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Disruption of pulmonary lipid homeostasis drives cigarette smoke-induced lung inflammation in mice

Eur Respir J. 2015 Nov;46(5):1451-60. doi: 10.1183/09031936.00216914. Epub 2015 Jun 25.

Abstract

Overwhelming evidence links inflammation to the pathogenesis of smoking-related pulmonary diseases, especially chronic obstructive pulmonary disease (COPD). Despite an increased understanding of the disease pathogenesis, mechanisms initiating smoking-induced inflammatory processes remain incompletely understood. To investigate the mechanisms that initiate and propagate smoke-induced inflammation, we used a well-characterised mouse model of cigarette smoke exposure, mice deficient for interleukin (IL)-1α, IL-1β and Toll-like receptor 4, and antibodies blocking granulocyte-macrophage colony-stimulating factor (GM-CSF). Studies were also pursued using intranasal delivery of human oxidised low-density lipoprotein (hOxLDL), a source of oxidised lipids, to investigate the inflammatory processes associated with impaired lipid homeostasis. We found that cigarette smoke exposure rapidly led to lipid accumulation in pulmonary macrophages, a defining feature of foam cells, which in turn released high levels of IL-1α. In smoke-exposed IL-1α-deficient mice, phospholipids accumulated in the bronchoalveolar lavage, a phenomenon also observed when blocking GM-CSF. Intranasal administration of hOxLDL led to lipid accumulation in macrophages and initiated an inflammatory process that mirrored the characteristics of cigarette smoke-induced inflammation. These findings identify a link between lipid accumulation in macrophages, inflammation and damaged surfactant, suggesting that the response to damaged pulmonary surfactant is a central mechanism that drives cigarette smoke-induced inflammation. Further investigations are required to explore the role of distorted lipid homeostasis in the pathogenesis of COPD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bronchoalveolar Lavage Fluid
  • Disease Models, Animal
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism
  • Homeostasis
  • Humans
  • Interleukin-1alpha / metabolism*
  • Interleukin-1beta / metabolism
  • Lipoproteins, LDL / administration & dosage*
  • Macrophages, Alveolar / pathology*
  • Mice
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Pneumonia / chemically induced
  • Pneumonia / metabolism*
  • Pneumonia / physiopathology
  • Smoking / adverse effects*
  • Toll-Like Receptor 4 / metabolism

Substances

  • Interleukin-1alpha
  • Interleukin-1beta
  • Lipoproteins, LDL
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • oxidized low density lipoprotein
  • Granulocyte-Macrophage Colony-Stimulating Factor