Loss of the Notch effector RBPJ promotes tumorigenesis

J Exp Med. 2015 Jan 12;212(1):37-52. doi: 10.1084/jem.20121192. Epub 2014 Dec 15.

Abstract

Aberrant Notch activity is oncogenic in several malignancies, but it is unclear how expression or function of downstream elements in the Notch pathway affects tumor growth. Transcriptional regulation by Notch is dependent on interaction with the DNA-binding transcriptional repressor, RBPJ, and consequent derepression or activation of associated gene promoters. We show here that RBPJ is frequently depleted in human tumors. Depletion of RBPJ in human cancer cell lines xenografted into immunodeficient mice resulted in activation of canonical Notch target genes, and accelerated tumor growth secondary to reduced cell death. Global analysis of activated regions of the genome, as defined by differential acetylation of histone H4 (H4ac), revealed that the cell death pathway was significantly dysregulated in RBPJ-depleted tumors. Analysis of transcription factor binding data identified several transcriptional activators that bind promoters with differential H4ac in RBPJ-depleted cells. Functional studies demonstrated that NF-κB and MYC were essential for survival of RBPJ-depleted cells. Thus, loss of RBPJ derepresses target gene promoters, allowing Notch-independent activation by alternate transcription factors that promote tumorigenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Animals
  • Carcinogenesis / genetics*
  • Carcinogenesis / metabolism
  • Cell Line, Tumor
  • Female
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • Histones / metabolism
  • Humans
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein / genetics*
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein / metabolism
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Mutation
  • NF-kappa B / metabolism
  • Neoplasms / genetics*
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • Promoter Regions, Genetic / genetics
  • Protein Binding
  • Proto-Oncogene Proteins c-myc / metabolism
  • RNA Interference
  • Receptors, Notch / genetics*
  • Receptors, Notch / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / genetics
  • Transplantation, Heterologous

Substances

  • Histones
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein
  • MYC protein, human
  • NF-kappa B
  • Proto-Oncogene Proteins c-myc
  • RBPJ protein, human
  • Receptors, Notch