STAT6 activation in ulcerative colitis: a new target for prevention of IL-13-induced colon epithelial cell dysfunction

Inflamm Bowel Dis. 2011 Nov;17(11):2224-34. doi: 10.1002/ibd.21628. Epub 2011 Feb 9.

Abstract

Background: Interleukin 13 (IL-13) is upregulated in ulcerative colitis (UC) and increases colon epithelial permeability by inducing apoptosis and expression of the pore-forming tight junction protein claudin-2. IL-13 induces activation of signal transducer and activator of transcription 6 (STAT6). However, the STAT6 phosphorylation status in patients with UC is unknown, as is the effect of STAT6 inhibition on colonic epithelium exposed to IL-13. The study aims were to determine if mucosal STAT6 phosphorylation is increased in patients with UC, and if STAT6 inhibition attenuates IL-13-induced colon epithelial cell dysfunction.

Methods: Immunohistochemical staining for phosphorylated (p) STAT6 was performed on colonic tissue from newly diagnosed pediatric subjects with UC (early UC) or Crohn's disease (CD), colectomy tissue from adults with UC (advanced UC), and controls. Colon HT-29 and T84 cells were transfected with STAT6 small interfering RNA (siRNA), or treated with suberoylanilide hydroxamic acid (SAHA), a histone deacetylase inhibitor that inhibits STAT6, prior to IL-13 treatment.

Results: The median score for epithelial pSTAT6 was 0 in control subjects, 2 in early UC (versus control P = 0.019), 4 in advanced UC (P = 0.003), and 0 in CD (P = 0.4). Cell transfection with STAT6 siRNA prevented IL-13-induced apoptosis and claudin-2 expression. SAHA inhibited IL-13-induced STAT6 phosphorylation, apoptosis, and claudin-2 expression, and mitigated IL-13-induced reductions in transepithelial resistance.

Conclusions: UC is associated with increased colonic epithelial STAT6 phosphorylation, and STAT6 inhibition prevents IL-13-induced apoptosis and barrier disruption. These data identify STAT6 as a novel target for UC treatment and support further study of SAHA as a therapeutic agent.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / drug effects
  • Blotting, Western
  • Case-Control Studies
  • Cells, Cultured
  • Child
  • Claudins / genetics
  • Claudins / metabolism
  • Colitis, Ulcerative / genetics
  • Colitis, Ulcerative / metabolism*
  • Colitis, Ulcerative / pathology
  • Colon / drug effects
  • Colon / metabolism*
  • Colon / pathology
  • Crohn Disease / genetics
  • Crohn Disease / metabolism*
  • Crohn Disease / pathology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology*
  • Female
  • Humans
  • Hydroxamic Acids / pharmacology
  • Immunoenzyme Techniques
  • Interleukin-13 / pharmacology*
  • Male
  • Phosphorylation
  • RNA, Messenger / genetics
  • RNA, Small Interfering / genetics
  • Real-Time Polymerase Chain Reaction
  • STAT6 Transcription Factor / antagonists & inhibitors
  • STAT6 Transcription Factor / genetics
  • STAT6 Transcription Factor / metabolism*
  • Signal Transduction
  • Up-Regulation
  • Vorinostat

Substances

  • CLDN2 protein, human
  • Claudins
  • Hydroxamic Acids
  • Interleukin-13
  • RNA, Messenger
  • RNA, Small Interfering
  • STAT6 Transcription Factor
  • STAT6 protein, human
  • Vorinostat