FBXO7 Confers Mesenchymal Properties and Chemoresistance in Glioblastoma by Controlling Rbfox2-Mediated Alternative Splicing

Adv Sci (Weinh). 2023 Nov;10(33):e2303561. doi: 10.1002/advs.202303561. Epub 2023 Oct 11.

Abstract

Mesenchymal glioblastoma (GBM) is highly resistant to radio-and chemotherapy and correlates with worse survival outcomes in GBM patients; however, the underlying mechanism determining the mesenchymal phenotype remains largely unclear. Herein, it is revealed that FBXO7, a substrate-recognition component of the SCF complex implicated in the pathogenesis of Parkinson's disease, confers mesenchymal properties and chemoresistance in GBM by controlling Rbfox2-mediated alternative splicing. Specifically, FBXO7 ubiquitinates Rbfox2 Lys249 through K63-linked ubiquitin chains upon arginine dimethylation at Arg341 and Arg441 by PRMT5, leading to Rbfox2 stabilization. FBXO7 controls Rbfox2-mediated splicing of mesenchymal genes, including FoxM1, Mta1, and Postn. FBXO7-induced exon Va inclusion of FoxM1 promotes FoxM1 phosphorylation by MEK1 and nuclear translocation, thereby upregulates CD44, CD9, and ID1 levels, resulting in GBM stem cell self-renewal and mesenchymal transformation. Moreover, FBXO7 is stabilized by temozolomide, and FBXO7 depletion sensitizes tumor xenografts in mice to chemotherapy. The findings demonstrate that the FBXO7-Rbfox2 axis-mediated splicing contributes to mesenchymal transformation and tumorigenesis, and targeting FBXO7 represents a potential strategy for GBM treatment.

Keywords: FBXO7; alternative splicing; chemoresistance; glioblastoma; mesenchymal transformation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alternative Splicing / genetics
  • Animals
  • Drug Resistance, Neoplasm / genetics
  • F-Box Proteins* / genetics
  • F-Box Proteins* / metabolism
  • Glioblastoma* / drug therapy
  • Glioblastoma* / genetics
  • Humans
  • Mice
  • Protein-Arginine N-Methyltransferases / genetics
  • RNA Splicing
  • RNA Splicing Factors / genetics
  • Repressor Proteins / genetics
  • Trans-Activators / genetics

Substances

  • F-Box Proteins
  • FBXO7 protein, human
  • PRMT5 protein, human
  • Protein-Arginine N-Methyltransferases
  • Repressor Proteins
  • RNA Splicing Factors
  • Trans-Activators
  • RBFOX2 protein, human