A PRC2-Kdm5b axis sustains tumorigenicity of acute myeloid leukemia

Proc Natl Acad Sci U S A. 2022 Mar 1;119(9):e2122940119. doi: 10.1073/pnas.2122940119.

Abstract

Acute myeloid leukemias (AMLs) with the NUP98-NSD1 or mixed lineage leukemia (MLL) rearrangement (MLL-r) share transcriptomic profiles associated with stemness-related gene signatures and display poor prognosis. The molecular underpinnings of AML aggressiveness and stemness remain far from clear. Studies with EZH2 enzymatic inhibitors show that polycomb repressive complex 2 (PRC2) is crucial for tumorigenicity in NUP98-NSD1+ AML, whereas transcriptomic analysis reveal that Kdm5b, a lysine demethylase gene carrying "bivalent" chromatin domains, is directly repressed by PRC2. While ectopic expression of Kdm5b suppressed AML growth, its depletion not only promoted tumorigenicity but also attenuated anti-AML effects of PRC2 inhibitors, demonstrating a PRC2-|Kdm5b axis for AML oncogenesis. Integrated RNA sequencing (RNA-seq), chromatin immunoprecipitation followed by sequencing (ChIP-seq), and Cleavage Under Targets & Release Using Nuclease (CUT&RUN) profiling also showed that Kdm5b directly binds and represses AML stemness genes. The anti-AML effect of Kdm5b relies on its chromatin association and/or scaffold functions rather than its demethylase activity. Collectively, this study describes a molecular axis that involves histone modifiers (PRC2-|Kdm5b) for sustaining AML oncogenesis.

Keywords: AML; Kdm5b; PRC2; stemness; tumorigenicity.

MeSH terms

  • Animals
  • Carcinogenesis
  • Gene Expression Profiling
  • Histone Demethylases / metabolism
  • Humans
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • Leukemia, Myeloid, Acute / metabolism
  • Leukemia, Myeloid, Acute / pathology*
  • Mice
  • Nuclear Proteins / metabolism*
  • Oncogene Proteins / metabolism
  • Polycomb Repressive Complex 2 / antagonists & inhibitors
  • Polycomb Repressive Complex 2 / metabolism*
  • Protein Binding
  • Repressor Proteins / metabolism*
  • Sequence Analysis, RNA / methods

Substances

  • Nuclear Proteins
  • Oncogene Proteins
  • Repressor Proteins
  • Histone Demethylases
  • Jumonji Domain-Containing Histone Demethylases
  • KDM5B protein, human
  • Polycomb Repressive Complex 2