-1759(94)90384-0. [DOI] [PubMed] [Google Scholar]
  8. Finotto S., Ohno I., Marshall J. S., Gauldie J., Denburg J. A., Dolovich J., Clark D. A., Jordana M. TNF-alpha production by eosinophils in upper airways inflammation (nasal polyposis). J Immunol. 1994 Sep 1;153(5):2278–2289. [PubMed] [Google Scholar]
  9. Folkman J., Haudenschild C. C., Zetter B. R. Long-term culture of capillary endothelial cells. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5217–5221. doi: 10.1073/pnas.76.10.5217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gerritsen M. E., Niedbala M. J., Szczepanski A., Carley W. W. Cytokine activation of human macro- and microvessel-derived endothelial cells. Blood Cells. 1993;19(2):325–342. [PubMed] [Google Scholar]
  11. Gille J., Swerlick R. A., Lawley T. J., Caughman S. W. Differential regulation of vascular cell adhesion molecule-1 gene transcription by tumor necrosis factor alpha and interleukin-1 alpha in dermal microvascular endothelial cells. Blood. 1996 Jan 1;87(1):211–217. [PubMed] [Google Scholar]
  12. Haraldsen G., Kvale D., Lien B., Farstad I. N., Brandtzaeg P. Cytokine-regulated expression of E-selectin, intercellular adhesion molecule-1 (ICAM-1), and vascular cell adhesion molecule-1 (VCAM-1) in human microvascular endothelial cells. J Immunol. 1996 Apr 1;156(7):2558–2565. [PubMed] [Google Scholar]
  13. Haraldsen G., Rugtveit J., Kvale D., Scholz T., Muller W. A., Hovig T., Brandtzaeg P. Isolation and longterm culture of human intestinal microvascular endothelial cells. Gut. 1995 Aug;37(2):225–234. doi: 10.1136/gut.37.2.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Holthöfer H., Virtanen I., Kariniemi A. L., Hormia M., Linder E., Miettinen A. Ulex europaeus I lectin as a marker for vascular endothelium in human tissues. Lab Invest. 1982 Jul;47(1):60–66. [PubMed] [Google Scholar]
  15. Huang S. K., Xiao H. Q., Kleine-Tebbe J., Paciotti G., Marsh D. G., Lichtenstein L. M., Liu M. C. IL-13 expression at the sites of allergen challenge in patients with asthma. J Immunol. 1995 Sep 1;155(5):2688–2694. [PubMed] [Google Scholar]
  16. Iademarco M. F., Barks J. L., Dean D. C. Regulation of vascular cell adhesion molecule-1 expression by IL-4 and TNF-alpha in cultured endothelial cells. J Clin Invest. 1995 Jan;95(1):264–271. doi: 10.1172/JCI117650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jahnsen F. L., Haraldsen G., Aanesen J. P., Haye R., Brandtzaeg P. Eosinophil infiltration is related to increased expression of vascular cell adhesion molecule-1 in nasal polyps. Am J Respir Cell Mol Biol. 1995 Jun;12(6):624–632. doi: 10.1165/ajrcmb.12.6.7539273. [DOI] [PubMed] [Google Scholar]
  18. Knedler A., Ham R. G. Optimized medium for clonal growth of human microvascular endothelial cells with minimal serum. In Vitro Cell Dev Biol. 1987 Jul;23(7):481–491. doi: 10.1007/BF02628418. [DOI] [PubMed] [Google Scholar]
  19. Kvale D., Krajci P., Brandtzaeg P. Expression and regulation of adhesion molecules ICAM-1 (CD54) and LFA-3 (CD58) in human intestinal epithelial cell lines. Scand J Immunol. 1992 Jun;35(6):669–676. doi: 10.1111/j.1365-3083.1992.tb02973.x. [DOI] [PubMed] [Google Scholar]
  20. Lampugnani M. G., Resnati M., Raiteri M., Pigott R., Pisacane A., Houen G., Ruco L. P., Dejana E. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J Cell Biol. 1992 Sep;118(6):1511–1522. doi: 10.1083/jcb.118.6.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lee B. J., Naclerio R. M., Bochner B. S., Taylor R. M., Lim M. C., Baroody F. M. Nasal challenge with allergen upregulates the local expression of vascular endothelial adhesion molecules. J Allergy Clin Immunol. 1994 Dec;94(6 Pt 1):1006–1016. doi: 10.1016/0091-6749(94)90119-8. [DOI] [PubMed] [Google Scholar]
  22. Masinovsky B., Urdal D., Gallatin W. M. IL-4 acts synergistically with IL-1 beta to promote lymphocyte adhesion to microvascular endothelium by induction of vascular cell adhesion molecule-1. J Immunol. 1990 Nov 1;145(9):2886–2895. [PubMed] [Google Scholar]
