IFN regulatory factor-1-mediated transcriptional activation of mouse STAT-induced STAT inhibitor-1 gene promoter by IFN-gamma

J Immunol. 2000 Jun 1;164(11):5833-43. doi: 10.4049/jimmunol.164.11.5833.

Abstract

STAT-induced STAT inhibitor-1 (SSI-1), also referred to as suppressor of cytokine signaling-1 and JAK-binding protein, is a member of a new family, the members of which are negative regulators of cytokine signals. SSI-1 is induced by various cytokines; however, the transcriptional mechanism of the SSI-1 gene is not fully understood. Here, we showed that transcription of the mouse SSI-1 gene was initiated from six adjoining sites accompanying three GC boxes and a single GC box-like element near them, but not from the TATA box or an initiator sequence. We also showed that IFN-gamma induced SSI-1 mRNA more strongly than IL-6 in NIH-3T3 fibroblasts and that this IFN-gamma effect was mediated by Stat1. To determine the signal pathway downstream of Stat1, transcriptional activities of several mutant promoters were examined. The region mediating stimulatory effect of IFN-gamma to the gene transcription was localized to the -88/-60 region containing three tandem GAAA units, named variant IFN-gamma-responsive element (VIRE), while four IFN-gamma activation site (GAS)-like elements located far upstream were not related to the IFN-gamma response. Gel-shift assays revealed that IFN-gamma induced IFN regulatory factor-1 (IRF-1) binding to VIRE, but not that of IRF-2 or three components of ISGF3. Furthermore, forced expression of IRF-1 mimicked and that of IRF-2 inhibited the stimulatory effect of IFN-gamma on SSI-1 gene transcription. Finally, mouse embryonal fibroblasts lacking IRF-1 showed impaired SSI-1 mRNA induction by IFN-gamma. These results demonstrated that IRF-1, which is induced by activation of Stat1, mediated transcriptional activation of the SSI-1 gene by IFN-gamma via VIRE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells / metabolism
  • Animals
  • Base Sequence
  • Carrier Proteins / biosynthesis
  • Carrier Proteins / chemistry
  • Carrier Proteins / genetics*
  • Carrier Proteins / metabolism
  • Cytokines / pharmacology
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology*
  • Drug Synergism
  • Electrophoresis, Polyacrylamide Gel
  • Fibroblasts / metabolism
  • Growth Substances / pharmacology
  • Interferon Regulatory Factor-1
  • Interferon-gamma / physiology*
  • Mice
  • Molecular Sequence Data
  • Phosphoproteins / deficiency
  • Phosphoproteins / genetics
  • Phosphoproteins / physiology*
  • Promoter Regions, Genetic / immunology*
  • RNA, Messenger / biosynthesis
  • Repressor Proteins*
  • Response Elements / immunology
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Tandem Repeat Sequences / immunology
  • Trans-Activators / physiology*
  • Transcription, Genetic / immunology
  • Tumor Necrosis Factor-alpha / physiology

Substances

  • Carrier Proteins
  • Cytokines
  • DNA-Binding Proteins
  • Growth Substances
  • Interferon Regulatory Factor-1
  • Irf1 protein, mouse
  • Phosphoproteins
  • RNA, Messenger
  • Repressor Proteins
  • Socs1 protein, mouse
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins
  • Trans-Activators
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma