Folliculin haploinsufficiency causes cellular dysfunction of pleural mesothelial cells

Sci Rep. 2021 May 24;11(1):10814. doi: 10.1038/s41598-021-90184-9.

Abstract

Birt-Hogg-Dubé syndrome (BHDS), an autosomal dominant inheritance disease caused by folliculin (FLCN) mutations, is associated with lung cysts and spontaneous pneumothorax. The possibility of FLCN haploinsufficiency in pleural mesothelial cells (PMCs) contributing to development of pneumothorax has not yet been clarified. Electron microscopy revealed exposed intercellular boundaries between PMCs on visceral pleura and decreased electron density around the adherens junctions in BHDS. To characterize cellular function of PMCs in BHDS patients (BHDS-PMCs), during surgery for pneumothorax, we established the flow cytometry-based methods of isolating high-purity PMCs from pleural lavage fluid. BHDS-PMCs showed impaired cell attachment and a significant decrease in proliferation and migration, but a significant increase in apoptosis compared with PMCs from primary spontaneous pneumothorax (PSP) patients (PSP-PMCs). Microarray analysis using isolated PMCs revealed a significant alteration in the expression of genes belonging to Gene Ontology terms "cell-cell adhesion junction" and "cell adhesion molecule binding". Gene set enrichment analysis demonstrated that CDH1, encoding E-cadherin, was identified in the down-regulated leading edge of a plot in BHDS-PMCs. AMPK and LKB1 activation were significantly impaired in BHDS-PMCs compared with PSP-PMCs. Our findings indicate that FLCN haploinsufficiency may affect the E-cadherin-LKB1-AMPK axis and lead to abnormal cellular function in BHDS-PMCs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Apoptosis
  • Birt-Hogg-Dube Syndrome / genetics
  • Birt-Hogg-Dube Syndrome / pathology*
  • Bronchoalveolar Lavage Fluid / cytology*
  • Cell Movement
  • Cell Proliferation
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Haploinsufficiency*
  • Humans
  • Male
  • Microscopy, Electron
  • Middle Aged
  • Oligonucleotide Array Sequence Analysis
  • Pleura / cytology*
  • Pleura / pathology
  • Primary Cell Culture
  • Proto-Oncogene Proteins / genetics*
  • Tumor Suppressor Proteins / genetics*
  • Young Adult

Substances

  • FLCN protein, human
  • Proto-Oncogene Proteins
  • Tumor Suppressor Proteins