  23. Moser R., Fehr J., Bruijnzeel P. L. IL-4 controls the selective endothelium-driven transmigration of eosinophils from allergic individuals. J Immunol. 1992 Aug 15;149(4):1432–1438. [PubMed] [Google Scholar]
  24. Nakajima H., Sano H., Nishimura T., Yoshida S., Iwamoto I. Role of vascular cell adhesion molecule 1/very late activation antigen 4 and intercellular adhesion molecule 1/lymphocyte function-associated antigen 1 interactions in antigen-induced eosinophil and T cell recruitment into the tissue. J Exp Med. 1994 Apr 1;179(4):1145–1154. doi: 10.1084/jem.179.4.1145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nonaka M., Nonaka R., Woolley K., Adelroth E., Miura K., Okhawara Y., Glibetic M., Nakano K., O'Byrne P., Dolovich J. Distinct immunohistochemical localization of IL-4 in human inflamed airway tissues. IL-4 is localized to eosinophils in vivo and is released by peripheral blood eosinophils. J Immunol. 1995 Sep 15;155(6):3234–3244. [PubMed] [Google Scholar]
  26. Parks D. R., Bryan V. M., Oi V. T., Herzenberg L. A. Antigen-specific identification and cloning of hybridomas with a fluorescence-activated cell sorter. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1962–1966. doi: 10.1073/pnas.76.4.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Petzelbauer P., Bender J. R., Wilson J., Pober J. S. Heterogeneity of dermal microvascular endothelial cell antigen expression and cytokine responsiveness in situ and in cell culture. J Immunol. 1993 Nov 1;151(9):5062–5072. [PubMed] [Google Scholar]
  28. Robinson D. S., Hamid Q., Ying S., Tsicopoulos A., Barkans J., Bentley A. M., Corrigan C., Durham S. R., Kay A. B. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med. 1992 Jan 30;326(5):298–304. doi: 10.1056/NEJM199201303260504. [DOI] [PubMed] [Google Scholar]
  29. Schleimer R. P., Sterbinsky S. A., Kaiser J., Bickel C. A., Klunk D. A., Tomioka K., Newman W., Luscinskas F. W., Gimbrone M. A., Jr, McIntyre B. W. IL-4 induces adherence of human eosinophils and basophils but not neutrophils to endothelium. Association with expression of VCAM-1. J Immunol. 1992 Feb 15;148(4):1086–1092. [PubMed] [Google Scholar]
  30. Sironi M., Sciacca F. L., Matteucci C., Conni M., Vecchi A., Bernasconi S., Minty A., Caput D., Ferrara P., Colotta F. Regulation of endothelial and mesothelial cell function by interleukin-13: selective induction of vascular cell adhesion molecule-1 and amplification of interleukin-6 production. Blood. 1994 Sep 15;84(6):1913–1921. [PubMed] [Google Scholar]
  31. Swerlick R. A., Lee K. H., Li L. J., Sepp N. T., Caughman S. W., Lawley T. J. Regulation of vascular cell adhesion molecule 1 on human dermal microvascular endothelial cells. J Immunol. 1992 Jul 15;149(2):698–705. [PubMed] [Google Scholar]
  32. Thornhill M. H., Haskard D. O. IL-4 regulates endothelial cell activation by IL-1, tumor necrosis factor, or IFN-gamma. J Immunol. 1990 Aug 1;145(3):865–872. [PubMed] [Google Scholar]
  33. Thornhill M. H., Wellicome S. M., Mahiouz D. L., Lanchbury J. S., Kyan-Aung U., Haskard D. O. Tumor necrosis factor combines with IL-4 or IFN-gamma to selectively enhance endothelial cell adhesiveness for T cells. The contribution of vascular cell adhesion molecule-1-dependent and -independent binding mechanisms. J Immunol. 1991 Jan 15;146(2):592–598. [PubMed] [Google Scholar]
  34. Wong D., Dorovini-Zis K. Expression of vascular cell adhesion molecule-1 (VCAM-1) by human brain microvessel endothelial cells in primary culture. Microvasc Res. 1995 May;49(3):325–339. doi: 10.1006/mvre.1995.1028. [DOI] [PubMed] [Google Scholar]
  35. Yao L., Pan J., Setiadi H., Patel K. D., McEver R. P. Interleukin 4 or oncostatin M induces a prolonged increase in P-selectin mRNA and protein in human endothelial cells. J Exp Med. 1996 Jul 1;184(1):81–92. doi: 10.1084/jem.184.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]

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