p53 mediates particulate matter-induced alveolar epithelial cell mitochondria-regulated apoptosis

Am J Respir Crit Care Med. 2006 Dec 1;174(11):1229-38. doi: 10.1164/rccm.200602-203OC. Epub 2006 Aug 31.

Abstract

Rationale: Exposure to particulate matter (PM) causes lung cancer by mechanisms that are unknown, but p53 dysfunction is implicated.

Objective: We determined whether p53 is required for PM-induced apoptosis in both human and rodent alveolar type (AT) 2 cells.

Methods: A well-characterized form of urban PM was used to determine whether it induces mitochondrial dysfunction (mitochondrial membrane potential change [DeltaPsi m] and caspase-9 activation), p53 protein and mRNA expression, and apoptosis (DNA fragmentation and annexin V staining) in vitro using A549 cells and primary isolated human and rat AT2 cells. The role of p53 was assessed using inhibitors of p53-dependent transcription, pifithrin-alpha, and a genetic approach (overexpressing E6 or dominant negative p53). In mice, the in vivo effects of PM causing p53 expression and apoptosis were assessed 72 h after a single PM intratracheal instillation.

Measurements and main results: PM-induced apoptosis in A549 cells was characterized by increased p53 mRNA and protein expression, mitochondrial translocation of Bax and p53, a reduction in DeltaPsi m, and caspase-9 activation, and these effects were blocked by inhibiting p53-dependent transcription. Similar findings were noted in primary isolated human and rat AT2 cells. A549-rho degrees cells that are incapable of mitochondrial reactive oxygen species production were protected against PM-induced DeltaPsi m, p53 expression, and apoptosis. In mice, PM induced p53 expression and apoptosis at the bronchoalveolar duct junctions.

Conclusions: These data suggest a novel interaction between p53 and the mitochondria in mediating PM-induced apoptosis that is relevant to the pathogenesis of lung cancer from air pollution.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / physiology*
  • Benzothiazoles / pharmacology
  • Cells, Cultured
  • DNA Fragmentation
  • Genes, p53 / physiology*
  • Humans
  • Immunohistochemistry
  • In Situ Nick-End Labeling
  • Mitochondria / drug effects
  • Mitochondria / physiology*
  • Particulate Matter / pharmacology*
  • Pulmonary Alveoli / drug effects
  • Pulmonary Alveoli / physiology*
  • Rats
  • Reactive Oxygen Species
  • Toluene / analogs & derivatives
  • Toluene / pharmacology
  • Transcription, Genetic / drug effects
  • Translocation, Genetic / physiology

Substances

  • Benzothiazoles
  • Particulate Matter
  • Reactive Oxygen Species
  • Toluene
  • pifithrin