ZBTB7A is a modulator of KDM5-driven transcriptional networks in basal breast cancer

Cell Rep. 2024 Dec 24;43(12):114991. doi: 10.1016/j.celrep.2024.114991. Epub 2024 Nov 20.

Abstract

We previously described that the KDM5B histone H3 lysine 4 demethylase is an oncogene in estrogen-receptor-positive breast cancer. Here, we report that KDM5A is amplified and overexpressed in basal breast tumors, and KDM5 inhibition (KDM5i) suppresses the growth of KDM5-amplified breast cancer cell lines. Using CRISPR knockout screens in a basal breast cancer cell line with or without KDM5i, we found that deletion of the ZBTB7A transcription factor and core SAGA complex sensitizes cells to KDM5i, whereas deletion of RHO-GTPases leads to resistance. Chromatin immunoprecipitation sequencing (ChIP-seq) and RNA sequencing (RNA-seq) revealed co-localization of ZBTB7A and KDM5A/B at promoters with high histone H3K4me3 and dependence of KDM5A chromatin binding on ZBTB7A. ZBTB7A knockout altered the transcriptional response to KDM5i at NF-κB targets and mitochondrion-related pathways. High expression of ZBTB7A in triple-negative breast cancer is significantly associated with poor response to neoadjuvant chemotherapy. Our work furthers the understanding of KDM5-mediated gene regulation and identifies mediators of sensitivity to KDM5i.

Keywords: CP: Cancer; CRISPR screen; breast cancer; histone demethylase; mitochondrial signaling.

MeSH terms

  • Animals
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / pathology
  • Cell Line, Tumor
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Gene Regulatory Networks
  • Histones / metabolism
  • Humans
  • NF-kappa B / metabolism
  • Promoter Regions, Genetic / genetics
  • Retinoblastoma-Binding Protein 2 / genetics
  • Retinoblastoma-Binding Protein 2 / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Transcription Factors
  • DNA-Binding Proteins
  • KDM5A protein, human
  • ZBTB7A protein, human
  • Retinoblastoma-Binding Protein 2
  • Histones
  • NF-kappa B