Skip to main content
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1994 Aug 1;180(2):711–715. doi: 10.1084/jem.180.2.711

Interleukin 10 inhibits lipopolysaccharide-induced survival and cytokine production by human peripheral blood eosinophils

PMCID: PMC2191606  PMID: 8046346

Abstract

In this study we have investigated the effects of interleukin 10 (IL- 10) on human peripheral blood eosinophils stimulated with granulocyte/macrophage colony stimulating factor (GM-CSF) and lipopolysaccharide (LPS). We show that LPS was able to enhance eosinophil survival in a dose-dependent manner, as well as release of the cytokines GM-CSF, tumor necrosis factor alpha, and IL-8. LPS- induced eosinophil survival was largely inhibited by an anti-GM-CSF neutralizing antibody and completely blocked by polymyxin B, suggesting GM-CSF involvement in the survival enhancing mechanism and LPS specificity, respectively. IL-10 significantly inhibited survival of, and cytokine production from, eosinophils induced by LPS, but did not inhibit the survival induced by GM-CSF. These observations suggest a novel activation mechanism of eosinophils and, also, that IL-10 may participate in the regulation of diseases characterized by eosinophil infiltration.

Full Text

The Full Text of this article is available as a PDF (564.9 KB).

Selected References

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

  1. Begley C. G., Lopez A. F., Nicola N. A., Warren D. J., Vadas M. A., Sanderson C. J., Metcalf D. Purified colony-stimulating factors enhance the survival of human neutrophils and eosinophils in vitro: a rapid and sensitive microassay for colony-stimulating factors. Blood. 1986 Jul;68(1):162–166. [PubMed] [Google Scholar]
  2. Braun R. K., Franchini M., Erard F., Rihs S., De Vries I. J., Blaser K., Hansel T. T., Walker C. Human peripheral blood eosinophils produce and release interleukin-8 on stimulation with calcium ionophore. Eur J Immunol. 1993 Apr;23(4):956–960. doi: 10.1002/eji.1830230429. [DOI] [PubMed] [Google Scholar]
  3. Broide D. H., Paine M. M., Firestein G. S. Eosinophils express interleukin 5 and granulocyte macrophage-colony-stimulating factor mRNA at sites of allergic inflammation in asthmatics. J Clin Invest. 1992 Oct;90(4):1414–1424. doi: 10.1172/JCI116008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cassatella M. A., Meda L., Bonora S., Ceska M., Constantin G. Interleukin 10 (IL-10) inhibits the release of proinflammatory cytokines from human polymorphonuclear leukocytes. Evidence for an autocrine role of tumor necrosis factor and IL-1 beta in mediating the production of IL-8 triggered by lipopolysaccharide. J Exp Med. 1993 Dec 1;178(6):2207–2211. doi: 10.1084/jem.178.6.2207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cavaillon J. M., Haeffner-Cavaillon N. Signals involved in interleukin 1 synthesis and release by lipopolysaccharide-stimulated monocytes/macrophages. Cytokine. 1990 Sep;2(5):313–329. doi: 10.1016/1043-4666(90)90061-w. [DOI] [PubMed] [Google Scholar]
  6. Costa J. J., Matossian K., Resnick M. B., Beil W. J., Wong D. T., Gordon J. R., Dvorak A. M., Weller P. F., Galli S. J. Human eosinophils can express the cytokines tumor necrosis factor-alpha and macrophage inflammatory protein-1 alpha. J Clin Invest. 1993 Jun;91(6):2673–2684. doi: 10.1172/JCI116506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cox G., Ohtoshi T., Vancheri C., Denburg J. A., Dolovich J., Gauldie J., Jordana M. Promotion of eosinophil survival by human bronchial epithelial cells and its modulation by steroids. Am J Respir Cell Mol Biol. 1991 Jun;4(6):525–531. doi: 10.1165/ajrcmb/4.6.525. [DOI] [PubMed] [Google Scholar]
  8. Del Pozo V., De Andres B., Martin E., Maruri N., Zubeldia J. M., Palomino P., Lahoz C. Murine eosinophils and IL-1: alpha IL-1 mRNA detection by in situ hybridization. Production and release of IL-1 from peritoneal eosinophils. J Immunol. 1990 Apr 15;144(8):3117–3122. [PubMed] [Google Scholar]
  9. Frigas E., Loegering D. A., Gleich G. J. Cytotoxic effects of the guinea pig eosinophil major basic protein on tracheal epithelium. Lab Invest. 1980 Jan;42(1):35–43. [PubMed] [Google Scholar]
  10. Hamid Q., Barkans J., Meng Q., Ying S., Abrams J. S., Kay A. B., Moqbel R. Human eosinophils synthesize and secrete interleukin-6, in vitro. Blood. 1992 Sep 15;80(6):1496–1501. [PubMed] [Google Scholar]
  11. Hansel T. T., De Vries I. J., Iff T., Rihs S., Wandzilak M., Betz S., Blaser K., Walker C. An improved immunomagnetic procedure for the isolation of highly purified human blood eosinophils. J Immunol Methods. 1991 Dec 15;145(1-2):105–110. doi: 10.1016/0022-1759(91)90315-7. [DOI] [PubMed] [Google Scholar]
