Activation of SOX2 expression by BRD4-NUT oncogenic fusion drives neoplastic transformation in NUT midline carcinoma

Cancer Res. 2014 Jun 15;74(12):3332-43. doi: 10.1158/0008-5472.CAN-13-2658. Epub 2014 Apr 15.

Abstract

BRD4 is implicated in the pathogenesis of a number of different cancers. It is also the target of translocation t(15;19) that accounts for the highly aggressive NUT midline carcinoma (NMC). We discovered that t(15;19) NMC cells display the ability to grow into stem cell-like spheres and express an exceptionally high level of the stem cell marker, SOX2. The BRD4-NUT fusion oncogene resulting from t(15;19) translocation is required for the abnormal activation of SOX2, which drives the stem cell-like proliferation and cellular transformation in NMC cells. SOX2 knockdown phenocopies the effects of BRD4-NUT inhibition, whereas ectopic SOX2 expression rescues the phenotype. The BRD4-NUT-induced abnormal SOX2 activation was observed in multiple NMC cell lines as well as in NMC primary tumors. We further demonstrate that BRD4-NUT oncoprotein recruits p300 to stimulate transcription activation and that inhibition of p300 represses SOX2 transcription in NMC cells. These studies identify this stem cell marker as a novel BRD4-NUT target that supports the highly aggressive transforming activity of t(15;19) carcinomas. Our study provides new mechanistic insights for understanding how alteration of BRD4 function by BRD4-NUT oncogene leads to the highly malignant NMC carcinoma. Because abnormal stem cell self-renewal is frequently observed during tumor formation and metastasis, the aberrant stem cell-like proliferation associated with BRD4 dysregulation observed in NMC carcinoma may have implications for studying the oncogenic mechanism of other BRD4-associated tumors.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Antineoplastic Agents / pharmacology
  • Azepines / pharmacology
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / metabolism*
  • Carcinoma, Squamous Cell / pathology
  • Cell Line, Tumor
  • Cell Transformation, Neoplastic / genetics
  • Cell Transformation, Neoplastic / metabolism*
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Nuclear Proteins / physiology*
  • Oncogene Proteins, Fusion / physiology*
  • Protein Binding
  • SOXB1 Transcription Factors / genetics
  • SOXB1 Transcription Factors / metabolism*
  • Spheroids, Cellular / drug effects
  • Spheroids, Cellular / metabolism
  • Transcription, Genetic
  • Transcriptional Activation
  • Triazoles / pharmacology
  • p300-CBP Transcription Factors / metabolism

Substances

  • (+)-JQ1 compound
  • Antineoplastic Agents
  • Azepines
  • BRD4-NUT fusion oncogene protein, human
  • Nuclear Proteins
  • Oncogene Proteins, Fusion
  • SOX2 protein, human
  • SOXB1 Transcription Factors
  • Triazoles
  • p300-CBP Transcription Factors