Differential inflammatory conditioning of the bone marrow by acute myeloid leukemia and its impact on progression

Blood Adv. 2024 Oct 8;8(19):4983-4996. doi: 10.1182/bloodadvances.2024012867.

Abstract

Inflammation promotes solid tumor progression, but how regulatory mechanisms of inflammation may affect leukemia is less well studied. Using annexin A5 (ANXA5), a calcium-binding protein known for apoptosis, which we discovered to be differentially expressed in the bone marrow microenvironment (BMM) of mice with acute myeloid (AML) vs chronic myeloid leukemia, as a model system, we unravel here a circuit in which AML-derived tumor necrosis factor α (TNF-α) dose-dependently reduces ANXA5 in the BMM. This creates an inflammatory BMM via elevated levels of prostaglandin E2 (PGE2). Via binding to its EP4 receptor, PGE2 increases β-catenin and hypoxia-inducible factor 1α signaling in AML cells, thereby accelerating PGE2-sensitive AML. Human trephine biopsies may show lower ANXA5 expression and higher PGE2 expression in AML than other hematologic malignancies. Furthermore, syngeneic and xenogeneic transplantation models suggest a survival benefit after treatment with the inhibitor of prostaglandin-endoperoxide synthase 2 (cyclooxygenase 2 [COX2]), celecoxib, plus cytarabine in those AML types highly sensitive to PGE2 compared with cytarabine alone. Taken together, TNF-α/ANXA5/NF-κB/COX2/PGE2-mediated inflammation influences AML course in a highly differential and circular manner, and patients with AML with "inflammatory AML" may benefit from antiphlogistic agents as adjunct therapy.

MeSH terms

  • Animals
  • Bone Marrow* / metabolism
  • Bone Marrow* / pathology
  • Dinoprostone* / metabolism
  • Disease Models, Animal
  • Disease Progression*
  • Humans
  • Inflammation* / metabolism
  • Inflammation* / pathology
  • Leukemia, Myeloid, Acute* / metabolism
  • Leukemia, Myeloid, Acute* / pathology
  • Mice
  • Signal Transduction
  • Tumor Microenvironment
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Dinoprostone
  • Tumor Necrosis Factor-alpha