Distinct roles of hematopoietic cytokines in the regulation of leukemia stem cells in murine MLL-AF9 leukemia

Stem Cell Reports. 2024 Jan 9;19(1):100-111. doi: 10.1016/j.stemcr.2023.11.003. Epub 2023 Dec 14.

Abstract

Lymphoid-primed multipotent progenitor (LMPP)-like and granulocyte-monocyte progenitor (GMP)-like leukemia stem cells (LSCs) co-exist in the blood of most patients with acute myeloid leukemia (AML). Complete elimination of both types of LSCs is required to cure AML. Using an MLL-AF9-induced murine AML model, we studied the role of hematopoietic cytokines in the survival of LMPP- and GMP-like LSCs. We found that SCF or FLT3L promotes the survival of LMPP-like LSCs by stimulating Stat5-mediated Mcl1 expression, whereas interleukin-3 (IL-3) or IL-6 induces the survival of GMP-like LSCs by stimulating Stat3/nuclear factor κB (NF-κB)-mediated Bcl2 expression. Functional study demonstrated that, compared to AML cells cultured in IL-3 and IL-6 medium, AML cells in SCF- or Flt3L-only culture are highly clonogenic in in vitro culture and are highly leukemogenic in vivo. Our study suggests that co-inhibition of both STAT5-MCL1 and STAT3/NF-κB-BCL2 signaling might represent an improved treatment strategy against AML, specifically AML cases with a monocytic phenotype and/or FLT3 mutations.

Keywords: AML; Bcl2; Mcl1; hematopoietic cytokines; leukemia stem cells; survival signaling.

MeSH terms

  • Animals
  • Hematopoietic Stem Cells / metabolism
  • Humans
  • Interleukin-3* / metabolism
  • Interleukin-6 / metabolism
  • Leukemia, Myeloid, Acute* / genetics
  • Mice
  • Myeloid Cell Leukemia Sequence 1 Protein / metabolism
  • Myeloid-Lymphoid Leukemia Protein / genetics
  • Myeloid-Lymphoid Leukemia Protein / metabolism
  • NF-kappa B / metabolism
  • Neoplastic Stem Cells / metabolism
  • Oncogene Proteins, Fusion / genetics
  • STAT5 Transcription Factor / metabolism

Substances

  • Interleukin-3
  • STAT5 Transcription Factor
  • Myeloid Cell Leukemia Sequence 1 Protein
  • NF-kappa B
  • Interleukin-6
  • MLL-AF9 fusion protein, human
  • Oncogene Proteins, Fusion
  • Myeloid-Lymphoid Leukemia Protein