Exposure to ambient particulate matter induces a NASH-like phenotype and impairs hepatic glucose metabolism in an animal model

J Hepatol. 2013 Jan;58(1):148-54. doi: 10.1016/j.jhep.2012.08.009. Epub 2012 Aug 15.

Abstract

Background & aims: Air pollution is a global challenge to public health. Epidemiological studies have linked exposure to ambient particulate matter with aerodynamic diameters<2.5 μm (PM(2.5)) to the development of metabolic diseases. In this study, we investigated the effect of PM(2.5) exposure on liver pathogenesis and the mechanism by which ambient PM(2.5) modulates hepatic pathways and glucose homeostasis.

Methods: Using "Ohio's Air Pollution Exposure System for the Interrogation of Systemic Effects (OASIS)-1", we performed whole-body exposure of mice to concentrated ambient PM(2.5) for 3 or 10 weeks. Histological analyses, metabolic studies, as well as gene expression and molecular signal transduction analyses were performed to determine the effects and mechanisms by which PM(2.5) exposure promotes liver pathogenesis.

Results: Mice exposed to PM(2.5) for 10 weeks developed a non-alcoholic steatohepatitis (NASH)-like phenotype, characterized by hepatic steatosis, inflammation, and fibrosis. After PM(2.5) exposure, mice displayed impaired hepatic glycogen storage, glucose intolerance, and insulin resistance. Further investigation revealed that exposure to PM(2.5) led to activation of inflammatory response pathways mediated through c-Jun N-terminal kinase (JNK), nuclear factor kappa B (NF-κB), and Toll-like receptor 4 (TLR4), but suppression of the insulin receptor substrate 1 (IRS1)-mediated signaling. Moreover, PM(2.5) exposure repressed expression of the peroxisome proliferator-activated receptor (PPAR)γ and PPARα in the liver.

Conclusions: Our study suggests that PM(2.5) exposure represents a significant "hit" that triggers a NASH-like phenotype and impairs hepatic glucose metabolism. The information from this work has important implications in our understanding of air pollution-associated metabolic disorders.

Publication types

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

MeSH terms

  • Animals
  • Disease Models, Animal
  • Fatty Liver / etiology*
  • Fatty Liver / metabolism*
  • Glucose / metabolism*
  • Glucose Intolerance / etiology*
  • Glucose Intolerance / metabolism*
  • Glycogen / metabolism
  • Hepatitis / etiology
  • Hepatitis / metabolism
  • Homeostasis / physiology
  • Inhalation Exposure
  • Insulin / metabolism
  • Insulin Receptor Substrate Proteins / metabolism
  • Insulin Resistance / physiology
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Liver / metabolism
  • Liver Cirrhosis / etiology
  • Liver Cirrhosis / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NF-kappa B / metabolism
  • Non-alcoholic Fatty Liver Disease
  • PPAR alpha / metabolism
  • PPAR gamma / metabolism
  • Particulate Matter / toxicity*
  • Phenotype
  • Signal Transduction / physiology
  • Toll-Like Receptor 4 / metabolism

Substances

  • Insulin
  • Insulin Receptor Substrate Proteins
  • Irs1 protein, mouse
  • NF-kappa B
  • PPAR alpha
  • PPAR gamma
  • Particulate Matter
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Glycogen
  • JNK Mitogen-Activated Protein Kinases
  • Glucose