Sulforaphane enriched transcriptome of lung mitochondrial energy metabolism and provided pulmonary injury protection via Nrf2 in mice

Toxicol Appl Pharmacol. 2019 Feb 1:364:29-44. doi: 10.1016/j.taap.2018.12.004. Epub 2018 Dec 5.

Abstract

Nrf2 is essential to antioxidant response element (ARE)-mediated host defense. Sulforaphane (SFN) is a phytochemical antioxidant known to affect multiple cellular targets including Nrf2-ARE pathway in chemoprevention. However, the role of SFN in non-malignant airway disorders remain unclear. To test if pre-activation of Nrf2-ARE signaling protects lungs from oxidant-induced acute injury, wild-type (Nrf2+/+) and Nrf2-deficient (Nrf2-/-) mice were given SFN orally or as standardized broccoli sprout extract diet (SBE) before hyperoxia or air exposure. Hyperoxia-induced pulmonary injury and oxidation indices were significantly reduced by SFN or SBE in Nrf2+/+ mice but not in Nrf2-/- mice. SFN upregulated a large cluster of basal lung genes that are involved in mitochondrial oxidative phosphorylation, energy metabolism, and cardiovascular protection only in Nrf2+/+ mice. Bioinformatic analysis elucidated ARE-like motifs on these genes. Transcript abundance of the mitochondrial machinery genes remained significantly higher after hyperoxia exposure in SFN-treated Nrf2+/+ mice than in SFN-treated Nrf2-/- mice. Nuclear factor-κB was suggested to be a central molecule in transcriptome networks affected by SFN. Minor improvement of hyperoxia-caused lung histopathology and neutrophilia by SFN in Nrf2-/- mice implies Nrf2-independent or alternate effector mechanisms. In conclusion, SFN is suggested to be as a preventive intervention in a preclinical model of acute lung injury by linking mitochondria and Nrf2. Administration of SFN alleviated acute lung injury-like pathogenesis in a Nrf2-dependent manner. Potential AREs in the SFN-inducible transcriptome for mitochondria bioenergetics provided a new insight into the downstream mechanisms of Nrf2-mediated pulmonary protection.

Keywords: Antioxidant response element; Broccoli; Hyperoxia; Lung; Microarray.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Acute Lung Injury / etiology
  • Acute Lung Injury / genetics
  • Acute Lung Injury / metabolism
  • Acute Lung Injury / prevention & control*
  • Animals
  • Antioxidant Response Elements
  • Antioxidants / pharmacology*
  • DNA, Mitochondrial / genetics
  • DNA, Mitochondrial / metabolism
  • Disease Models, Animal
  • Energy Metabolism / drug effects*
  • Energy Metabolism / genetics
  • Gene Expression Profiling / methods
  • Glutathione Peroxidase / genetics
  • Glutathione Peroxidase / metabolism
  • Hyperoxia / complications
  • Isothiocyanates / pharmacology*
  • Lung / drug effects*
  • Lung / metabolism
  • Lung / pathology
  • Male
  • Mice, Inbred C57BL
  • Mice, Inbred ICR
  • Mice, Knockout
  • Mitochondria / drug effects*
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • NAD(P)H Dehydrogenase (Quinone) / genetics
  • NAD(P)H Dehydrogenase (Quinone) / metabolism
  • NF-E2-Related Factor 2 / deficiency
  • NF-E2-Related Factor 2 / genetics
  • NF-E2-Related Factor 2 / metabolism*
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • Oligonucleotide Array Sequence Analysis
  • Signal Transduction / drug effects
  • Sulfoxides
  • Transcriptome*

Substances

  • Antioxidants
  • DNA, Mitochondrial
  • Isothiocyanates
  • NF-E2-Related Factor 2
  • NF-kappa B
  • Nfe2l2 protein, mouse
  • Sulfoxides
  • Gpx2 protein, mouse
  • Glutathione Peroxidase
  • NAD(P)H Dehydrogenase (Quinone)
  • Nqo1 protein, mouse
  • sulforaphane