The effect of smoking on the transcriptional regulation of lung inflammation in patients with chronic obstructive pulmonary disease

Am J Respir Crit Care Med. 2006 Jul 1;174(1):41-50. doi: 10.1164/rccm.200505-725OC. Epub 2006 Mar 30.

Abstract

Rationale: Chronic obstructive pulmonary disease (COPD) is believed to result from an abnormal inflammatory response in the lungs to noxious particles and gases usually found in cigarette smoke.

Objectives: In this study, the molecular mechanisms for the enhanced proinflammatory cytokine gene transcription in COPD were investigated.

Methods: Lung tissue was examined from 56 subjects undergoing resection for peripheral lung tumors as follows: current smokers with (n = 14) and without COPD (n = 17), ex-smokers with COPD (n = 13), and nonsmokers (n = 12). The levels of inhibitor kappaB-alpha (IkappaB-alpha), histone deacetylase 2 (HDAC2), acetylated (ac-) histone H3 and H4, the transcription factor nuclear factor-kappaB (NF-kappaB), proinflammatory cytokine messenger RNA, and 8-isoprostane were measured.

Measurements and main results: IkappaB-alpha levels were significantly decreased in healthy smokers and current and ex-smoking patients with COPD when compared with nonsmokers (p < 0.001), with an associated increase in NF-kappaB DNA binding in current smokers (p < 0.05). An increase in acetylated histone 4 (ac-H4; p < 0.01) was found in current smokers. Conversely, ex-smokers with COPD showed an increase in ac-H3 (p < 0.05). Decreased levels of cytoplasmic, but not nuclear, HDAC2 protein levels were detected. From the cytokine profiles, no significant differences were detected; however, interleukin-12p40 expression correlated with ac-H4 in current smokers with COPD (p < 0.01).

Conclusion: These data propose a role for modification of nucleosomal structure in inflammatory cytokine gene transcription in response to smoking. The imbalance between histone deacetylation and acetylation in favor of acetylation may contribute to the enhanced inflammation in smokers susceptible to the development of COPD.

MeSH terms

  • Aged
  • Case-Control Studies
  • Cytokines / genetics
  • Cytokines / metabolism
  • Dinoprost / analogs & derivatives
  • Dinoprost / metabolism
  • Female
  • Histone Deacetylase 2
  • Histone Deacetylases / metabolism*
  • Histones / metabolism
  • Humans
  • I-kappa B Proteins / metabolism*
  • Male
  • Middle Aged
  • NF-KappaB Inhibitor alpha
  • NF-kappa B / metabolism*
  • Pulmonary Disease, Chronic Obstructive / metabolism*
  • Pulmonary Disease, Chronic Obstructive / pathology
  • RNA, Messenger / metabolism
  • Repressor Proteins / metabolism*
  • Smoking / metabolism*
  • Smoking / pathology

Substances

  • Cytokines
  • Histones
  • I-kappa B Proteins
  • NF-kappa B
  • NFKBIA protein, human
  • RNA, Messenger
  • Repressor Proteins
  • NF-KappaB Inhibitor alpha
  • 8-epi-prostaglandin F2alpha
  • Dinoprost
  • Histone Deacetylase 2
  • Histone Deacetylases