Cigarette smoke exposure enhances transforming acidic coiled-coil-containing protein 2 turnover and thereby promotes emphysema

JCI Insight. 2020 Jan 30;5(2):e125895. doi: 10.1172/jci.insight.125895.

Abstract

Our integrative genomic and functional analysis identified transforming acidic coiled-coil-containing protein 2 (TACC2) as a chronic obstructive pulmonary disease (COPD) candidate gene. Here, we found that smokers with COPD exhibit a marked decrease in lung TACC2 protein levels relative to smokers without COPD. Single cell RNA sequencing reveals that TACC2 is expressed primarily in lung epithelial cells in normal human lungs. Furthermore, suppression of TACC2 expression impairs the efficiency of homologous recombination repair and augments spontaneous and cigarette smoke extract-induced (CSE-induced) DNA damage and cytotoxicity in immortalized human bronchial epithelial cells. By contrast, enforced expression of TACC2 attenuates the CSE effects. We also found that CSE enhances TACC2 degradation via the ubiquitin-proteasome system mediated by the ubiquitin E3 ligase subunit, F box L7. Furthermore, cellularly expressed TACC2 proteins harboring naturally occurring mutations exhibited altered protein lifespan coupled with modified DNA damage repair and cytotoxic responses. CS triggers emphysematous changes accompanied by accumulated DNA damage, apoptosis of alveolar epithelia, and lung inflammation in Tacc2-/- compared with Tacc2+/+ mice. Our results suggest that CS destabilizes TACC2 protein in lung epithelia by the ubiquitin proteasome system, leading to subsequent DNA damage, cytotoxicity, and emphysema.

Keywords: COPD; Cell Biology; DNA repair; Pulmonology.

MeSH terms

  • Aged
  • Animals
  • Apoptosis / drug effects
  • Carrier Proteins
  • Cell Line
  • DNA Damage / drug effects
  • DNA Repair
  • Emphysema
  • Epithelial Cells / metabolism
  • Female
  • Humans
  • Lung / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • Mutagenesis, Site-Directed
  • Nicotiana / adverse effects
  • Proteasome Endopeptidase Complex / metabolism
  • Pulmonary Emphysema / chemically induced*
  • Pulmonary Emphysema / genetics*
  • Smoke / adverse effects*
  • Smoking / adverse effects*
  • Transcriptome
  • Tumor Suppressor Proteins / drug effects*
  • Tumor Suppressor Proteins / genetics*
  • Tumor Suppressor Proteins / metabolism*
  • Ubiquitin / metabolism
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Carrier Proteins
  • Smoke
  • TACC2 protein, human
  • Tacc2 protein, mouse
  • Tumor Suppressor Proteins
  • Ubiquitin
  • Ubiquitin-Protein Ligases
  • Proteasome Endopeptidase Complex