A novel FOXM1-BCL2A1 axis determines unfavorable response to venetoclax in AML

J Biol Chem. 2025 Mar;301(3):108240. doi: 10.1016/j.jbc.2025.108240. Epub 2025 Jan 27.

Abstract

Forkhead box M1 (FOXM1), a Forkhead family transcription factor, is often overexpressed in a variety of human cancers, including acute myeloid leukemia (AML), and is strongly associated with therapy resistance and unfavorable outcomes. In AML with NPM1 mutations, NPM1-FOXM1 complex sequesters FOXM1 in the cytoplasm and confers favorable treatment outcomes for AML patients because of FOXM1 inactivation. Inhibition of FOXM1 in AML cell lines and animal models of AML sensitizes AML cells to the BCL2 inhibitor, venetoclax. In a recent study, the upregulation of the BCL2-family protein, BCL2A1, conferred resistance to venetoclax and multiple venetoclax combinations. In this study, we investigated the FOXM1-BCL2A1 axis and determined that FOXM1 specifically inhibits venetoclax-induced apoptosis in AML via upregulation of BCL2A1. The knockdown of BCL2A1 in AML in the presence of high levels of FOXM1 led to sensitization of AML cells to venetoclax, suggesting that BCL2A1 is a major target of FOXM1 responsible for resistance to venetoclax. Venetoclax in combination with FOXM1 inhibitor STL001 inhibited BCL2A1 and circumvented venetoclax resistance. Pharmacological inhibition of the FOXM1-BCL2A1 axis represents a therapeutic strategy to sensitize AML cells to venetoclax-induced apoptosis.

Keywords: AML; BCL2A1; FOXM1; apoptosis; venetoclax.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects
  • Bridged Bicyclo Compounds, Heterocyclic* / pharmacology
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm / drug effects
  • Forkhead Box Protein M1* / antagonists & inhibitors
  • Forkhead Box Protein M1* / genetics
  • Forkhead Box Protein M1* / metabolism
  • Humans
  • Leukemia, Myeloid, Acute* / drug therapy
  • Leukemia, Myeloid, Acute* / genetics
  • Leukemia, Myeloid, Acute* / metabolism
  • Leukemia, Myeloid, Acute* / pathology
  • Mice
  • Minor Histocompatibility Antigens
  • Nucleophosmin
  • Proto-Oncogene Proteins c-bcl-2* / antagonists & inhibitors
  • Proto-Oncogene Proteins c-bcl-2* / genetics
  • Proto-Oncogene Proteins c-bcl-2* / metabolism
  • Sulfonamides* / pharmacology

Substances

  • venetoclax
  • Forkhead Box Protein M1
  • Bridged Bicyclo Compounds, Heterocyclic
  • Sulfonamides
  • FOXM1 protein, human
  • Proto-Oncogene Proteins c-bcl-2
  • BCL2-related protein A1
  • Nucleophosmin
  • NPM1 protein, human
  • Antineoplastic Agents
  • Minor Histocompatibility Antigens