Abstract
Whereas the signaling function of the interleukin 1 (IL-1) receptor type I (IL-1R I) has been well documented, the type II "receptor" has been suggested to act as a decoy target for this cytokine. Since IL-1 may represent a key target of the immunomodulatory and antiinflammatory properties of glucocorticoids (GC), the aim of this study was to investigate the effects of dexamethasone (Dex) on IL-1R expression in human polymorphonuclear leukocytes (PMN), which express predominantly the type II molecule (IL-1R II). We found that Dex augments the levels of steady state transcripts encoding the IL-1R I and, most prominently, those of IL-1R II. Dex induced both transcripts via transcription-dependent mechanisms and by prolongation of the mRNAs half-lives. Inhibition of protein synthesis superinduced basal and Dex-augmented IL-1R II mRNA, whereas it completely inhibited the induction by Dex of IL-1R I transcripts. Induction of IL-1R II mRNA by Dex was associated with augmented membrane expression and release of the type II IL-1 binding molecule. This effect was mediated by the GC receptor. Other steroids (17 beta-estradiol, progesterone, and testosterone) were ineffective. The concentrations of IL-1 alpha and IL-1 receptor antagonist required to displace the binding of IL-1 beta to the soluble form of the decoy molecule induced by Dex from PMN were, respectively, 100 and 2 times higher compared with IL-1 beta. The induction by Dex of the type II receptor, a decoy molecule for IL-1, may contribute to the immunosuppressive and antiinflammatory activities of Dex.
MeSH Terms
Dexamethasone/pharmacology
Half-Life
Humans
In Vitro Techniques
Interleukin-1/metabolism
Ligands
Neutrophils/drug effects,metabolism
RNA, Messenger/metabolism
Receptors, Interleukin-1/antagonists & inhibitors,biosynthesis,metabolism
Solubility
Chemicals
Interleukin-1
Ligands
RNA, Messenger
Receptors, Interleukin-1
Dexamethasone
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Re F
Istituto di Ricerche Farmacologiche Mario Negri, Centro Daniela e Catullo Borgomainerio, Milano, Italy.
Muzio M
De Rossi M
Polentarutti N
Giri J G
Mantovani A
Colotta F
References (28)
28 references, click to expand
-
Analysis of the suppression of IL-1 alpha and IL-1 beta production in human peripheral blood mononuclear adherent cells by a glucocorticoid hormone.
J Immunol. 1988 Mar 15;140(6):1895-902
PMID: 3257992
-
Induction of high-affinity interleukin 1 receptor on human peripheral blood lymphocytes by glucocorticoid hormones.
J Exp Med. 1988 Mar 1;167(3):924-36
PMID: 2965211
-
cDNA expression cloning of the IL-1 receptor, a member of the immunoglobulin superfamily.
Science. 1988 Jul 29;241(4865):585-9
PMID: 2969618
-
Differential binding of IL-1 alpha and IL-1 beta to receptors on B and T cells.
FEBS Lett. 1989 Jan 30;243(2):394-8
PMID: 2521831
-
T-cell interleukin 1 receptor cDNA expressed in Chinese hamster ovary cells regulates functional responses to interleukin 1.
Proc Natl Acad Sci U S A. 1989 May;86(9):3045-9
PMID: 2470087
-
Potential antiinflammatory effects of interleukin 4: suppression of human monocyte tumor necrosis factor alpha, interleukin 1, and prostaglandin E2.
Proc Natl Acad Sci U S A. 1989 May;86(10):3803-7
PMID: 2786204
-
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):17416-9
PMID: 2145273
-
A soluble form of the interleukin-1 receptor produced by a human B cell line.
FEBS Lett. 1990 Oct 15;272(1-2):133-6
PMID: 1699802
-
Endotoxin-induced cytokine gene expression in vivo. II. Regulation of tumor necrosis factor and interleukin-1 alpha/beta expression and suppression.
Am J Pathol. 1990 Nov;137(5):1173-85
PMID: 2240164
-
IL-1 signal transduction pathways. I. Two functional IL-1 receptors are expressed in T cells.
J Immunol. 1991 Jan 1;146(1):136-43
PMID: 1845804
-
Interleukin-1 and interleukin-1 antagonism.
Blood. 1991 Apr 15;77(8):1627-52
PMID: 1826616
-
Interleukin-1 receptor antagonist competitively inhibits the binding of interleukin-1 to the type II interleukin-1 receptor.
J Biol Chem. 1991 Aug 5;266(22):14147-50
PMID: 1830582
-
Endothelial cells express the interleukin-1 receptor type I.
Blood. 1991 Sep 1;78(5):1262-7
PMID: 1831679
-
Binding of IL-1 beta to IL-1R type II at single cell level.
J Immunol. 1991 Sep 1;147(5):1561-6
PMID: 1831828
-
A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types.
EMBO J. 1991 Oct;10(10):2821-32
PMID: 1833184
-
Interleukin-1 receptor antagonist binds to the type II interleukin-1 receptor on B cells and neutrophils.
J Biol Chem. 1991 Oct 25;266(30):20311-5
PMID: 1834644
-
Interleukin-1 represents a new modality for the activation of extracellular signal-regulated kinases/microtubule-associated protein-2 kinases.
J Biol Chem. 1991 Nov 25;266(33):22661-70
PMID: 1658005
-
Purification and characterization of a novel soluble receptor for interleukin 1.
J Exp Med. 1991 Nov 1;174(5):1251-4
PMID: 1834761
-
Interleukin 1 induces NF-kappa B through its type I but not its type II receptor in lymphocytes.
J Biol Chem. 1992 Aug 5;267(22):15836-41
PMID: 1386364
-
Type II interleukin-1 receptor is not expressed in cultured endothelial cells and is not involved in endothelial cell activation.
Blood. 1993 Mar 1;81(5):1347-51
PMID: 8443394
-
Interleukin-1 modulation of cytokine receptors on human neutrophils: in vitro and in vivo studies.
Blood. 1993 Apr 1;81(7):1745-54
PMID: 7681702
-
Interleukin 1 signaling occurs exclusively via the type I receptor.
Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6155-9
PMID: 8327496
-
Corticosteroids inhibit murine macrophage Ia expression and interleukin 1 production.
J Immunol. 1982 Nov;129(5):1803-5
PMID: 6811653
-
Ligand: a versatile computerized approach for characterization of ligand-binding systems.
Anal Biochem. 1980 Sep 1;107(1):220-39
PMID: 6254391
-
Interleukin-1 type II receptor: a decoy target for IL-1 that is regulated by IL-4.
Science. 1993 Jul 23;261(5120):472-5
PMID: 8332913
-
Dexamethasone inhibition of interleukin 1 beta production by human monocytes. Posttranscriptional mechanisms.
J Clin Invest. 1988 Jan;81(1):237-44
PMID: 3257219
-
Glucocorticoids inhibit transcriptional and post-transcriptional expression of interleukin 1 in U937 cells.
J Immunol. 1987 Dec 15;139(12):4129-34
PMID: 2826581
-
Glucocorticoids selectively inhibit the transcription of the interleukin 1 beta gene and decrease the stability of interleukin 1 beta mRNA.
Proc Natl Acad Sci U S A. 1988 Feb;85(4):1204-8
PMID: 3257575