Germline BARD1 variants predispose to mesothelioma by impairing DNA repair and calcium signaling

Proc Natl Acad Sci U S A. 2024 Jul 16;121(29):e2405231121. doi: 10.1073/pnas.2405231121. Epub 2024 Jul 11.

Abstract

We report that ~1.8% of all mesothelioma patients and 4.9% of those younger than 55, carry rare germline variants of the BRCA1 associated RING domain 1 (BARD1) gene that were predicted to be damaging by computational analyses. We conducted functional assays, essential for accurate interpretation of missense variants, in primary fibroblasts that we established in tissue culture from a patient carrying the heterozygous BARD1V523A mutation. We found that these cells had genomic instability, reduced DNA repair, and impaired apoptosis. Investigating the underlying signaling pathways, we found that BARD1 forms a trimeric protein complex with p53 and SERCA2 that regulates calcium signaling and apoptosis. We validated these findings in BARD1-silenced primary human mesothelial cells exposed to asbestos. Our study elucidated mechanisms of BARD1 activity and revealed that heterozygous germline BARD1 mutations favor the development of mesothelioma and increase the susceptibility to asbestos carcinogenesis. These mesotheliomas are significantly less aggressive compared to mesotheliomas in asbestos workers.

Keywords: cancer prevention; carcinogenesis; gene × environment; genetics; mesothelioma.

MeSH terms

  • Apoptosis / genetics
  • Asbestos / toxicity
  • Calcium Signaling* / genetics
  • DNA Repair* / genetics
  • Female
  • Fibroblasts / metabolism
  • Genetic Predisposition to Disease*
  • Genomic Instability
  • Germ-Line Mutation*
  • Humans
  • Male
  • Mesothelioma* / genetics
  • Middle Aged
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism
  • Tumor Suppressor Proteins* / genetics
  • Tumor Suppressor Proteins* / metabolism
  • Ubiquitin-Protein Ligases* / genetics
  • Ubiquitin-Protein Ligases* / metabolism

Substances

  • BARD1 protein, human
  • Tumor Suppressor Proteins
  • Ubiquitin-Protein Ligases
  • Tumor Suppressor Protein p53
  • Asbestos
  • TP53 protein, human