Skip to main content
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1988 May;81(5):1415–1418. doi: 10.1172/JCI113471

Interleukin 1 stimulates T lymphocytes to produce granulocyte-monocyte colony-stimulating factor.

F Herrmann 1, W Oster 1, S C Meuer 1, A Lindemann 1, R H Mertelsmann 1
PMCID: PMC442572  PMID: 2452833

Abstract

T lymphocytes are thought to cooperatively interact with monocytes to produce colony-stimulating factors (CSF). However, little is known about monocyte-mediated signals leading to CSF-secretion by T lymphocytes, although soluble monocyte products have been implicated. We have employed monoclonal antibody anti-T3B covalently coupled to CnBr-activated Sepharose 4B beads, to show that multimeric ligation of T cell antigen receptor leads to T cell receptiveness to interleukin 1 (IL-1), as indicated by T cell production of CSF, which induces growth of myeloid progenitor cells into neutrophil, eosinophil, and monocyte colonies. To investigate the molecular basis of these findings, total RNA was extracted from T3B Sepharose-primed and IL-1-stimulated T lymphocytes and probed for granulocyte-monocyte-CSF (GM-CSF), granulocyte-CSF (G-CSF), and monocyte-CSF (M-CSF) mRNA. GM-CSF, but not G-CSF or M-CSF, messages were detected. Nuclear "run on" assays revealed that IL-1 action is effective primarily at the level of GM-CSF gene transcription. These results suggest a previously unrecognized role of IL-1 in the regulation of GM-CSF secretion by T cells.

