Transcriptional and epigenetic modulation of human rhinovirus-induced CXCL10 production by cigarette smoke

Am J Respir Cell Mol Biol. 2014 Mar;50(3):571-82. doi: 10.1165/rcmb.2013-0129OC.

Abstract

Human rhinovirus (HRV) triggers exacerbations of asthma and chronic obstructive pulmonary disease. Cigarette smoking is the primary risk factor for the development of chronic obstructive pulmonary disease, and 25% of individuals with asthma smoke. Smokers experience both longer and more severe colds. We previously showed that cigarette smoke extract (CSE) inhibited HRV-induced expression of a range of epithelial antiviral molecules. Here, we use CXCL10 as a model antiviral gene to examine the mechanisms by which CSE inhibits epithelial antiviral immunity. HRV-induced CXCL10 transcription depends on activation of NF-ĸB and IFN-regulatory factor-1 (IRF-1), and we now also implicate two signal transducer and activator of transcription (STAT) consensus sequences in the CXCL10 promoter in HRV-induced CXCL10 expression. CSE inhibited HRV-induced activation and nuclear translocation/binding of both NF-ĸB, and IRF-1 to their respective recognition sequences in the CXCL10 promoter. HRV also induced formation of complexes at the STAT region in the CXCL10 promoter, and HRV-induced activation of STAT-1 was inhibited by CSE. In addition, CSE inhibited HRV-induced chromatin accessibility around the transcriptional start site of the CXCL10 promoter. Although CSE inhibited HRV-induced expression of both the viral double-stranded RNA sensors, retinoic acid-inducible gene-I and melanoma differentiation-associated gene (MDA) 5, only specific short interfering RNA (siRNA) to MDA5, but not nontargeting siRNA, or siRNA to retinoic acid-inducible gene-I, inhibited HRV-induced CXCL10 induction. We conclude that CSE reduces chromatin accessibility and inhibits viral signaling via NF-ĸB, IRF-1, STAT-1, and MDA5. Thus, we show that CSE can simultaneously modulate multiple pathways linked to innate immune responses to HRV infection.

MeSH terms

  • Binding Sites
  • Cell Line
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL10 / metabolism*
  • Chromatin Assembly and Disassembly / drug effects
  • DEAD-box RNA Helicases / metabolism
  • Epigenesis, Genetic / drug effects*
  • Epithelial Cells / drug effects*
  • Epithelial Cells / immunology
  • Epithelial Cells / virology
  • Humans
  • Immunity, Innate / drug effects
  • Interferon Regulatory Factor-1 / metabolism
  • Interferon-Induced Helicase, IFIH1
  • Lung / drug effects*
  • Lung / immunology
  • Lung / virology
  • NF-kappa B / metabolism
  • Promoter Regions, Genetic
  • Rhinovirus / immunology
  • Rhinovirus / metabolism
  • Rhinovirus / pathogenicity*
  • STAT1 Transcription Factor / metabolism
  • Signal Transduction / drug effects
  • Smoke / adverse effects*
  • Smoking / adverse effects*
  • Transcription, Genetic / drug effects*
  • Transfection
  • Up-Regulation

Substances

  • CXCL10 protein, human
  • Chemokine CXCL10
  • IRF1 protein, human
  • Interferon Regulatory Factor-1
  • NF-kappa B
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • Smoke
  • IFIH1 protein, human
  • DEAD-box RNA Helicases
  • Interferon-Induced Helicase, IFIH1