BRD4 Connects Enhancer Remodeling to Senescence Immune Surveillance

Cancer Discov. 2016 Jun;6(6):612-29. doi: 10.1158/2159-8290.CD-16-0217. Epub 2016 Apr 20.

Abstract

Oncogene-induced senescence is a potent barrier to tumorigenesis that limits cellular expansion following certain oncogenic events. Senescent cells display a repressive chromatin configuration thought to stably silence proliferation-promoting genes while simultaneously activating an unusual form of immune surveillance involving a secretory program referred to as the senescence-associated secretory phenotype (SASP). Here, we demonstrate that senescence also involves a global remodeling of the enhancer landscape with recruitment of the chromatin reader BRD4 to newly activated super-enhancers adjacent to key SASP genes. Transcriptional profiling and functional studies indicate that BRD4 is required for the SASP and downstream paracrine signaling. Consequently, BRD4 inhibition disrupts immune cell-mediated targeting and elimination of premalignant senescent cells in vitro and in vivo Our results identify a critical role for BRD4-bound super-enhancers in senescence immune surveillance and in the proper execution of a tumor-suppressive program.

Significance: This study reveals how cells undergoing oncogene-induced senescence acquire a distinctive enhancer landscape that includes formation of super-enhancers adjacent to immune-modulatory genes required for paracrine immune activation. This process links BRD4 and super-enhancers to a tumor-suppressive immune surveillance program that can be disrupted by small molecule inhibitors of the bromo and extra terminal domain family of proteins. Cancer Discov; 6(6); 612-29. ©2016 AACR.See related commentary by Vizioli and Adams, p. 576This article is highlighted in the In This Issue feature, p. 561.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Binding Sites
  • Cell Cycle / genetics
  • Cell Cycle Proteins
  • Cell Line, Tumor
  • Cell Proliferation
  • Cellular Senescence / genetics*
  • Chromatin Assembly and Disassembly*
  • Chromatin Immunoprecipitation
  • Cluster Analysis
  • Computational Biology / methods
  • Enhancer Elements, Genetic*
  • Fibroblasts
  • GTP Phosphohydrolases / genetics
  • GTP Phosphohydrolases / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Hepatocytes / metabolism
  • High-Throughput Nucleotide Sequencing
  • Histones / metabolism
  • Humans
  • Immunologic Surveillance / genetics*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Nuclear Proteins / metabolism*
  • Nucleotide Motifs
  • Oncogenes
  • Paracrine Communication
  • Position-Specific Scoring Matrices
  • Protein Binding
  • Transcription Factors / metabolism*

Substances

  • BRD4 protein, human
  • Cell Cycle Proteins
  • Histones
  • Membrane Proteins
  • Nuclear Proteins
  • Transcription Factors
  • GTP Phosphohydrolases
  • NRAS protein, human