Oral administration of transforming growth factor-β1 (TGF-β1) protects the immature gut from injury via Smad protein-dependent suppression of epithelial nuclear factor κB (NF-κB) signaling and proinflammatory cytokine production

J Biol Chem. 2013 Nov 29;288(48):34757-66. doi: 10.1074/jbc.M113.503946. Epub 2013 Oct 15.

Abstract

Inflammatory immune responses play an important role in mucosal homeostasis and gut diseases. Nuclear factor κB (NF-κB), central to the proinflammatory cascade, is activated in necrotizing enterocolitis (NEC), a devastating condition of intestinal injury with extensive inflammation in premature infants. TGF-β is a strong immune suppressor and a factor in breast milk, which has been shown to be protective against NEC. In an NEC animal model, oral administration of the isoform TGF-β1 activated the downstream effector Smad2 in intestine and significantly reduced NEC incidence. In addition, TGF-β1 suppressed NF-κB activation, maintained levels of the NF-κB inhibitor IκBα in the intestinal epithelium, and systemically decreased serum levels of IL-6 and IFN-γ. The immature human fetal intestinal epithelial cell line H4 was used as a reductionistic model of the immature enterocyte to investigate mechanism. TGF-β1 pretreatment inhibited the TNF-α-induced IκBα phosphorylation that targets the IκBα protein for degradation and inhibited NF-κB activation. Chromatin immunoprecipitation (ChIP) assays demonstrated decreased NF-κB binding to the promoters of IL-6, IL-8, and IκBα in response to TNF-α with TGF-β1 pretreatment. These TGF-β1 effects appear to be mediated through the canonical Smad pathway as silencing of the TGF-β central mediator Smad4 resulted in loss of the TGF-β1 effects. Thus, TGF-β1 is capable of eliciting anti-inflammatory effects by inhibiting NF-κB specifically in the intestinal epithelium as well as by decreasing systemic IL-6 and IFN-γ levels. Oral administration of TGF-β1 therefore can potentially be used to protect against gastrointestinal diseases.

Keywords: Chromatin Immunoprecipitation (ChIP); Inflammation; Innate Immunity; Intestinal Epithelium; NF-kappa B (NF-KB); SMAD Transcription Factor; Transforming Growth Factor Beta (TGFbeta).

Publication types

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

MeSH terms

  • Administration, Oral
  • Animals
  • Cell Line
  • Gastrointestinal Diseases / drug therapy*
  • Gastrointestinal Diseases / metabolism
  • Gastrointestinal Diseases / pathology
  • Humans
  • Immunity, Innate / genetics
  • Inflammation / drug therapy
  • Inflammation / genetics
  • Inflammation / metabolism*
  • Interferon-gamma / metabolism
  • Interleukin-6 / metabolism
  • Interleukin-8
  • Intestinal Mucosa / injuries
  • Intestinal Mucosa / metabolism
  • NF-kappa B / metabolism*
  • Promoter Regions, Genetic
  • Rats
  • Signal Transduction
  • Smad Proteins / metabolism*
  • Smad2 Protein / metabolism
  • Transforming Growth Factor beta1 / administration & dosage*
  • Transforming Growth Factor beta1 / metabolism

Substances

  • Interleukin-6
  • Interleukin-8
  • NF-kappa B
  • SMAD2 protein, human
  • Smad Proteins
  • Smad2 Protein
  • Transforming Growth Factor beta1
  • Interferon-gamma