IFN-alpha priming results in a gain of proinflammatory function by IL-10: implications for systemic lupus erythematosus pathogenesis

J Immunol. 2004 May 15;172(10):6476-81. doi: 10.4049/jimmunol.172.10.6476.

Abstract

Interleukin-10 is a predominantly anti-inflammatory cytokine that inhibits macrophage and dendritic cell function, but can acquire proinflammatory activity during immune responses. We investigated whether type I IFNs, which are elevated during infections and in autoimmune diseases, modulate the activity of IL-10. Priming of primary human macrophages with low concentrations of IFN-alpha diminished the ability of IL-10 to suppress TNF-alpha production. IFN-alpha conferred a proinflammatory gain of function on IL-10, leading to IL-10 activation of expression of IFN-gamma-inducible, STAT1-dependent genes such as IFN regulatory factor 1, IFN-gamma-inducible protein-10 (CXCL10), and monokine induced by IFN-gamma (CXCL9). IFN-alpha priming resulted in greatly enhanced STAT1 activation in response to IL-10, and STAT1 was required for IL-10 activation of IFN-gamma-inducible protein-10 and monokine induced by IFN-gamma expression in IFN-alpha-primed cells. In control, unprimed cells, IL-10 activation of STAT1 was suppressed by constitutive activity of protein kinase C and Src homology 2 domain-containing phosphatase 1. These results demonstrate that type I IFNs regulate the balance between IL-10 anti- and proinflammatory activity, and provide insight into molecular mechanisms that regulate IL-10 function. Gain of IL-10 proinflammatory functions may contribute to its pathogenic role in autoimmune diseases characterized by elevated type I IFN levels, such as systemic lupus erythematosus.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Cells, Cultured
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drug Synergism
  • Humans
  • Inflammation Mediators / antagonists & inhibitors
  • Inflammation Mediators / physiology*
  • Interferon-alpha / immunology*
  • Interferon-alpha / pharmacology
  • Interleukin-10 / antagonists & inhibitors
  • Interleukin-10 / physiology*
  • Lipopolysaccharides / antagonists & inhibitors
  • Lipopolysaccharides / pharmacology
  • Lupus Erythematosus, Systemic / genetics
  • Lupus Erythematosus, Systemic / immunology*
  • Macrophage Activation / immunology
  • Macrophage Colony-Stimulating Factor / pharmacology
  • Macrophages / immunology
  • Macrophages / metabolism
  • Mice
  • Mice, Knockout
  • Mice, Mutant Strains
  • Protein Kinase C / metabolism
  • Protein Kinase C / physiology
  • Protein Kinase C-delta
  • Protein Phosphatase 1
  • Protein Tyrosine Phosphatases / metabolism
  • Protein Tyrosine Phosphatases / physiology
  • STAT1 Transcription Factor
  • Trans-Activators / antagonists & inhibitors
  • Trans-Activators / deficiency
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Up-Regulation / immunology

Substances

  • DNA-Binding Proteins
  • Inflammation Mediators
  • Interferon-alpha
  • Lipopolysaccharides
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Stat1 protein, mouse
  • Trans-Activators
  • Interleukin-10
  • Macrophage Colony-Stimulating Factor
  • Prkcd protein, mouse
  • PRKCD protein, human
  • Protein Kinase C
  • Protein Kinase C-delta
  • Protein Phosphatase 1
  • Protein Tyrosine Phosphatases