Full text

PDF
1415

Images in this article

Selected References

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

  1. Bagby G. C., Jr, McCall E., Bergstrom K. A., Burger D. A monokine regulates colony-stimulating activity production by vascular endothelial cells. Blood. 1983 Sep;62(3):663–668. [PubMed] [Google Scholar]
  2. Bagby G. C., Jr, McCall E., Layman D. L. Regulation of colony-stimulating activity production. Interactions of fibroblasts, mononuclear phagocytes, and lactoferrin. J Clin Invest. 1983 Feb;71(2):340–344. doi: 10.1172/JCI110774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bagby G. C., Jr, Rigas V. D., Bennett R. M., Vandenbark A. A., Garewal H. S. Interaction of lactoferrin, monocytes, and T lymphocyte subsets in the regulation of steady-state granulopoiesis in vitro. J Clin Invest. 1981 Jul;68(1):56–63. doi: 10.1172/JCI110254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Broudy V. C., Kaushansky K., Segal G. M., Harlan J. M., Adamson J. W. Tumor necrosis factor type alpha stimulates human endothelial cells to produce granulocyte/macrophage colony-stimulating factor. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7467–7471. doi: 10.1073/pnas.83.19.7467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cantrell M. A., Anderson D., Cerretti D. P., Price V., McKereghan K., Tushinski R. J., Mochizuki D. Y., Larsen A., Grabstein K., Gillis S. Cloning, sequence, and expression of a human granulocyte/macrophage colony-stimulating factor. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6250–6254. doi: 10.1073/pnas.82.18.6250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dessein A. J., Vadas M. A., Nicola N. A., Metcalf D., David J. R. Enhancement of human blood eosinophil cytotoxicity by semi-purified eosinophil colony-stimulating factor(s). J Exp Med. 1982 Jul 1;156(1):90–103. doi: 10.1084/jem.156.1.90. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  8. Handman E., Burgess A. W. Stimulation by granulocyte-macrophage colony-stimulating factor of Leishmania tropica killing by macrophages. J Immunol. 1979 Mar;122(3):1134–1137. [PubMed] [Google Scholar]
  9. Harvey A. R., Kaiser J., Clarke B. J. Monocytes direct T lymphocyte stimulation of human peripheral blood granulocyte-macrophage colony formation. Br J Haematol. 1984 Sep;58(1):129–136. doi: 10.1111/j.1365-2141.1984.tb06067.x. [DOI] [PubMed] [Google Scholar]
  10. Herrmann F., Cannistra S. A., Griffin J. D. T cell-monocyte interactions in the production of humoral factors regulating human granulopoiesis in vitro. J Immunol. 1986 Apr 15;136(8):2856–2861. [PubMed] [Google Scholar]
  11. Kawasaki E. S., Ladner M. B., Wang A. M., Van Arsdell J., Warren M. K., Coyne M. Y., Schweickart V. L., Lee M. T., Wilson K. J., Boosman A. Molecular cloning of a complementary DNA encoding human macrophage-specific colony-stimulating factor (CSF-1). Science. 1985 Oct 18;230(4723):291–296. doi: 10.1126/science.2996129. [DOI] [PubMed] [Google Scholar]
  12. McKnight G. S., Palmiter R. D. Transcriptional regulation of the ovalbumin and conalbumin genes by steroid hormones in chick oviduct. J Biol Chem. 1979 Sep 25;254(18):9050–9058. [PubMed] [Google Scholar]
  13. Meuer S. C., Hussey R. E., Cantrell D. A., Hodgdon J. C., Schlossman S. F., Smith K. A., Reinherz E. L. Triggering of the T3-Ti antigen-receptor complex results in clonal T-cell proliferation through an interleukin 2-dependent autocrine pathway. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1509–1513. doi: 10.1073/pnas.81.5.1509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Meuer S. C., Meyer zum Büschenfelde K. H. T cell receptor triggering induces responsiveness to interleukin 1 and interleukin 2 but does not lead to T cell proliferation. J Immunol. 1986 Jun 1;136(11):4106–4112. [PubMed] [Google Scholar]
  15. Munker R., Gasson J., Ogawa M., Koeffler H. P. Recombinant human TNF induces production of granulocyte-monocyte colony-stimulating factor. Nature. 1986 Sep 4;323(6083):79–82. doi: 10.1038/323079a0. [DOI] [PubMed] [Google Scholar]
  16. Piacibello W., Lu L., Wachter M., Rubin B., Broxmeyer H. E. Release of granulocyte-macrophage colony stimulating factors from major histocompatibility complex class II antigen-positive monocytes is enhanced by human gamma interferon. Blood. 1985 Dec;66(6):1343–1351. [PubMed] [Google Scholar]
  17. Rambaldi A., Young D. C., Griffin J. D. Expression of the M-CSF (CSF-1) gene by human monocytes. Blood. 1987 May;69(5):1409–1413. [PubMed] [Google Scholar]
  18. Sieff C. A., Niemeyer C. M., Nathan D. G., Ekern S. C., Bieber F. R., Yang Y. C., Wong G., Clark S. C. Stimulation of human hematopoietic colony formation by recombinant gibbon multi-colony-stimulating factor or interleukin 3. J Clin Invest. 1987 Sep;80(3):818–823. doi: 10.1172/JCI113139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sieff C. A., Tsai S., Faller D. V. Interleukin 1 induces cultured human endothelial cell production of granulocyte-macrophage colony-stimulating factor. J Clin Invest. 1987 Jan;79(1):48–51. doi: 10.1172/JCI112806. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Silberstein D. S., Owen W. F., Gasson J. C., DiPersio J. F., Golde D. W., Bina J. C., Soberman R., Austen K. F., David J. R. Enhancement of human eosinophil cytotoxicity and leukotriene synthesis by biosynthetic (recombinant) granulocyte-macrophage colony-stimulating factor. J Immunol. 1986 Nov 15;137(10):3290–3294. [PubMed] [Google Scholar]
  21. Souza L. M., Boone T. C., Gabrilove J., Lai P. H., Zsebo K. M., Murdock D. C., Chazin V. R., Bruszewski J., Lu H., Chen K. K. Recombinant human granulocyte colony-stimulating factor: effects on normal and leukemic myeloid cells. Science. 1986 Apr 4;232(4746):61–65. doi: 10.1126/science.2420009. [DOI] [PubMed] [Google Scholar]
  22. Unanue E. R. Cooperation between mononuclear phagocytes and lymphocytes in immunity. N Engl J Med. 1980 Oct 23;303(17):977–985. doi: 10.1056/NEJM198010233031706. [DOI] [PubMed] [Google Scholar]
  23. Villalta F., Kierszenbaum F. Effects of human colony-stimulating factor on the uptake and destruction of a pathogenic parasite (Trypanosoma cruzi) by human neutrophils. J Immunol. 1986 Sep 1;137(5):1703–1707. [PubMed] [Google Scholar]
  24. Weisbart R. H., Golde D. W., Clark S. C., Wong G. G., Gasson J. C. Human granulocyte-macrophage colony-stimulating factor is a neutrophil activator. 1985 Mar 28-Apr 3Nature. 314(6009):361–363. doi: 10.1038/314361a0. [DOI] [PubMed] [Google Scholar]
  25. Weisbart R. H., Golde D. W., Gasson J. C. Biosynthetic human GM-CSF modulates the number and affinity of neutrophil f-Met-Leu-Phe receptors. J Immunol. 1986 Dec 1;137(11):3584–3587. [PubMed] [Google Scholar]

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

RESOURCES