RPL22 is a tumor suppressor in MSI-high cancers and a splicing regulator of MDM4

Cell Rep. 2024 Aug 27;43(8):114622. doi: 10.1016/j.celrep.2024.114622. Epub 2024 Aug 14.

Abstract

Microsatellite instability-high (MSI-H) tumors are malignant tumors that, despite harboring a high mutational burden, often have intact TP53. One of the most frequent mutations in MSI-H tumors is a frameshift mutation in RPL22, a ribosomal protein. Here, we identified RPL22 as a modulator of MDM4 splicing through an alternative splicing switch in exon 6. RPL22 loss increases MDM4 exon 6 inclusion and cell proliferation and augments resistance to the MDM inhibitor Nutlin-3a. RPL22 represses the expression of its paralog, RPL22L1, by mediating the splicing of a cryptic exon corresponding to a truncated transcript. Therefore, damaging mutations in RPL22 drive oncogenic MDM4 induction and reveal a common splicing circuit in MSI-H tumors that may inform therapeutic targeting of the MDM4-p53 axis and oncogenic RPL22L1 induction.

Keywords: CP: Cancer; CP: Molecular biology; MDM4; MDM4 exon 6 inclusion; MSI-H; RPL22; RPL22 p.K15fs; alternative splicing; microsattelite instability-high; p53; ribosomal proteins; tumor suppressor.

MeSH terms

  • Alternative Splicing / genetics
  • Animals
  • Cell Cycle Proteins* / genetics
  • Cell Cycle Proteins* / metabolism
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Exons / genetics
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Imidazoles / pharmacology
  • Mice
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Piperazines / pharmacology
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Ribosomal Proteins* / genetics
  • Ribosomal Proteins* / metabolism
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Ribosomal Proteins
  • MDM4 protein, human
  • Cell Cycle Proteins
  • Proto-Oncogene Proteins
  • Tumor Suppressor Protein p53
  • Nuclear Proteins
  • Piperazines
  • Imidazoles