AITC inhibits fibroblast-myofibroblast transition via TRPA1-independent MAPK and NRF2/HO-1 pathways and reverses corticosteroids insensitivity in human lung fibroblasts

Respir Res. 2021 Feb 12;22(1):51. doi: 10.1186/s12931-021-01636-9.

Abstract

Background: Little is known on the role of transient receptor potential ankyrin 1 (TRPA1) in fibroblast-myofibroblast transition (FMT) that can lead to airway remodeling which is a major problem for severe asthma and fibrosis. Thus, this study investigated the effect of TRPA1 modulators on transforming growth factor beta 1(TGF-β1) -treated lung fibroblasts.

Methods: MRC-5 cells were preincubated with TGF-β1 for 24 h. TRPA1 agonist or antagonist were added and further incubated for 24 h. The changes in TRPA1 and alpha-smooth muscle actin (α-SMA) expressions by stimuli were evaluated using qRT-PCR, western blot and immunohistochemical analyses. Statistical significance was determined by using one- or two-way ANOVA, followed by Bonferroni's post hoc analysis for comparison of multiple groups and paired 2-tailed Student's t-test between 2 groups.

Results: MRC-5 cells treated by TGF-β1 significantly upregulated α-SMA mRNA expressions (P < 0.01), but downregulated TRPA1 gene expression (P < 0.001). Post-treatment of TRPA1 activator, allyl isothiocyanate (AITC), after TGF-β1 significantly downregulated the α-SMA gene induction (P < 0.01 at 24 h), protein expression (P < 0.05) and immunoreactivity with stress fibers (P < 0.05). On the other hand, TRPA1 antagonist HC-030031 did not prevent this effect, and instead tended to facilitate the suppressive effect of AITC when co-stimulated. AITC significantly increased phosphorylated- extracellular signal-regulated kinase (ERK) 1/2 and heme oxygenase (HO)-1 protein expressions (P < 0.05) in TGF-β1-treated cells. Combined inhibition with ERK1/2 mitogen-activated protein kinase (MAPK) and nuclear factor erythroid 2-related factor (NRF2) almost completely reversed AITC-induced α-SMA suppression (P < 0.05). Dexamethasone was not able to inhibit the upregulated α-SMA induction by TGF-β1. However, AITC improved dexamethasone-insensitive myodifferentiation in the presence of the corticosteroid (P < 0.01).

Conclusion: We found that AITC exerts protective effect on TGF-β1-induced α-SMA induction by activating ERK1/2 MAPK and NRF2/HO-1 pathways in lung fibroblasts. It also overcomes corticosteroids insensitivity in TGF-β1-induced α-SMA induction. TRPA1 antagonist modulates the suppressive effect, but not prevent it. AITC and TRPA1 antagonist may be therapeutic agents in treating chronic respiratory diseases.

Keywords: AITC; ERK1/2 MAPK pathway; NRF2/HO-1 pathway; TRPA1.

MeSH terms

  • Adrenal Cortex Hormones / toxicity*
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Heme Oxygenase-1 / metabolism*
  • Humans
  • Isothiocyanates / pharmacology*
  • Lung / drug effects
  • Lung / metabolism*
  • Mitogen-Activated Protein Kinase Kinases / metabolism*
  • Myofibroblasts / drug effects
  • Myofibroblasts / metabolism
  • NF-E2-Related Factor 2 / metabolism*
  • TRPA1 Cation Channel / antagonists & inhibitors
  • TRPA1 Cation Channel / metabolism*
  • Transforming Growth Factor beta1 / toxicity

Substances

  • Adrenal Cortex Hormones
  • Isothiocyanates
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • TGFB1 protein, human
  • TRPA1 Cation Channel
  • TRPA1 protein, human
  • Transforming Growth Factor beta1
  • allyl isothiocyanate
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • Mitogen-Activated Protein Kinase Kinases

Grants and funding