Pulmonary Neoplasms in Patients with Birt-Hogg-Dubé Syndrome: Histopathological Features and Genetic and Somatic Events

PLoS One. 2016 Mar 14;11(3):e0151476. doi: 10.1371/journal.pone.0151476. eCollection 2016.

Abstract

Birt-Hogg-Dubé syndrome (BHD) is an inherited disorder caused by genetic mutations in the folliculin (FLCN) gene. Individuals with BHD have multiple pulmonary cysts and are at a high risk for developing renal cell carcinomas (RCCs). Currently, little information is available about whether pulmonary cysts are absolutely benign or if the lungs are at an increased risk for developing neoplasms. Herein, we describe 14 pulmonary neoplastic lesions in 7 patients with BHD. All patients were confirmed to have germline FLCN mutations. Neoplasm histologies included adenocarcinoma in situ (n = 2), minimally invasive adenocarcinoma (n = 1), papillary adenocarcinoma (n = 1), micropapillary adenocarcinoma (n = 1), atypical adenomatous hyperplasia (n = 8), and micronodular pneumocyte hyperplasia (MPH)-like lesion (n = 1). Five of the six adenocarcinoma/MPH-like lesions (83.3%) demonstrated a loss of heterozygosity (LOH) of FLCN. All of these lesions lacked mutant alleles and preserved wild-type alleles. Three invasive adenocarcinomas possessed additional somatic events: 2 had a somatic mutation in the epidermal growth factor receptor gene (EGFR) and another had a somatic mutation in KRAS. Immunohistochemical analysis revealed that most of the lesions were immunostained for phospho-mammalian target of rapamycin (p-mTOR) and phospho-S6. Collective data indicated that pulmonary neoplasms of peripheral adenocarcinomatous lineage in BHD patients frequently exhibit LOH of FLCN with mTOR pathway signaling. Additional driver gene mutations were detected only in invasive cases, suggesting that FLCN LOH may be an underlying abnormality that cooperates with major driver gene mutations in the progression of pulmonary adenocarcinomas in BHD patients.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / complications
  • Adenocarcinoma / genetics
  • Adenocarcinoma / pathology
  • Adenocarcinoma of Lung
  • Aged
  • Alveolar Epithelial Cells / pathology
  • Base Sequence
  • Birt-Hogg-Dube Syndrome / complications
  • Birt-Hogg-Dube Syndrome / genetics*
  • Birt-Hogg-Dube Syndrome / pathology*
  • DNA Mutational Analysis
  • Female
  • Germ-Line Mutation / genetics
  • Humans
  • Lung Neoplasms / complications
  • Lung Neoplasms / genetics*
  • Lung Neoplasms / pathology*
  • Male
  • Middle Aged
  • Molecular Sequence Data
  • Phosphorylation
  • Signal Transduction / genetics
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • TOR Serine-Threonine Kinases

Grants and funding

This work is supported by JSPS KAKENHI Grant Number 26460422 (M.F.) and 15K08374 (Y. N.), Yokohama Foundation for Advancement of Medical Science (M.F.), Yokohama Academic Foundation (M.F.), Project Mirai Cancer Research Grants (M.F.), and the Mitsubishi Foundation (M.F.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.