The SS18-SSX Oncoprotein Hijacks KDM2B-PRC1.1 to Drive Synovial Sarcoma

Cancer Cell. 2018 Mar 12;33(3):527-541.e8. doi: 10.1016/j.ccell.2018.01.018. Epub 2018 Mar 1.

Abstract

Synovial sarcoma is an aggressive cancer invariably associated with a chromosomal translocation involving genes encoding the SWI-SNF complex component SS18 and an SSX (SSX1 or SSX2) transcriptional repressor. Using functional genomics, we identify KDM2B, a histone demethylase and component of a non-canonical polycomb repressive complex 1 (PRC1.1), as selectively required for sustaining synovial sarcoma cell transformation. SS18-SSX1 physically interacts with PRC1.1 and co-associates with SWI/SNF and KDM2B complexes on unmethylated CpG islands. Via KDM2B, SS18-SSX1 binds and aberrantly activates expression of developmentally regulated genes otherwise targets of polycomb-mediated repression, which is restored upon KDM2B depletion, leading to irreversible mesenchymal differentiation. Thus, SS18-SSX1 deregulates developmental programs to drive transformation by hijacking a transcriptional repressive complex to aberrantly activate gene expression.

Keywords: CRISPR/Cas9-mediated endogenous protein tagging; DNA methylation; SWI/SNF; epigenetics; non-canonical polycomb repressive complex; oncogenic gene fusion; sarcoma.

Publication types

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

MeSH terms

  • Cell Nucleus / metabolism
  • Cell Transformation, Neoplastic / genetics
  • F-Box Proteins / metabolism*
  • Gene Expression / physiology
  • Humans
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism*
  • Oncogene Proteins, Fusion / genetics
  • Polycomb Repressive Complex 1 / metabolism*
  • Proto-Oncogene Proteins / metabolism*
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Sarcoma, Synovial / genetics
  • Sarcoma, Synovial / metabolism*

Substances

  • F-Box Proteins
  • Neoplasm Proteins
  • Oncogene Proteins, Fusion
  • Proto-Oncogene Proteins
  • Repressor Proteins
  • SS18 protein, human
  • synovial sarcoma X breakpoint proteins
  • Jumonji Domain-Containing Histone Demethylases
  • KDM2A protein, human
  • Polycomb Repressive Complex 1