The transcriptional co-repressor Runx1t1 is essential for MYCN-driven neuroblastoma tumorigenesis

Nat Commun. 2024 Jul 11;15(1):5585. doi: 10.1038/s41467-024-49871-0.

Abstract

MYCN oncogene amplification is frequently observed in aggressive childhood neuroblastoma. Using an unbiased large-scale mutagenesis screen in neuroblastoma-prone transgenic mice, we identify a single germline point mutation in the transcriptional corepressor Runx1t1, which abolishes MYCN-driven tumorigenesis. This loss-of-function mutation disrupts a highly conserved zinc finger domain within Runx1t1. Deletion of one Runx1t1 allele in an independent Runx1t1 knockout mouse model is also sufficient to prevent MYCN-driven neuroblastoma development, and reverse ganglia hyperplasia, a known pre-requisite for tumorigenesis. Silencing RUNX1T1 in human neuroblastoma cells decreases colony formation in vitro, and inhibits tumor growth in vivo. Moreover, RUNX1T1 knockdown inhibits the viability of PAX3-FOXO1 fusion-driven rhabdomyosarcoma and MYC-driven small cell lung cancer cells. Despite the role of Runx1t1 in MYCN-driven tumorigenesis neither gene directly regulates the other. We show RUNX1T1 forms part of a transcriptional LSD1-CoREST3-HDAC repressive complex recruited by HAND2 to enhancer regions to regulate chromatin accessibility and cell-fate pathway genes.

MeSH terms

  • Animals
  • Carcinogenesis* / genetics
  • Cell Line, Tumor
  • Co-Repressor Proteins / genetics
  • Co-Repressor Proteins / metabolism
  • Gene Expression Regulation, Neoplastic
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism
  • Humans
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • N-Myc Proto-Oncogene Protein* / genetics
  • N-Myc Proto-Oncogene Protein* / metabolism
  • Neuroblastoma* / genetics
  • Neuroblastoma* / metabolism
  • Neuroblastoma* / pathology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Co-Repressor Proteins
  • Histone Demethylases
  • MYCN protein, human
  • MYCN protein, mouse
  • N-Myc Proto-Oncogene Protein
  • Transcription Factors
  • RUNX1T1 protein, human
  • Runx1 protein, mouse