SALL4 is a CRL3REN/KCTD11 substrate that drives Sonic Hedgehog-dependent medulloblastoma

Cell Death Differ. 2024 Feb;31(2):170-187. doi: 10.1038/s41418-023-01246-6. Epub 2023 Dec 7.

Abstract

The Sonic Hedgehog (SHH) pathway is crucial regulator of embryonic development and stemness. Its alteration leads to medulloblastoma (MB), the most common malignant pediatric brain tumor. The SHH-MB subgroup is the best genetically characterized, however the molecular mechanisms responsible for its pathogenesis are not fully understood and therapeutic benefits are still limited. Here, we show that the pro-oncogenic stemness regulator Spalt-like transcriptional factor 4 (SALL4) is re-expressed in mouse SHH-MB models, and its high levels correlate with worse overall survival in SHH-MB patients. Proteomic analysis revealed that SALL4 interacts with REN/KCTD11 (here REN), a substrate receptor subunit of the Cullin3-RING ubiquitin ligase complex (CRL3REN) and a tumor suppressor lost in ~30% of human SHH-MBs. We demonstrate that CRL3REN induces polyubiquitylation and degradation of wild type SALL4, but not of a SALL4 mutant lacking zinc finger cluster 1 domain (ΔZFC1). Interestingly, SALL4 binds GLI1 and cooperates with HDAC1 to potentiate GLI1 deacetylation and transcriptional activity. Notably, inhibition of SALL4 suppresses SHH-MB growth both in murine and patient-derived xenograft models. Our findings identify SALL4 as a CRL3REN substrate and a promising therapeutic target in SHH-dependent cancers.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Neoplasms*
  • Cell Cycle Proteins
  • Cerebellar Neoplasms* / genetics
  • Cerebellar Neoplasms* / pathology
  • Hedgehog Proteins / metabolism
  • Humans
  • Medulloblastoma* / genetics
  • Mice
  • Proteomics
  • Transcription Factors / genetics
  • Transferases
  • Zinc Finger Protein GLI1 / genetics

Substances

  • Cell Cycle Proteins
  • Hedgehog Proteins
  • KCTD11 protein, human
  • SALL4 protein, human
  • Transcription Factors
  • Transferases
  • Zinc Finger Protein GLI1
  • Kctd11 protein, mouse
  • Sall4 protein, mouse
  • SHH protein, human
  • Shh protein, mouse