Trichostatin A attenuates ventilation-augmented epithelial-mesenchymal transition in mice with bleomycin-induced acute lung injury by suppressing the Akt pathway

PLoS One. 2017 Feb 24;12(2):e0172571. doi: 10.1371/journal.pone.0172571. eCollection 2017.

Abstract

Background: Mechanical ventilation (MV) used in patients with acute respiratory distress syndrome (ARDS) can cause diffuse lung inflammation, an effect termed ventilator-induced lung injury, which may produce profound pulmonary fibrogenesis. Histone deacetylases (HDACs) and serine/threonine kinase/protein kinase B (Akt) are crucial in modulating the epithelial-mesenchymal transition (EMT) during the reparative phase of ARDS; however, the mechanisms regulating the interactions among MV, EMT, HDACs, and Akt remain unclear. We hypothesized that trichostatin A (TSA), a HDAC inhibitor, can reduce MV-augmented bleomycin-induced EMT by inhibiting the HDAC4 and Akt pathways.

Methods: Five days after bleomycin treatment to mimic acute lung injury (ALI), wild-type or Akt-deficient C57BL/6 mice were exposed to low-tidal-volume (low-VT, 6 mL/kg) or high-VT (30 mL/kg) MV with room air for 5 h after receiving 2 mg/kg TSA. Nonventilated mice were examined as controls.

Results: Following bleomycin exposure in wild-type mice, high-VT MV induced substantial increases in microvascular leaks; matrix metalloproteinase-9 (MMP-9) and plasminogen activator inhibitor-1 proteins; free radical production; Masson's trichrome staining; fibronectin, MMP-9, and collagen 1a1 gene expression; EMT (identified by increased localized staining of α-smooth muscle actin and decreased staining of E-cadherin); total HDAC activity; and HDAC4 and Akt activation (P < 0.05). In Akt-deficient mice, the MV-augmented lung inflammation, profibrotic mediators, EMT profiles, Akt activation, and pathological fibrotic scores were reduced and pharmacologic inhibition of HDAC4 expression was triggered by TSA (P < 0.05).

Conclusions: Our data indicate that TSA treatment attenuates high-VT MV-augmented EMT after bleomycin-induced ALI, in part by inhibiting the HDAC4 and Akt pathways.

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Acute Lung Injury / chemically induced
  • Acute Lung Injury / genetics
  • Acute Lung Injury / pathology
  • Acute Lung Injury / prevention & control*
  • Animals
  • Bleomycin
  • Cadherins / genetics
  • Cadherins / metabolism
  • Collagen Type I / genetics
  • Collagen Type I / metabolism
  • Epithelial-Mesenchymal Transition / drug effects*
  • Free Radicals / antagonists & inhibitors
  • Free Radicals / metabolism
  • Gene Expression Regulation
  • Histone Deacetylase Inhibitors / pharmacology*
  • Histone Deacetylases / genetics*
  • Histone Deacetylases / metabolism
  • Humans
  • Hydroxamic Acids / pharmacology*
  • Matrix Metalloproteinase 9 / genetics
  • Matrix Metalloproteinase 9 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / genetics*
  • Proto-Oncogene Proteins c-akt / metabolism
  • Respiration, Artificial / adverse effects
  • Serpin E2 / genetics
  • Serpin E2 / metabolism
  • Signal Transduction
  • Tidal Volume
  • Ventilator-Induced Lung Injury / etiology
  • Ventilator-Induced Lung Injury / genetics
  • Ventilator-Induced Lung Injury / metabolism
  • Ventilator-Induced Lung Injury / prevention & control*

Substances

  • Actins
  • Cadherins
  • Cdh1 protein, mouse
  • Collagen Type I
  • Free Radicals
  • Histone Deacetylase Inhibitors
  • Hydroxamic Acids
  • Serpin E2
  • Serpine2 protein, mouse
  • alpha-smooth muscle actin, mouse
  • Bleomycin
  • trichostatin A
  • Proto-Oncogene Proteins c-akt
  • Matrix Metalloproteinase 9
  • Mmp9 protein, mouse
  • Hdac5 protein, mouse
  • Histone Deacetylases

Grants and funding

This research was supported by the Ministry of Science and Technology (https://www.most.gov.tw) (105-2314-B-182A-091-MY2; to LFL) and Chang Gung Medical Research Project (https://www.cgmh.org.tw) (CMRPG3E1712; to CSL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.