Benzo[a]pyrene and tumor necrosis factor-α coordinately increase genotoxic damage and the production of proinflammatory mediators in alveolar epithelial type II cells

Toxicol Lett. 2011 Oct 10;206(2):121-9. doi: 10.1016/j.toxlet.2011.06.029. Epub 2011 Jul 2.

Abstract

Alveolar type II epithelial (AEII) cells regulate lung inflammatory response and, simultaneously, they are a target of environmental carcinogenic factors. We employed an in vitro model of rat AEII cells, the RLE-6TN cell line, in order to analyze the interactive effects of tumor necrosis factor-α (TNF-α), a cytokine which plays a key role in the initiation of inflammatory responses in the lung, and benzo[a]pyrene (BaP), a highly carcinogenic polycyclic aromatic hydrocarbon. TNF-α strongly augmented the formation of stable BaP diol epoxide-DNA adducts in AEII cells, which was associated with enhanced p53-Ser15 phosphorylation and decreased cell survival. The increased genotoxicity of BaP was associated with altered expression of cytochrome P450 (CYP) enzymes involved in its bioactivation, a simultaneous suppression of CYP1A1 and enhancement of CYP1B1 expression. Importantly, BaP and TNF-α acted synergistically to upregulate key inflammatory regulators in AEII cells, including the expression of inducible NO synthase and cyclooxygenase-2 (COX-2), and enhanced prostaglandin E2 production and expression of proinflammatory cytokines, such as TNF-α, interleukin-1β and interleukin-6. We observed that BaP and TNF-α together strongly activated p38 kinase, a principal regulator of inflammatory response. SB202190, a specific p38 inhibitor, prevented induction of both COX-2 and proinflammatory cytokines, thus confirming that p38 activity was crucial for the observed inflammatory reaction. Taken together, our data demonstrated, for the first time, that a proinflammatory cytokine and an environmental PAH may interact to potentiate both DNA damage and the inflammatory response in AEII cells, which may occur through coordinated upregulation of p38 activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alveolar Epithelial Cells / drug effects*
  • Alveolar Epithelial Cells / immunology
  • Alveolar Epithelial Cells / metabolism*
  • Animals
  • Apoptosis / drug effects
  • Aryl Hydrocarbon Hydroxylases / genetics
  • Aryl Hydrocarbon Hydroxylases / metabolism
  • Benzo(a)pyrene / metabolism
  • Benzo(a)pyrene / toxicity*
  • Carcinogens, Environmental / toxicity
  • Cell Line
  • Cell Proliferation / drug effects
  • Cytochrome P-450 CYP1A1 / genetics
  • Cytochrome P-450 CYP1A1 / metabolism
  • Cytochrome P-450 CYP1B1
  • DNA Adducts / metabolism*
  • Enzyme Activation / drug effects
  • Gene Expression Regulation / drug effects
  • Inflammation Mediators / metabolism*
  • Mutagens / toxicity*
  • Phosphorylation / drug effects
  • Protein Kinase Inhibitors / pharmacology
  • Protein Processing, Post-Translational / drug effects
  • RNA, Messenger / metabolism
  • Rats
  • Tumor Necrosis Factor-alpha / metabolism*
  • Tumor Suppressor Protein p53 / metabolism
  • p38 Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Carcinogens, Environmental
  • DNA Adducts
  • Inflammation Mediators
  • Mutagens
  • Protein Kinase Inhibitors
  • RNA, Messenger
  • Tumor Necrosis Factor-alpha
  • Tumor Suppressor Protein p53
  • Benzo(a)pyrene
  • Aryl Hydrocarbon Hydroxylases
  • Cyp1b1 protein, rat
  • Cytochrome P-450 CYP1A1
  • Cytochrome P-450 CYP1B1
  • p38 Mitogen-Activated Protein Kinases