Aberrant splicing in neuroblastoma generates RNA-fusion transcripts and provides vulnerability to spliceosome inhibitors

Nucleic Acids Res. 2021 Mar 18;49(5):2509-2521. doi: 10.1093/nar/gkab054.

Abstract

The paucity of recurrent mutations has hampered efforts to understand and treat neuroblastoma. Alternative splicing and splicing-dependent RNA-fusions represent mechanisms able to increase the gene product repertoire but their role in neuroblastoma remains largely unexplored. Here we investigate the presence and possible roles of aberrant splicing and splicing-dependent RNA-fusion transcripts in neuroblastoma. In addition, we attend to establish whether the spliceosome can be targeted to treat neuroblastoma. Through analysis of RNA-sequenced neuroblastoma we show that elevated expression of splicing factors is a strong predictor of poor clinical outcome. Furthermore, we identified >900 primarily intrachromosomal fusions containing canonical splicing sites. Fusions included transcripts from well-known oncogenes, were enriched for proximal genes and in chromosomal regions commonly gained or lost in neuroblastoma. As a proof-of-principle that these fusions can generate altered gene products, we characterized a ZNF451-BAG2 fusion, producing a truncated BAG2-protein which inhibited retinoic acid induced differentiation. Spliceosome inhibition impeded neuroblastoma fusion expression, induced apoptosis and inhibited xenograft tumor growth. Our findings elucidate a splicing-dependent mechanism generating altered gene products in neuroblastoma and show that the spliceosome is a potential target for clinical intervention.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aminoacyltransferases / metabolism
  • Animals
  • Apoptosis
  • Cell Differentiation
  • Cell Line, Tumor
  • Female
  • Gene Fusion
  • HSC70 Heat-Shock Proteins / metabolism
  • Humans
  • Mice
  • Mice, Nude
  • Molecular Chaperones / genetics*
  • Molecular Chaperones / metabolism
  • Mutant Chimeric Proteins / genetics*
  • Mutant Chimeric Proteins / metabolism
  • Neuroblastoma / genetics*
  • Neuroblastoma / metabolism
  • Neuroblastoma / pathology
  • RNA Splicing Factors / genetics
  • RNA Splicing Factors / metabolism
  • RNA Splicing*
  • Sequence Deletion
  • Spliceosomes / drug effects*
  • Transcription Factors / metabolism
  • tau Proteins / metabolism

Substances

  • BAG2 protein, human
  • HSC70 Heat-Shock Proteins
  • MAPT protein, human
  • Molecular Chaperones
  • Mutant Chimeric Proteins
  • RNA Splicing Factors
  • Transcription Factors
  • tau Proteins
  • Aminoacyltransferases
  • ZNF451 protein, human