Inhibiting H3K27 Demethylases Downregulates CREB-CREBBP, Overcoming Resistance in Relapsed Acute Lymphoblastic Leukemia

Cancer Med. 2025 Jan;14(1):1-7. doi: 10.1002/cam4.70596.

Abstract

Background: CREB binding protein (CREBBP) is a key epigenetic regulator, altered in a fifth of relapsed cases of acute lymphoblastic leukemia (ALL). Selectively targeting epigenetic signaling may be an effective novel therapeutic approach to overcome drug resistance. Anti-tumor effects have previously been demonstrated for GSK-J4, a selective H3K27 histone demethylase inhibitor, in several animal models of cancers.

Methods: To characterize the effect of GSK-J4, drug response profiling, CRISPR-Dropout Screening, BH3 profiling and immunoblotting were carried out in ALL cell lines or patient derived samples.

Results: Here we provide evidence that GSK-J4 downregulates cyclic AMP-responsive element-binding protein (CREB) and CREBBP in B-cell precursor-ALL cell lines and patient samples. High CREBBP expression in BCP-ALL cell lines correlated with high GSK-J4 sensitivity and low dexamethasone sensitivity. GSK-J4 treatment also induced Bcl-2 and Bcl-XL dependency and apoptosis.

Conclusions: This study proposes H3K27 demethylase inhibition as a potential treatment strategy for patients with treatment-resistant ALL, using CREBBP as a biomarker for drug response and combining GSK-J4 with venetoclax and navitoclax as synergistic partners.

Keywords: apoptosis; drug discovery and delivery; epigenetics; leukemia.

MeSH terms

  • Apoptosis / drug effects
  • Benzazepines
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Bridged Bicyclo Compounds, Heterocyclic / therapeutic use
  • CREB-Binding Protein* / genetics
  • CREB-Binding Protein* / metabolism
  • Cell Line, Tumor
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Down-Regulation
  • Drug Resistance, Neoplasm*
  • Histone Demethylases / antagonists & inhibitors
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism
  • Humans
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma* / drug therapy
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma* / genetics
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma* / metabolism
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma* / pathology
  • Pyrimidines / pharmacology
  • Sulfonamides / pharmacology

Substances

  • CREB-Binding Protein
  • GSK-J4
  • CREBBP protein, human
  • Histone Demethylases
  • Pyrimidines
  • Cyclic AMP Response Element-Binding Protein
  • Bridged Bicyclo Compounds, Heterocyclic
  • Sulfonamides
  • Benzazepines