GADD45a promoter regulation by a functional genetic variant associated with acute lung injury

PLoS One. 2014 Jun 18;9(6):e100169. doi: 10.1371/journal.pone.0100169. eCollection 2014.

Abstract

Rationale: Growth arrest DNA damage inducible alpha (GADD45a) is a stress-induced gene we have shown to participate in the pathophysiology of ventilator-induced lung injury (VILI) via regulation of mechanical stress-induced Akt ubiquitination and phosphorylation. The regulation of GADD45a expression by mechanical stress and its relationship with acute lung injury (ALI) susceptibility and severity, however, remains unknown.

Objectives: We examined mechanical stress-dependent regulatory elements (MSRE) in the GADD45a promoter and the contribution of promoter polymorphisms in GADD45a expression and ALI susceptibility.

Methods and results: Initial studies in GADD45a knockout and heterozygous mice confirmed the relationship of GADD45a gene dose to VILI severity. Human lung endothelial cells (EC) transfected with a luciferase vector containing the full length GADD45a promoter sequence (-771 to +223) demonstrated a >4 fold increase in GADD45a expression in response to 18% cyclic stretch (CS, 4 h) compared to static controls while specific promoter regions harboring CS-dependent MSRE were identified using vectors containing serial deletion constructs of the GADD45a promoter. In silico analyses of GADD45a promoter region (-371 to -133) revealed a potential binding site for specificity protein 1 (SP1), a finding supported by confirmed SP1 binding with the GADD45a promoter and by the significant attenuation of CS-dependent GADD45a promoter activity in response to SP1 silencing. Separately, case-control association studies revealed a significant association of a GADD45a promoter SNP at -589 (rs581000, G>C) with reduced ALI susceptibility. Subsequently, we found allelic variation of this SNP is associated with both differential GADD45a expression in mechanically stressed EC (18% CS, 4 h) and differential binding site of interferon regulatory factor 7 (IRF7) at this site.

Conclusion: These results strongly support a functional role for GADD45a in ALI/VILI and identify a specific gene variant that confers risk for ALI.

MeSH terms

  • Acute Lung Injury / genetics*
  • Acute Lung Injury / metabolism
  • Acute Lung Injury / pathology
  • Adult
  • Aged
  • Animals
  • Binding Sites
  • Cell Cycle Proteins / genetics*
  • Cell Cycle Proteins / metabolism
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Female
  • Gene Dosage
  • Gene Expression Regulation
  • Genes, Reporter
  • Heterozygote
  • Humans
  • Interferon Regulatory Factor-7 / genetics
  • Interferon Regulatory Factor-7 / metabolism
  • Luciferases / genetics
  • Luciferases / metabolism
  • Lung / metabolism
  • Lung / pathology
  • Male
  • Mechanotransduction, Cellular
  • Mice
  • Mice, Knockout
  • Middle Aged
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Polymorphism, Single Nucleotide
  • Promoter Regions, Genetic*
  • Protein Binding
  • Sp1 Transcription Factor / genetics
  • Sp1 Transcription Factor / metabolism
  • Stress, Mechanical
  • Ventilator-Induced Lung Injury / genetics*
  • Ventilator-Induced Lung Injury / metabolism
  • Ventilator-Induced Lung Injury / pathology

Substances

  • Cell Cycle Proteins
  • GADD45A protein, human
  • Gadd45a protein, mouse
  • Interferon Regulatory Factor-7
  • Irf7 protein, mouse
  • Nuclear Proteins
  • Sp1 Transcription Factor
  • Luciferases