MBD5 and MBD6 stabilize the BAP1 complex and promote BAP1-dependent cancer

Genome Biol. 2022 Sep 30;23(1):206. doi: 10.1186/s13059-022-02776-x.

Abstract

Background: BRCA1-associated protein 1 (BAP1) is an ubiquitin carboxy-terminal hydrolase, which forms a multi-protein complex with different epigenetic factors, such as ASXL1-3 and FOXK1/2. At the chromatin level, BAP1 catalyzes the removal of mono-ubiquitination on histone H2AK119 in collaboration with other subunits within the complex and functions as a transcriptional activator in mammalian cells. However, the crosstalk between different subunits and how these subunits impact BAP1's function remains unclear.

Results: We report the identification of the methyl-CpG-binding domain proteins 5 and 6 (MBD5 and MBD6) that bind to the C-terminal PHD fingers of the large scaffold subunits ASXL1-3 and stabilize the BAP1 complex at the chromatin. We further identify a novel Drosophila protein, the six-banded (SBA), as an ortholog of human MBD5 and MBD6, and demonstrate that the core modules of the BAP1 complex is structurally and functionally conserved from Drosophila (Calypso/ASX/SBA) to human cells (BAP1/ASXL/MBD). Dysfunction of the BAP1 complex induced by the misregulation/mutations in its subunit(s) are frequent in many human cancers. In BAP1-dependent human cancers, such as small cell lung cancer (SCLC), MBD6 tends to be a part of the predominant complex formed. Therefore, depletion of MBD6 leads to a global loss of BAP1 occupancy at the chromatin, resulting in a reduction of BAP1-dependent gene expression and tumor growth in vitro and in vivo.

Conclusions: We characterize MBD5 and MBD6 as important regulators of the BAP1 complex and maintain its transcriptional landscape, shedding light on the therapeutic potential of targeting MBD5 and MBD6 in BAP1-dependent human cancers.

Keywords: MBD5; MBD6; PHD fingers; SCLC; The BAP1 complex.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Chromatin
  • DNA-Binding Proteins / metabolism
  • Drosophila / genetics
  • Drosophila Proteins* / genetics
  • Drosophila Proteins* / metabolism
  • Forkhead Transcription Factors / genetics
  • Histones / metabolism
  • Humans
  • Mammals / genetics
  • Neoplasms* / genetics
  • Repressor Proteins / genetics
  • Transcription Factors / metabolism
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism
  • Ubiquitin Thiolesterase / genetics
  • Ubiquitin Thiolesterase / metabolism

Substances

  • BAP1 protein, human
  • Chromatin
  • DNA-Binding Proteins
  • Drosophila Proteins
  • FOXK1 protein, human
  • Forkhead Transcription Factors
  • Histones
  • MBD5 protein, human
  • MBD6 protein, human
  • Repressor Proteins
  • Transcription Factors
  • Tumor Suppressor Proteins
  • Ubiquitin Thiolesterase