Protective role of cytochrome P450 1A1 (CYP1A1) against benzo[a]pyrene-induced toxicity in mouse aorta

Toxicology. 2014 Feb 28:316:34-42. doi: 10.1016/j.tox.2013.12.005. Epub 2014 Jan 3.

Abstract

Benzo[a]pyrene (BaP) is an environmental pollutant produced by combustive processes, such as cigarette smoke and coke ovens, and is implicated in the pathogenesis of atherosclerosis. Cytochrome P450 1A1 (CYP1A1) plays a role in both metabolic activation and detoxication of BaP in a context-dependent manner. The role of CYP1A1 in BaP-induced toxicity in aorta remains unknown. First, we fed Apoe⁻/⁻ mice an atherogenic diet plus BaP and found that oral BaP-enhanced atherosclerosis is associated with increased reactive oxygen species (ROS) and inflammatory markers, such as plasma tumor necrosis factor levels and aortic mRNA expression of vascular endothelial growth factor A (Vegfa). We next examined the effect of an atherogenic diet plus BaP on ROS and inflammatory markers in Cyp1a1⁻/⁻ mice. Although this treatment was not sufficient to induce atherosclerotic lesions in Cyp1a1⁻/⁻ mice, plasma antioxidant levels were decreased in Cyp1a1⁻/⁻ mice even in the absence of BaP treatment. The atherogenic diet plus BaP effectively elevated plasma ROS levels and expression of atherosclerosis-related genes, specifically Vegfa, in Cyp1a1⁻/⁻ mice compared with wild-type mice. BaP treatment increased Vegfa mRNA levels in mouse embryonic fibroblasts from Cyp1a1⁻/⁻ mice but not from wild-type mice. BaP-induced DNA adduct formation was increased in the aorta of Cyp1a1⁻/⁻ mice, but not wild-type or Apoe⁻/⁻ mice, and the atherogenic diet decreased BaP-induced DNA adducts in Cyp1a1⁻/⁻ mice compared with mice on a control diet. These data suggest that ROS production contributes to BaP-exacerbated atherosclerosis and that CYP1A1 plays a protective role against oral BaP toxicity in aorta.

Keywords: Apoe(−/−) mice; Atherosclerosis; Benzo[a]pyrene; Cyp1a1(−/−) mice; DNA adduct formation; Reactive oxygen species.

Publication types

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

MeSH terms

  • Administration, Oral
  • Animals
  • Antioxidants / metabolism
  • Aorta / drug effects*
  • Aorta / pathology
  • Apolipoproteins E / genetics
  • Atherosclerosis / etiology*
  • Atherosclerosis / genetics
  • Atherosclerosis / pathology
  • Benzo(a)pyrene / administration & dosage
  • Benzo(a)pyrene / toxicity*
  • Cytochrome P-450 CYP1A1 / metabolism*
  • DNA Adducts
  • Environmental Pollutants / administration & dosage
  • Environmental Pollutants / toxicity*
  • Inflammation Mediators / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • RNA, Messenger / metabolism
  • Reactive Oxygen Species / metabolism
  • Vascular Endothelial Growth Factor A / genetics

Substances

  • Antioxidants
  • Apolipoproteins E
  • DNA Adducts
  • Environmental Pollutants
  • Inflammation Mediators
  • RNA, Messenger
  • Reactive Oxygen Species
  • Vascular Endothelial Growth Factor A
  • Benzo(a)pyrene
  • Cytochrome P-450 CYP1A1