The interleukin-22/STAT3 pathway potentiates expression of inducible nitric-oxide synthase in human colon carcinoma cells

J Biol Chem. 2007 Jun 1;282(22):16006-15. doi: 10.1074/jbc.M611040200. Epub 2007 Apr 16.

Abstract

Inducible nitric-oxide synthase (iNOS) has been identified as a marker and mediator of disease in human colonic inflammation and carcinogenesis. Accordingly, identification of mediators that trigger iNOS in colon carcinoma/epithelial cells is an important topic of current research. Here we demonstrate that interleukin (IL)-22, a newly described member of the IL-10 cytokine family, potently synergizes with interferon (IFN)-gamma for iNOS expression in human DLD-1 colon carcinoma cells. Detection of both IL-22 receptor chains and STAT3 phosphorylation proved robust IL-22 responsiveness of these cells. Short interfering RNA technology identified STAT3 as being crucial for up-regulation of iNOS. Compared with IFNgamma, STAT1 phosphorylation by IL-22 was insufficient. IL-22 did not stabilize IL-1beta/tumor necrosis factor-alpha/IFNgamma-induced iNOS mRNA. IL-22 also failed to amplify expression of the prototypic IFNgamma-inducible parameters IL-18-binding protein and CXCL-10, indicating that IL-22 is not a general amplifier of IFNgamma functions. This assumption is furthermore supported by the observation that IL-22 was unable to enhance cellular activation of the pro-inflammatory transcription factor nuclear factor-kappaB. In contrast, IL-22 increased iNOS promoter activation as detected by using DLD-1 cells stably transfected with a corresponding 16-kb promoter construct (pNOS2(16)-Luc). IL-22 likewise enhanced iNOS in Caco-2 colon carcinoma cells. With IL-22 we introduce a novel potent determinant of iNOS expression in human colon carcinoma/epithelial cells. Considering the eminent functions of STAT3 and iNOS in inflammation and carcinogenesis, IL-22 may represent a novel target for immunotherapeutic intervention.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Caco-2 Cells
  • Colonic Neoplasms / drug therapy
  • Colonic Neoplasms / genetics
  • Colonic Neoplasms / metabolism*
  • Cytokines / metabolism
  • Cytokines / pharmacology
  • Gene Expression Regulation, Enzymologic / drug effects*
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Humans
  • Immunotherapy
  • Inflammation / drug therapy
  • Inflammation / genetics
  • Inflammation / metabolism
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Interleukin-22
  • Interleukins / pharmacology*
  • Interleukins / therapeutic use
  • NF-kappa B / metabolism
  • Neoplasm Proteins / biosynthesis*
  • Neoplasm Proteins / genetics
  • Nitric Oxide Synthase Type II / biosynthesis*
  • Nitric Oxide Synthase Type II / genetics
  • Promoter Regions, Genetic / genetics
  • RNA, Messenger / biosynthesis
  • RNA, Neoplasm / biosynthesis
  • RNA, Neoplasm / genetics
  • Receptors, Interleukin / biosynthesis
  • STAT1 Transcription Factor / metabolism
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction / drug effects*

Substances

  • Cytokines
  • Intercellular Signaling Peptides and Proteins
  • Interleukins
  • NF-kappa B
  • Neoplasm Proteins
  • RNA, Messenger
  • RNA, Neoplasm
  • Receptors, Interleukin
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • interleukin-18 binding protein
  • Nitric Oxide Synthase Type II