The powerful tumor suppressor activity of BRCA1-associated protein 1
(BAP1) and its ability to regulate gene x environment interactions (GxE) in
carcinogenesis are related to its dual role in the nucleus, where BAP1
contributes to DNA repair by modulating homologous recombination (HR), and in
the cytoplasm where BAP1 regulates cell death and mitochondrial
respiration30. In the
cytoplasm, BAP1 localizes at the endoplasmic reticulum (ER) where it binds,
deubiquitylates (following F-box and leucine-rich repeat protein 2 (FBXL2)
ubiquitylation), and stabilizes type 3 inositol-1,4,5-trisphosphate receptor
(IP3R3), modulating calcium ion (Ca2+) release from
the ER into the cytosol and mitochondria, and thus promoting apoptosis30. In primary cells exposed to
either asbestos, ionizing radiation (IR) or ultraviolet (UV) radiation, reduced
levels of nuclear BAP1 impair DNA repair. At the same time, reduced cytoplasmic
BAP1 levels impair apoptosis, increasing the fraction of cells that survive DNA
damage and that over time may become malignant30. In addition, mitochondria need
Ca2+ for aerobic oxidative phosphorylation (OXPHOS). In response
to tumor hypoxia, cancer cells need to adjust their metabolism from aerobic
(blue) to glycolytic (red) in order to sustain growth and survival. Primary
cells from BAP1+/− individuals have reduced
mitochondrial OXPHOS and increased aerobic glycolysis and lactate production,
even in the presence of oxygen, a phenomenon known as the ‘Warburg
effect’56.
Therefore, the ‘Warburg effect’ in addition to being a hallmark of
cancer cells is also found in normal cells from BAP1-mutant
carriers, and contributes to the adaptation to metabolic stress during
tumorigenesis56.
BAP1+/+, cells with BAP1
wild-type; BAP1+/−, cells with heterozygous
BAP1 mutations, containing about 50% of BAP1 protein levels
compared to wild-type cells30.
[Ca2+]m, mitochondrial calcium; MCU, mitochondrial
calcium uniporter; Re-O2 reoxygenation; TCA, tricarboxylic acid; Ub,
ubiquitin; VDAC, voltage-dependent anion channel.