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Modulating BAP1 expression affects ROS homeostasis, cell motility and mitochondrial function.

Lucie Hebert1, Dorine Bellanger1, Chloé Guillas1

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Summary

The BAP1 tumor suppressor protein stabilizes other proteins via its deubiquitinase activity, impacting cytoskeleton, mitochondria, and ROS levels. This proteomic approach reveals novel BAP1 functions in cancer.

Keywords:
BAP1de-ubiquitinationprotein stabilityproteomicstumor suppressor

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Area of Science:

  • Biochemistry
  • Molecular Biology
  • Cancer Research

Background:

  • The BAP1 (BRCA1-associated protein 1) gene product is a key component of the PR-DUB complex, involved in histone modification and protein deubiquitination.
  • Despite its role in a Polycomb complex, transcriptional changes are not consistently observed in BAP1-inactivated tumors, suggesting alternative mechanisms of tumor suppression.
  • BAP1's tumor suppressor activity may involve protein stabilization through its deubiquitinase function, independent of canonical transcriptional regulation.

Purpose of the Study:

  • To investigate the functional consequences of BAP1 inactivation and its deubiquitinase activity on cellular proteomes and pathways.
  • To explore the hypothesis that BAP1 stabilizes proteins, thereby exerting its tumor suppressor functions.
  • To identify novel cellular and tumorigenic roles of BAP1 and validate proteomic analysis as a readout for BAP1 inactivation.

Main Methods:

  • Quantitative mass spectrometry was employed to analyze protein expression changes.
  • Gene expression arrays were used to assess transcriptomic alterations.
  • Functional assays were performed in mesothelioma cell lines with varying BAP1 expression (inactivated, wild-type, catalytically dead).

Main Results:

  • Proteomic analysis revealed significant alterations in cytoskeleton organization, mitochondrial activity, and reactive oxygen species (ROS) management upon BAP1 modulation.
  • Gene expression profiling indicated enrichment in the epithelial-to-mesenchymal transition (EMT) pathway.
  • Functional studies confirmed that BAP1's deubiquitinase activity is essential for maintaining these cellular phenotypes, and ROS modulation partially restored cellular functions.

Conclusions:

  • BAP1 plays a crucial role in regulating cellular morphology, mitochondrial function, and ROS homeostasis, likely through its protein stabilization activity.
  • BAP1's deubiquitinase activity is mandatory for maintaining these cellular phenotypes, highlighting a non-transcriptional mechanism of tumor suppression.
  • Proteomic profiling offers a valuable approach to understanding the impact of BAP1 inactivation in cancer and identifying novel therapeutic targets.