IL-21 enhances SOCS gene expression and inhibits LPS-induced cytokine production in human monocyte-derived dendritic cells

J Leukoc Biol. 2006 Jun;79(6):1279-85. doi: 10.1189/jlb.0905503. Epub 2006 Mar 21.

Abstract

Dendritic cells (DCs) play an important role in innate and adaptive immune responses. In addition to their phagocytic activity, DCs present foreign antigens to naïve T cells and regulate the development of adaptive immune responses. Upon contact with DCs, activated T cells produce large quantities of cytokines such as interferon-gamma (IFN-gamma) and interleukin (IL)-21, which have important immunoregulatory functions. Here, we have analyzed the effect of IL-21 and IFN-gamma on lipopolysaccharide (LPS)-induced maturation and cytokine production of human monocyte-derived DCs. IL-21 and IFN-gamma receptor genes were expressed in high levels in immature DCs. Pretreatment of immature DCs with IL-21 inhibited LPS-stimulated DC maturation and expression of CD86 and human leukocyte antigen class II (HLAII). IL-21 pretreatment also dramatically reduced LPS-stimulated production of tumor necrosis factor alpha, IL-12, CC chemokine ligand 5 (CCL5), and CXC chemokine ligand 10 (CXCL10) but not that of CXCL8. In contrast, IFN-gamma had a positive feedback effect on immature DCs, and it enhanced LPS-induced DC maturation and the production of cytokines. IL-21 weakly induced the expression Toll-like receptor 4 (TLR4) and translation initiation region (TIR) domain-containing adaptor protein (TIRAP) genes, whereas the expression of TIR domain-containing adaptor-inducing IFN-beta (TRIF), myeloid differentiation (MyD88) 88 factor, or TRIF-related adaptor molecule (TRAM) genes remained unchanged. However, IL-21 strongly stimulated the expression of suppressor of cytokine signaling (SOCS)-1 and SOCS-3 genes. SOCS are known to suppress DC functions and interfere with TLR4 signaling. Our results demonstrate that IL-21, a cytokine produced by activated T cells, can directly inhibit the activation and cytokine production of myeloid DCs, providing a negative feedback loop between DCs and T lymphocytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Communication
  • Cells, Cultured / drug effects
  • Cells, Cultured / immunology
  • Cells, Cultured / metabolism
  • Chemokine CCL5
  • Chemokines, CC / biosynthesis
  • Chemokines, CC / genetics
  • Chemokines, CXC / biosynthesis
  • Chemokines, CXC / genetics
  • Cytokines / biosynthesis*
  • Cytokines / genetics
  • Dendritic Cells / drug effects*
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Feedback, Physiological
  • Gene Expression Profiling
  • Gene Expression Regulation / drug effects*
  • HLA-DR Antigens / biosynthesis
  • Humans
  • Interferon gamma Receptor
  • Interferon-gamma / pharmacology
  • Interleukin-12 / biosynthesis
  • Interleukin-12 / genetics
  • Interleukin-21 Receptor alpha Subunit
  • Interleukins / pharmacology*
  • Interleukins / physiology
  • Intracellular Signaling Peptides and Proteins / genetics
  • Lipopolysaccharides / antagonists & inhibitors
  • Lymphocyte Activation
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Membrane Glycoproteins / biosynthesis
  • Membrane Glycoproteins / genetics
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics
  • Receptors, Interferon / biosynthesis
  • Receptors, Interferon / genetics
  • Receptors, Interleukin / biosynthesis
  • Receptors, Interleukin / genetics
  • Receptors, Interleukin-1 / biosynthesis
  • Receptors, Interleukin-1 / genetics
  • Receptors, Interleukin-21
  • Recombinant Proteins / pharmacology
  • Repressor Proteins / biosynthesis*
  • Repressor Proteins / genetics
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins / biosynthesis*
  • Suppressor of Cytokine Signaling Proteins / genetics
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism*
  • Toll-Like Receptor 4 / biosynthesis
  • Toll-Like Receptor 4 / genetics
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Tumor Necrosis Factor-alpha / genetics

Substances

  • CCL5 protein, human
  • Chemokine CCL5
  • Chemokines, CC
  • Chemokines, CXC
  • Cytokines
  • HLA-DR Antigens
  • IL21R protein, human
  • Interleukin-21 Receptor alpha Subunit
  • Interleukins
  • Intracellular Signaling Peptides and Proteins
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • RNA, Messenger
  • Receptors, Interferon
  • Receptors, Interleukin
  • Receptors, Interleukin-1
  • Receptors, Interleukin-21
  • Recombinant Proteins
  • Repressor Proteins
  • SOCS1 protein, human
  • SOCS3 protein, human
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling 3 Protein
  • Suppressor of Cytokine Signaling Proteins
  • TIRAP protein, human
  • TLR4 protein, human
  • Toll-Like Receptor 4
  • Tumor Necrosis Factor-alpha
  • Interleukin-12
  • Interferon-gamma
  • interleukin-21