Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1995 Jun 1;181(6):2181–2186. doi: 10.1084/jem.181.6.2181

Chemoattractants induce rapid release of the interleukin 1 type II decoy receptor in human polymorphonuclear cells

PMCID: PMC2192047  PMID: 7760005

Abstract

Molecules representative of different classes of chemotactic agents, including formyl-Met-Leu-Phe (FMLP), C5a, leukotriene B4, platelet- activating factor, and interleukin (IL)-8, caused a rapid reduction in the IL-1 binding capacity by human polymorphonuclear leukocytes (PMN), a cell type expressing predominantly the IL-1 type II decoy receptor (IL-1 decoy RII). N-t-Boc-Met-Leu-Phe, an antagonist for the FMLP receptor, inhibited the loss of IL-1 binding capacity induced by FMLP. Monocyte chemotactic protein 1, a chemokine related to IL-8 but inactive on PMN, had no effect on IL-1 binding in this cell type. FMLP was selected for further detailed analysis of chemoattractant-induced loss of IL-1 binding by PMN. The action of FMLP was rapid, reaching 50% of its maximum (80%) at 30 s, the earliest measurable time point, and plateauing between 10 and 30 min. Dose-response analysis revealed that maximal reduction of IL-1 binding was reached at FMLP concentrations that were also optimal for chemotaxis (50% effective dose = 5 x 10(-9) M). The loss of IL-1 binding capacity caused by FMLP was determined by a reduction in receptor number with no change in their affinity. The effect of FMLP on IL-1 receptor (IL-1R) was selective in that the PMN surface structures IL-8R, CD16, CD18, and major histocompatibility complex class I antigens were unaffected under these conditions. Loss of surface IL-1R was not due to an augumented rate of internalization. FMLP caused rapid release of a 45-kD IL-1-binding molecule identified as the IL-1 decoy RII. After FMLP-induced release, PMN reexpressed newly synthesized receptors, reaching basal levels by 4 h. FMLP-induced release of the IL-1 decoy RII did not impair the responsiveness of PMN to IL-1 in terms of promotion of survival and cytokine production. FMLP- induced release of the IL-1 decoy RII was unaffected by protein synthesis inhibitors, was blocked by certain protease inhibitors, and was mimicked by agents (the Ca++ ionophore A23187 and phorbol myristate acetate) that recapitulate elements in the signal transduction pathway of chemoattractant receptors. The time frame and concentration range of chemoattractant-induced rapid release of the IL-1 decoy RII are consistent with the view that IL-1 decoy RII release is an early event in the multistep process of leukocyte recruitment.(ABSTRACT TRUNCATED AT 400 WORDS)

Full Text

The Full Text of this article is available as a PDF (851.2 KB).

