Targeting MCL1-driven anti-apoptotic pathways overcomes blast progression after hypomethylating agent failure in chronic myelomonocytic leukemia

Cell Rep Med. 2024 Jun 18;5(6):101585. doi: 10.1016/j.xcrm.2024.101585. Epub 2024 May 22.

Abstract

RAS pathway mutations, which are present in 30% of patients with chronic myelomonocytic leukemia (CMML) at diagnosis, confer a high risk of resistance to and progression after hypomethylating agent (HMA) therapy, the current standard of care for the disease. Here, using single-cell, multi-omics technologies, we seek to dissect the biological mechanisms underlying the initiation and progression of RAS pathway-mutated CMML. We identify that RAS pathway mutations induce transcriptional reprogramming of hematopoietic stem and progenitor cells (HSPCs) and downstream monocytic populations in response to cell-intrinsic and -extrinsic inflammatory signaling that also impair the functions of immune cells. HSPCs expand at disease progression after therapy with HMA or the BCL2 inhibitor venetoclax and rely on the NF-κB pathway effector MCL1 to maintain survival. Our study has implications for the development of therapies to improve the survival of patients with RAS pathway-mutated CMML.

Keywords: CMML; MCL1; NF-kB; RAS; multiomics; progression; transcriptomics.

MeSH terms

  • Animals
  • Apoptosis* / drug effects
  • Blast Crisis / drug therapy
  • Blast Crisis / genetics
  • Blast Crisis / metabolism
  • Blast Crisis / pathology
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Bridged Bicyclo Compounds, Heterocyclic / therapeutic use
  • DNA Methylation / drug effects
  • DNA Methylation / genetics
  • Disease Progression
  • Hematopoietic Stem Cells / drug effects
  • Hematopoietic Stem Cells / metabolism
  • Humans
  • Leukemia, Myelomonocytic, Chronic* / drug therapy
  • Leukemia, Myelomonocytic, Chronic* / genetics
  • Leukemia, Myelomonocytic, Chronic* / metabolism
  • Leukemia, Myelomonocytic, Chronic* / pathology
  • Mice
  • Mutation* / genetics
  • Myeloid Cell Leukemia Sequence 1 Protein* / antagonists & inhibitors
  • Myeloid Cell Leukemia Sequence 1 Protein* / genetics
  • Myeloid Cell Leukemia Sequence 1 Protein* / metabolism
  • NF-kappa B / metabolism
  • Signal Transduction / drug effects
  • Sulfonamides / pharmacology
  • Sulfonamides / therapeutic use

Substances

  • Myeloid Cell Leukemia Sequence 1 Protein
  • MCL1 protein, human
  • venetoclax
  • Sulfonamides
  • NF-kappa B
  • Bridged Bicyclo Compounds, Heterocyclic