Benzo(a)pyrene facilitates dermatophagoides group 1 (Der f 1)-induced epithelial cytokine release through aryl hydrocarbon receptor in asthma

Allergy. 2019 Sep;74(9):1675-1690. doi: 10.1111/all.13784. Epub 2019 Jun 19.

Abstract

Background: Environmental pollutants, which coexist with allergens, have been associated with the exacerbation of asthma. However, the underlying molecular mechanisms remain elusive. We sought to determine whether benzo(a)pyrene (BaP) co-exposure with dermatophagoides group 1 allergen (Der f 1) can potentiate Der f 1-induced asthma and its underlying mechanisms.

Methods: The effect of BaP was investigated in Der f 1-induced mouse model of asthma, including airway hyper-responsiveness, allergic inflammation, and epithelial-derived cytokines. The impact of BaP on Der f 1-induced airway epithelial cell oxidative stress (ROS) and cytokine release was further analyzed. The role of aryl hydrocarbon receptor (AhR) signaling in BaP-promoted Der f 1-induced ROS, cytokine production, and allergic inflammation was also investigated.

Results: Compared with Der f 1, BaP co-exposure with Der f 1 led to airway hyper-responsiveness and increased lung inflammation in mouse model of asthma. Increased expression of TSLP, IL-33, and IL-25 was also found in the airways of these mice. Moreover, BaP co-exposure with Der f 1 activated AhR signaling with increased expression of AhR and CYP1A1 and promoted airway epithelial ROS generation and TSLP and IL-33, but not IL-25, expression. Interestingly, AhR antagonist CH223191 or cells with AhR knockdown abrogated the increased expression of ROS, TSLP, and IL-33. Furthermore, ROS inhibitor N-acetyl-L-cysteine (NAC) also suppressed BaP co-exposure-induced expression of epithelial TSLP, IL-33, and IL-25. Finally, AhR antagonist CH223191 and NAC inhibited BaP co-exposure with Der f 1-induced lung inflammation.

Conclusions: Our findings suggest that BaP facilitates Der f 1-induced epithelial cytokine release through the AhR-ROS axis.

Keywords: Aryl hydrocarbon receptor; IL-25; IL-33; TSLP; benzo(a)pyrene (BaP); dermatophagoides group 1 allergen (Der f 1); reactive oxygen species.

Publication types

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

MeSH terms

  • Allergens / immunology
  • Animals
  • Antigens, Dermatophagoides / immunology*
  • Arthropod Proteins / immunology*
  • Asthma / etiology*
  • Asthma / metabolism*
  • Benzo(a)pyrene / adverse effects*
  • Cysteine Endopeptidases / immunology*
  • Cytokines / biosynthesis*
  • Disease Models, Animal
  • Environmental Pollutants / adverse effects
  • Epithelial Cells / metabolism
  • Humans
  • Mice
  • Reactive Oxygen Species / metabolism
  • Receptors, Aryl Hydrocarbon / metabolism*
  • Respiratory Mucosa / immunology*
  • Respiratory Mucosa / metabolism*

Substances

  • Allergens
  • Antigens, Dermatophagoides
  • Arthropod Proteins
  • Cytokines
  • Environmental Pollutants
  • Reactive Oxygen Species
  • Receptors, Aryl Hydrocarbon
  • Benzo(a)pyrene
  • Cysteine Endopeptidases
  • Dermatophagoides farinae antigen f 1