Selected References

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

  1. Bertani A., Polentarutti N., Sica A., Rambaldi A., Mantovani A., Colotta F. Expression of c-jun protooncogene in human myelomonocytic cells. Blood. 1989 Oct;74(5):1811–1816. [PubMed] [Google Scholar]
  2. Colotta F., Dower S. K., Sims J. E., Mantovani A. The type II 'decoy' receptor: a novel regulatory pathway for interleukin 1. Immunol Today. 1994 Dec;15(12):562–566. doi: 10.1016/0167-5699(94)90217-8. [DOI] [PubMed] [Google Scholar]
  3. Colotta F., Re F., Muzio M., Bertini R., Polentarutti N., Sironi M., Giri J. G., Dower S. K., Sims J. E., Mantovani A. Interleukin-1 type II receptor: a decoy target for IL-1 that is regulated by IL-4. Science. 1993 Jul 23;261(5120):472–475. doi: 10.1126/science.8332913. [DOI] [PubMed] [Google Scholar]
  4. Colotta F., Re F., Muzio M., Polentarutti N., Minty A., Caput D., Ferrara P., Mantovani A. Interleukin-13 induces expression and release of interleukin-1 decoy receptor in human polymorphonuclear cells. J Biol Chem. 1994 Apr 29;269(17):12403–12406. [PubMed] [Google Scholar]
  5. Dinarello C. A. Interleukin-1 and interleukin-1 antagonism. Blood. 1991 Apr 15;77(8):1627–1652. [PubMed] [Google Scholar]
  6. Eastgate J. A., Symons J. A., Duff G. W. Identification of an interleukin-1 beta binding protein in human plasma. FEBS Lett. 1990 Jan 29;260(2):213–216. doi: 10.1016/0014-5793(90)80106-s. [DOI] [PubMed] [Google Scholar]
  7. Falk W., Goodwin R. H., Jr, Leonard E. J. A 48-well micro chemotaxis assembly for rapid and accurate measurement of leukocyte migration. J Immunol Methods. 1980;33(3):239–247. doi: 10.1016/0022-1759(80)90211-2. [DOI] [PubMed] [Google Scholar]
  8. Giri J. G., Newton R. C., Horuk R. Identification of soluble interleukin-1 binding protein in cell-free supernatants. Evidence for soluble interleukin-1 receptor. J Biol Chem. 1990 Oct 15;265(29):17416–17419. [PubMed] [Google Scholar]
  9. Hechtman D. H., Cybulsky M. I., Fuchs H. J., Baker J. B., Gimbrone M. A., Jr Intravascular IL-8. Inhibitor of polymorphonuclear leukocyte accumulation at sites of acute inflammation. J Immunol. 1991 Aug 1;147(3):883–892. [PubMed] [Google Scholar]
  10. Luscinskas F. W., Kiely J. M., Ding H., Obin M. S., Hébert C. A., Baker J. B., Gimbrone M. A., Jr In vitro inhibitory effect of IL-8 and other chemoattractants on neutrophil-endothelial adhesive interactions. J Immunol. 1992 Sep 15;149(6):2163–2171. [PubMed] [Google Scholar]
  11. McMahan C. J., Slack J. L., Mosley B., Cosman D., Lupton S. D., Brunton L. L., Grubin C. E., Wignall J. M., Jenkins N. A., Brannan C. I. A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO J. 1991 Oct;10(10):2821–2832. doi: 10.1002/j.1460-2075.1991.tb07831.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Porteu F., Hieblot C. Tumor necrosis factor induces a selective shedding of its p75 receptor from human neutrophils. J Biol Chem. 1994 Jan 28;269(4):2834–2840. [PubMed] [Google Scholar]
  13. Porteu F., Nathan C. Shedding of tumor necrosis factor receptors by activated human neutrophils. J Exp Med. 1990 Aug 1;172(2):599–607. doi: 10.1084/jem.172.2.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Re F., Muzio M., De Rossi M., Polentarutti N., Giri J. G., Mantovani A., Colotta F. The type II "receptor" as a decoy target for interleukin 1 in polymorphonuclear leukocytes: characterization of induction by dexamethasone and ligand binding properties of the released decoy receptor. J Exp Med. 1994 Feb 1;179(2):739–743. doi: 10.1084/jem.179.2.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Sims J. E., Gayle M. A., Slack J. L., Alderson M. R., Bird T. A., Giri J. G., Colotta F., Re F., Mantovani A., Shanebeck K. Interleukin 1 signaling occurs exclusively via the type I receptor. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6155–6159. doi: 10.1073/pnas.90.13.6155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sironi M., Breviario F., Proserpio P., Biondi A., Vecchi A., Van Damme J., Dejana E., Mantovani A. IL-1 stimulates IL-6 production in endothelial cells. J Immunol. 1989 Jan 15;142(2):549–553. [PubMed] [Google Scholar]
  17. Sozzani S., Luini W., Molino M., Jílek P., Bottazzi B., Cerletti C., Matsushima K., Mantovani A. The signal transduction pathway involved in the migration induced by a monocyte chemotactic cytokine. J Immunol. 1991 Oct 1;147(7):2215–2221. [PubMed] [Google Scholar]
  18. Spriggs M. K., Lioubin P. J., Slack J., Dower S. K., Jonas U., Cosman D., Sims J. E., Bauer J. Induction of an interleukin-1 receptor (IL-1R) on monocytic cells. Evidence that the receptor is not encoded by a T cell-type IL-1R mRNA. J Biol Chem. 1990 Dec 25;265(36):22499–22505. [PubMed] [Google Scholar]
  19. Symons J. A., Duff G. W. A soluble form of the interleukin-1 receptor produced by a human B cell line. FEBS Lett. 1990 Oct 15;272(1-2):133–136. doi: 10.1016/0014-5793(90)80466-v. [DOI] [PubMed] [Google Scholar]
  20. Symons J. A., Eastgate J. A., Duff G. W. A soluble binding protein specific for interleukin 1 beta is produced by activated mononuclear cells. Cytokine. 1990 May;2(3):190–198. doi: 10.1016/1043-4666(90)90015-l. [DOI] [PubMed] [Google Scholar]
  21. Symons J. A., Eastgate J. A., Duff G. W. Purification and characterization of a novel soluble receptor for interleukin 1. J Exp Med. 1991 Nov 1;174(5):1251–1254. doi: 10.1084/jem.174.5.1251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Webster R. O., Larsen G. L., Mitchell B. C., Goins A. J., Henson P. M. Absence of inflammatory lung injury in rabbits challenged intravascularly with complement-derived chemotactic factors. Am Rev Respir Dis. 1982 Mar;125(3):335–340. doi: 10.1164/arrd.1982.125.3.335. [DOI] [PubMed] [Google Scholar]

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

RESOURCES