Super-enhancer-associated MEIS1 promotes transcriptional dysregulation in Ewing sarcoma in co-operation with EWS-FLI1

Nucleic Acids Res. 2019 Feb 20;47(3):1255-1267. doi: 10.1093/nar/gky1207.

Abstract

As the second most common malignant bone tumor in children and adolescents, Ewing sarcoma is initiated and exacerbated by a chimeric oncoprotein, most commonly, EWS-FLI1. In this study, we apply epigenomic analysis to characterize the transcription dysregulation in this cancer, focusing on the investigation of super-enhancer and its associated transcriptional regulatory mechanisms. We demonstrate that super-enhancer-associated transcripts are significantly enriched in EWS-FLI1 target genes, contribute to the aberrant transcriptional network of the disease, and mediate the exceptional sensitivity of Ewing sarcoma to transcriptional inhibition. Through integrative analysis, we identify MEIS1 as a super-enhancer-driven oncogene, which co-operates with EWS-FLI1 in transcriptional regulation, and plays a key pro-survival role in Ewing sarcoma. Moreover, APCDD1, another super-enhancer-associated gene, acting as a downstream target of both MEIS1 and EWS-FLI1, is also characterized as a novel tumor-promoting factor in this malignancy. These data delineate super-enhancer-mediated transcriptional deregulation in Ewing sarcoma, and uncover numerous candidate oncogenes which can be exploited for further understanding of the molecular pathogenesis for this disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / genetics
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Enhancer Elements, Genetic
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics*
  • Membrane Proteins / genetics*
  • Myeloid Ecotropic Viral Integration Site 1 Protein / genetics*
  • Nucleotide Motifs / genetics
  • Oncogene Proteins, Fusion / genetics
  • Proto-Oncogene Protein c-fli-1 / genetics
  • RNA-Binding Protein EWS / genetics
  • Sarcoma, Ewing / genetics*
  • Sarcoma, Ewing / pathology
  • Signal Transduction / genetics
  • Transcription, Genetic*

Substances

  • APCDD1 protein, human
  • EWS-FLI fusion protein
  • Intracellular Signaling Peptides and Proteins
  • MEIS1 protein, human
  • Membrane Proteins
  • Myeloid Ecotropic Viral Integration Site 1 Protein
  • Oncogene Proteins, Fusion
  • Proto-Oncogene Protein c-fli-1
  • RNA-Binding Protein EWS