Targeted epigenetic silencing of UCHL1 expression suppresses collagen-1 production in human lung epithelial cells

Epigenetics. 2023 Dec;18(1):2175522. doi: 10.1080/15592294.2023.2175522. Epub 2023 Feb 22.

Abstract

Ubiquitin carboxyl-terminal hydrolase L1 (UCHL1) is highly expressed in smokers, but little is known about the molecular mechanism of UCHL1 in airway epithelium and its possible role in affecting extracellular matrix (ECM) remodelling in the underlying submucosa. Since cigarette smoking is a major cause of lung diseases, we studied its effect on UCHL1 expression and DNA methylation patterns in human bronchial epithelial cells, obtained after laser capture micro-dissection (LCM) or isolated from residual tracheal/main stem bronchial tissue. Targeted regulation of UCHL1 expression via CRISPR/dCas9 based-epigenetic editing was used to explore the function of UCHL1 in lung epithelium. Our results show that cigarette smoke extract (CSE) stimulated the expression of UCHL1 in vitro. The methylation status of the UCHL1 gene was negatively associated with UCHL1 transcription in LCM-obtained airway epithelium at specific sites. Treatment with a UCHL1 inhibitor showed that the TGF-β1-induced upregulation of the ECM gene COL1A1 can be prevented by the inhibition of UCHL1 activity in cell lines. Furthermore, upon downregulation of UCHL1 by epigenetic editing using CRISPR/dCas-EZH2, mRNA expression of COL1A1 and fibronectin was reduced. In conclusion, we confirmed higher UCHL1 expression in current smokers compared to non- and ex-smokers, and induced downregulation of UCHL1 by epigenetic editing. The subsequent repression of genes encoding ECM proteins suggest a role for UCHL1 as a therapeutic target in fibrosis-related disease.

Keywords: DNA methylation; UCHL1; epigenetic editing; extracellular matrix; smoking.

MeSH terms

  • Bronchi
  • Collagen / metabolism
  • DNA Methylation*
  • Epigenesis, Genetic*
  • Epithelial Cells
  • Humans
  • Ubiquitin Thiolesterase / genetics
  • Ubiquitin Thiolesterase / metabolism

Substances

  • Collagen
  • Ubiquitin Thiolesterase
  • UCHL1 protein, human
  • COL1A1 protein, human

Grants and funding

COST CM1406 (www.epichembio.eu) is acknowledged for supporting scientific networking events. The study is supported by grants from the Jan Kornelis de Cock Stichting and partly funded by H2020-MSCA-ITN-2014-ETN 642691 (www.Epipredict.euwww.Epipredict.eu(www.Epipredict.eu), the GINOP-2.3.2-15-2016-00001 grant, and by the Abel Tasman Talent Program at the University Medical Center Groningen, the Netherlands; European Cooperation in Science and Technology European Cooperation in Science and Technology [COST CM1406; Marie Sklodowska-CurieMarie Sklodowska-Curie [H2020-MSCA-ITN-2014-ETN 642691].