The BET bromodomain inhibitor I-BET151 acts downstream of smoothened protein to abrogate the growth of hedgehog protein-driven cancers

J Biol Chem. 2014 Dec 19;289(51):35494-502. doi: 10.1074/jbc.M114.595348. Epub 2014 Oct 29.

Abstract

Epigenetic enzymes modulate signal transduction pathways in different biological contexts. We reasoned that epigenetic regulators might modulate the Hedgehog (HH) signaling pathway, a main driver of cell proliferation in various cancers including medulloblastoma. To test this hypothesis, we performed an unbiased small-molecule screen utilizing an HH-dependent reporter cell line (Light2 cells). We incubated Light2 cells with small molecules targeting different epigenetic modulators and identified four histone deacetylase inhibitors and a bromodomain and extra terminal domain (BET) protein inhibitor (I-BET151) that attenuate HH activity. I-BET151 was also able to inhibit the expression of HH target genes in Sufu(-/-) mouse embryonic fibroblasts, in which constitutive Gli activity is activated in a Smoothened (Smo)-independent fashion, consistent with it acting downstream of Smo. Knockdown of Brd4 (which encodes one of the BET proteins) phenocopies I-BET151 treatment, suggesting that Brd4 is a regulator of the HH signaling pathway. Consistent with this suggestion, Brd4 associates with the proximal promoter region of the Gli1 locus, and does so in a manner that can be reversed by I-BET151. Importantly, I-BET151 also suppressed the HH activity-dependent growth of medulloblastoma cells, in vitro and in vivo. These studies suggest that BET protein modulation may be an attractive therapeutic strategy for attenuating the growth of HH-dependent cancers, such as medulloblastoma.

Keywords: Bromodomain-containing Protein 4 (BRD4); Drug Screening; Epigenetics; Gli; Hedgehog Signaling Pathway; I-BET151; Medulloblastoma.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Cell Proliferation / drug effects*
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Embryo, Mammalian / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Gene Expression Regulation, Neoplastic / drug effects
  • Hedgehog Proteins / genetics*
  • Hedgehog Proteins / metabolism
  • Heterocyclic Compounds, 4 or More Rings / pharmacology*
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism
  • Medulloblastoma / genetics
  • Medulloblastoma / metabolism
  • Medulloblastoma / prevention & control*
  • Mice, Knockout
  • Mice, Nude
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • RNA Interference
  • Receptors, G-Protein-Coupled / genetics*
  • Receptors, G-Protein-Coupled / metabolism
  • Repressor Proteins / deficiency
  • Repressor Proteins / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Smoothened Receptor
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Zinc Finger Protein GLI1

Substances

  • Brd4 protein, mouse
  • GSK1210151A
  • Gli1 protein, mouse
  • Hedgehog Proteins
  • Heterocyclic Compounds, 4 or More Rings
  • Kruppel-Like Transcription Factors
  • Nuclear Proteins
  • Receptors, G-Protein-Coupled
  • Repressor Proteins
  • Smo protein, mouse
  • Smoothened Receptor
  • Sufu protein, mouse
  • Transcription Factors
  • Zinc Finger Protein GLI1