Inhibition of BRD4 attenuated IFNγ-induced apoptosis in colorectal cancer organoids

BMC Cancer. 2025 Jan 23;25(1):136. doi: 10.1186/s12885-025-13544-y.

Abstract

Background: This study aimed to analyze the functional role of Brd4 in colorectal cancer (CRC) organoids. Brd4 was identified as a CRC-related gene by our previous Sleeping Beauty mutagenesis transposon screening in mice. Brd4 is a transcriptional regulator that recognizes acetylated histones and is known to be involved in inflammatory responses. The role of Brd4 in CRC development remains largely unknown.

Methods: We knocked out Brd4 in tumor organoids carrying mutations in Apc and Kras to generate Brd4KO organoids, and performed RNA-seq. The response of Brd4KO organoids to IFNγ was analyzed via a cell viability assay, an apoptosis assay, and RNAseq. The results were validated by pharmacological inhibition experiments with JQ1 in human CRC organoids.

Results: In Brd4KO organoids, the IFNγ signaling genes Il33 and Myc target genes were downregulated. The addition of IFNγ to the colon organoids induced apoptosis, but IFNγ-induced apoptosis was attenuated in the Brd4KO organoids compared with the control organoids (two-sided t-test, P < 0.05). Similar results were obtained from pharmacological inhibition with JQ1 in human CRC organoids; IL33 expression was decreased, and IFNγ-induced apoptosis was attenuated in the presence of JQ1.

Conclusions: Our results showed that the inhibition of Brd4 suppressed IFNγ-induced cytotoxicity by modulating the Jak-Stat pathway. These data suggested that the inhibition of Brd4 could increase cell viability in the cancer microenvironment where IFNγ is abundant, revealing a new aspect of the molecular mechanism of CRC development. Our results may help in evaluating the application of Bet inhibitors in treating CRC. Additionally, our RNA-seq data sets will be helpful for clarifying the relationship between Brd4 and immunomodulators, such as Il33, or for studying the responses of colonic epithelial cells to IFNγ.

Keywords: Apoptosis; Brd4; Colorectal cancer; IFNγ; IL33; JQ1; Organoid.

MeSH terms

  • Animals
  • Apoptosis* / drug effects
  • Azepines* / pharmacology
  • Bromodomain Containing Proteins
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Colorectal Neoplasms* / drug therapy
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / metabolism
  • Colorectal Neoplasms* / pathology
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Interferon-gamma* / metabolism
  • Interferon-gamma* / pharmacology
  • Mice
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Organoids* / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism
  • Triazoles* / pharmacology

Substances

  • Transcription Factors
  • Interferon-gamma
  • BRD4 protein, human
  • Azepines
  • (+)-JQ1 compound
  • Triazoles
  • Brd4 protein, mouse
  • Cell Cycle Proteins
  • Nuclear Proteins
  • Bromodomain Containing Proteins