Pyrrolidine dithiocarbamate inhibits interleukin-6 signaling through impaired STAT3 activation and association with transcriptional coactivators in hepatocytes

J Biol Chem. 2006 Oct 20;281(42):31369-79. doi: 10.1074/jbc.M603762200. Epub 2006 Aug 22.

Abstract

Interleukin (IL)-6 is a proinflammatory cytokine that has been implicated in the expression of acute phase plasma proteins and hepatic insulin resistance through activation of the JAK/STAT3 pathway. Although previous studies have demonstrated that pyrrolidine dithiocarbamate (PDTC) exerts protection against inflammatory responses, its role in the regulation of IL-6 receptor signaling remains unclear. Here we show that treatment of cultured HepG2 hepatoma cells with PDTC inhibits IL-6-stimulated tyrosine phosphorylation and subsequent nuclear translocation of STAT3 in a dose- and time-dependent fashion. No inhibition of JAK-1 activity was observed. To provide insight into PDTC signaling, we constructed a conditionally active STAT3 by fusing it with the ligand binding domain of the estrogen receptor (STAT3-ER). In the presence of 4-hydroxytamoxifen STAT3-ER was translocated in the nucleus of HepG2 cells in a phosphorylation-independent manner, and treatment with PDTC mitigated the response. Although STAT3 coprecipitated with heat-shock protein 90 (Hsp90) in control cells, coprecipitation of the two proteins was greatly reduced after PDTC treatment or after exposure to geldanamycin, an Hsp90 inhibitor. As a result there was a decrease in IL-6-induced association of STAT3 with the transcriptional coactivators FOXO1a and C/EBPbeta together with significant reduction in the expression of SOCS-3 protein and that of two major acute phase plasma proteins. Importantly, treatment of HepG2 cells and a primary culture of rat hepatocytes with PDTC restored insulin responsiveness that was abrogated by IL-6. These studies are consistent with the ability of PDTC to down-regulate IL-6-induced STAT3 activation by altering the stability of STAT3-Hsp90 complex.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Active Transport, Cell Nucleus
  • Antioxidants / pharmacology
  • Cell Nucleus / metabolism
  • Chloramphenicol O-Acetyltransferase / metabolism
  • Down-Regulation
  • HSP90 Heat-Shock Proteins / metabolism
  • Hepatocytes / metabolism*
  • Humans
  • Interleukin-6 / metabolism*
  • Pyrrolidines / pharmacology*
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction*
  • Tamoxifen / analogs & derivatives
  • Tamoxifen / pharmacology
  • Thiocarbamates / pharmacology*
  • Transcriptional Activation

Substances

  • Antioxidants
  • HSP90 Heat-Shock Proteins
  • Interleukin-6
  • Pyrrolidines
  • STAT3 Transcription Factor
  • Thiocarbamates
  • Tamoxifen
  • afimoxifene
  • pyrrolidine dithiocarbamic acid
  • Chloramphenicol O-Acetyltransferase