Indoor radon exposure increases tumor mutation burden in never-smoker patients with lung adenocarcinoma

Lung Cancer. 2019 May:131:139-146. doi: 10.1016/j.lungcan.2019.04.002. Epub 2019 Apr 3.

Abstract

Objectives: Radon, a natural radiation, is the leading environmental cause of lung cancer in never-smokers. However, the radon exposure impact on the mutational landscape and tumor mutation burden (TMB) of lung cancer in never-smokers has not been explored. The aim of this study was to investigate the mutational landscape of lung adenocarcinoma in never-smokers who were exposed to various degrees of residential radon.

Materials and methods: To investigate the effect of indoor radon exposure, we estimated the cumulative exposure to indoor radon in each house of patients with lung cancer with a never-smoking history. Patients with at least 2 year-duration of residence before the diagnosis of lung adenocarcinoma were included. Patients were subgrouped based on the median radon exposure level (48 Bq/m3): radon-high vs. radon-low and targeted sequencing of tumor and matched blood were performed in all patients.

Results: Among 41 patients with lung adenocarcinoma, the TMB was significantly higher in the radon-high group than it was in the radon-low group (mean 4.94 vs. 2.6 mutations/Mb, P = 0.01). The recurrence rates between radon-high and radon-low group did not differ significantly. Mutational signatures of radon-high tumors showed features associated with inactivity of the base excision repair and DNA replication machineries. The analysis of tumor evolutionary trajectories also suggested a series of mutagenesis induced by radon exposure. In addition, radon-high tumors revealed a significant protein-protein interaction of genes involved in DNA damage and repair (P < 0.001).

Conclusions: Indoor radon exposure increased the TMB in never-smoker patients with lung adenocarcinoma and their mutational signature was associated with defective DNA mismatch repair.

Keywords: Mutation; Non-small-cell lung cancer; Radon.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma of Lung / genetics*
  • Adult
  • Aged
  • Air Pollutants, Radioactive / adverse effects*
  • Air Pollution, Indoor / adverse effects*
  • Carcinogenesis / genetics
  • DNA Repair / genetics
  • DNA Repair / radiation effects
  • Female
  • Humans
  • Lung Neoplasms / genetics*
  • Male
  • Middle Aged
  • Mutagenesis / radiation effects
  • Mutation / genetics*
  • Neoplasm Staging
  • Radiation Exposure / adverse effects*
  • Radon / adverse effects*
  • Transcriptome

Substances

  • Air Pollutants, Radioactive
  • Radon