Intestinal exposure to PCB 153 induces inflammation via the ATM/NEMO pathway

Toxicol Appl Pharmacol. 2018 Jan 15:339:24-33. doi: 10.1016/j.taap.2017.11.027. Epub 2017 Nov 29.

Abstract

Background: Polychlorinated biphenyls (PCBs) are persistent organic pollutants that adversely affect human health. PCBs bio-accumulate in organisms important for human consumption. PCBs accumulation in the body leads to activation of the transcription factor NF-κB, a major driver of inflammation. Despite dietary exposure being one of the main routes of exposure to PCBs, the gut has been widely ignored when studying the effects of PCBs.

Objectives: We investigated the effects of PCB 153 on the intestine and addressed whether PCB 153 affected intestinal permeability or inflammation and the mechanism by which this occurred.

Methods: Mice were orally exposed to PCB 153 and gut permeability was assessed. Intestinal epithelial cells (IECs) were collected and evaluated for evidence of genotoxicity and inflammation. A human IEC line (SW480) was used to examine the direct effects of PCB 153 on epithelial function. NF-кB activation was measured using a reporter assay, DNA damage was assessed, and cytokine expression was ascertained with real-time PCR.

Results: Mice orally exposed to PCB 153 had an increase in intestinal permeability and inflammatory cytokine expression in their IECs; inhibition of NF-кB ameliorated both these effects. This inflammation was associated with genotoxic damage and NF-кB activation. Exposure of SW480 cells to PCB 153 led to similar effects as seen in vivo. We found that activation of the ATM/NEMO pathway by genotoxic stress was upstream of NF-kB activation.

Conclusions: These results demonstrate that oral exposure to PCB 153 is genotoxic to IECs and induces downstream inflammation and barrier dysfunction in the intestinal epithelium.

Keywords: ATM; Intestinal inflammation; NF-κB; Nemo; PCB 153; Polychlorinated biphenyl.

Publication types

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

MeSH terms

  • Animals
  • Ataxia Telangiectasia Mutated Proteins / metabolism
  • Cell Line
  • DNA Damage / drug effects
  • DNA Damage / physiology
  • Humans
  • Inflammation / chemically induced
  • Inflammation / metabolism
  • Inflammation Mediators / metabolism
  • Intestinal Mucosa / drug effects*
  • Intestinal Mucosa / metabolism*
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Polychlorinated Biphenyls / toxicity*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology

Substances

  • Inflammation Mediators
  • Intracellular Signaling Peptides and Proteins
  • NEMO protein, mouse
  • Polychlorinated Biphenyls
  • Ataxia Telangiectasia Mutated Proteins
  • Atm protein, mouse
  • 2,4,5,2',4',5'-hexachlorobiphenyl