Environmental particulate matter induces murine intestinal inflammatory responses and alters the gut microbiome

PLoS One. 2013 Apr 24;8(4):e62220. doi: 10.1371/journal.pone.0062220. Print 2013.

Abstract

Background: Particulate matter (PM) is a key pollutant in ambient air that has been associated with negative health conditions in urban environments. The aim of this study was to examine the effects of orally administered PM on the gut microbiome and immune function under normal and inflammatory conditions.

Methods: Wild-type 129/SvEv mice were gavaged with Ottawa urban PM10 (EHC-93) for 7-14 days and mucosal gene expression analyzed using Ingenuity Pathways software. Intestinal permeability was measured by lactulose/mannitol excretion in urine. At sacrifice, segments of small and large intestine were cultured and cytokine secretion measured. Splenocytes were isolated and incubated with PM10 for measurement of proliferation. Long-term effects of exposure (35 days) on intestinal cytokine expression were measured in wild-type and IL-10 deficient (IL-10(-/-)) mice. Microbial composition of stool samples was assessed using terminal restriction fragment length polymorphism. Short chain fatty acids were measured in caecum.

Results: Short-term treatment of wild-type mice with PM10 altered immune gene expression, enhanced pro-inflammatory cytokine secretion in the small intestine, increased gut permeability, and induced hyporesponsiveness in splenocytes. Long-term treatment of wild-type and IL-10(-/-) mice increased pro-inflammatory cytokine expression in the colon and altered short chain fatty acid concentrations and microbial composition. IL-10(-/-) mice had increased disease as evidenced by enhanced histological damage.

Conclusions: Ingestion of airborne particulate matter alters the gut microbiome and induces acute and chronic inflammatory responses in the intestine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Air Pollutants / adverse effects*
  • Animals
  • Colon / immunology
  • Colon / metabolism
  • Colon / microbiology
  • Cytokines / metabolism
  • Environmental Exposure / adverse effects
  • Fatty Acids, Volatile / metabolism
  • Female
  • Gene Expression Regulation
  • Gene Regulatory Networks
  • Inflammation / etiology
  • Intestinal Mucosa / metabolism
  • Intestine, Small / immunology
  • Intestine, Small / metabolism
  • Intestine, Small / microbiology
  • Intestines / immunology*
  • Intestines / microbiology*
  • Intestines / pathology
  • Mice
  • Mice, Knockout
  • Microbiota*
  • Particulate Matter / administration & dosage
  • Particulate Matter / adverse effects*
  • Permeability
  • Spleen / cytology
  • Spleen / immunology
  • Time Factors

Substances

  • Air Pollutants
  • Cytokines
  • Fatty Acids, Volatile
  • Particulate Matter