  12. Kita H., Ohnishi T., Okubo Y., Weiler D., Abrams J. S., Gleich G. J. Granulocyte/macrophage colony-stimulating factor and interleukin 3 release from human peripheral blood eosinophils and neutrophils. J Exp Med. 1991 Sep 1;174(3):745–748. doi: 10.1084/jem.174.3.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lamas A. M., Leon O. G., Schleimer R. P. Glucocorticoids inhibit eosinophil responses to granulocyte-macrophage colony-stimulating factor. J Immunol. 1991 Jul 1;147(1):254–259. [PubMed] [Google Scholar]
  14. Moqbel R., Hamid Q., Ying S., Barkans J., Hartnell A., Tsicopoulos A., Wardlaw A. J., Kay A. B. Expression of mRNA and immunoreactivity for the granulocyte/macrophage colony-stimulating factor in activated human eosinophils. J Exp Med. 1991 Sep 1;174(3):749–752. doi: 10.1084/jem.174.3.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ohno I., Lea R. G., Flanders K. C., Clark D. A., Banwatt D., Dolovich J., Denburg J., Harley C. B., Gauldie J., Jordana M. Eosinophils in chronically inflamed human upper airway tissues express transforming growth factor beta 1 gene (TGF beta 1). J Clin Invest. 1992 May;89(5):1662–1668. doi: 10.1172/JCI115764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ohno I., Lea R., Finotto S., Marshall J., Denburg J., Dolovich J., Gauldie J., Jordana M. Granulocyte/macrophage colony-stimulating factor (GM-CSF) gene expression by eosinophils in nasal polyposis. Am J Respir Cell Mol Biol. 1991 Dec;5(6):505–510. doi: 10.1165/ajrcmb/5.6.505. [DOI] [PubMed] [Google Scholar]
  17. Owen W. F., Jr, Soberman R. J., Yoshimoto T., Sheffer A. L., Lewis R. A., Austen K. F. Synthesis and release of leukotriene C4 by human eosinophils. J Immunol. 1987 Jan 15;138(2):532–538. [PubMed] [Google Scholar]
  18. Ralph P., Nakoinz I., Sampson-Johannes A., Fong S., Lowe D., Min H. Y., Lin L. IL-10, T lymphocyte inhibitor of human blood cell production of IL-1 and tumor necrosis factor. J Immunol. 1992 Feb 1;148(3):808–814. [PubMed] [Google Scholar]
  19. Resnick M. B., Weller P. F. Mechanisms of eosinophil recruitment. Am J Respir Cell Mol Biol. 1993 Apr;8(4):349–355. doi: 10.1165/ajrcmb/8.4.349. [DOI] [PubMed] [Google Scholar]
  20. Vaara M., Vaara T., Jensen M., Helander I., Nurminen M., Rietschel E. T., Mäkelä P. H. Characterization of the lipopolysaccharide from the polymyxin-resistant pmrA mutants of Salmonella typhimurium. FEBS Lett. 1981 Jun 29;129(1):145–149. doi: 10.1016/0014-5793(81)80777-6. [DOI] [PubMed] [Google Scholar]
  21. Vancheri C., Gauldie J., Bienenstock J., Cox G., Scicchitano R., Stanisz A., Jordana M. Human lung fibroblast-derived granulocyte-macrophage colony stimulating factor (GM-CSF) mediates eosinophil survival in vitro. Am J Respir Cell Mol Biol. 1989 Oct;1(4):289–295. doi: 10.1165/ajrcmb/1.4.289. [DOI] [PubMed] [Google Scholar]
  22. Wong D. T., Weller P. F., Galli S. J., Elovic A., Rand T. H., Gallagher G. T., Chiang T., Chou M. Y., Matossian K., McBride J. Human eosinophils express transforming growth factor alpha. J Exp Med. 1990 Sep 1;172(3):673–681. doi: 10.1084/jem.172.3.673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wright S. D., Levin S. M., Jong M. T., Chad Z., Kabbash L. G. CR3 (CD11b/CD18) expresses one binding site for Arg-Gly-Asp-containing peptides and a second site for bacterial lipopolysaccharide. J Exp Med. 1989 Jan 1;169(1):175–183. doi: 10.1084/jem.169.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wright S. D., Ramos R. A., Tobias P. S., Ulevitch R. J., Mathison J. C. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science. 1990 Sep 21;249(4975):1431–1433. doi: 10.1126/science.1698311. [DOI] [PubMed] [Google Scholar]
  25. Xing Z., Jordana M., Braciak T., Ohtoshi T., Gauldie J. Lipopolysaccharide induces expression of granulocyte/macrophage colony-stimulating factor, interleukin-8, and interleukin-6 in human nasal, but not lung, fibroblasts: evidence for heterogeneity within the respiratory tract. Am J Respir Cell Mol Biol. 1993 Sep;9(3):255–263. doi: 10.1165/ajrcmb/9.3.255. [DOI] [PubMed] [Google Scholar]
  26. Xing Z., Kirpalani H., Torry D., Jordana M., Gauldie J. Polymorphonuclear leukocytes as a significant source of tumor necrosis factor-alpha in endotoxin-challenged lung tissue. Am J Pathol. 1993 Oct;143(4):1009–1015. [PMC free article] [PubMed] [Google Scholar]
  27. de Waal Malefyt R., Abrams J., Bennett B., Figdor C. G., de Vries J. E. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med. 1991 Nov 1;174(5):1209–1220. doi: 10.1084/jem.174.5.1209. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES