Macrophages are activated toward phagocytic lymphoma cell clearance by pentose phosphate pathway inhibition

Cell Rep Med. 2024 Dec 17;5(12):101830. doi: 10.1016/j.xcrm.2024.101830. Epub 2024 Nov 26.

Abstract

Macrophages in the B cell lymphoma microenvironment represent a functional node in progression and therapeutic response. We assessed metabolic regulation of macrophages in the context of therapeutic antibody-mediated phagocytosis. Pentose phosphate pathway (PPP) inhibition induces increased phagocytic lymphoma cell clearance by macrophages in vitro, in primary human chronic lymphocytic leukemia (CLL) patient co-cultures, and in mouse models. Addition of the PPP inhibitor S3 to antibody therapy achieves significantly prolonged overall survival in an aggressive B cell lymphoma mouse model. PPP inhibition induces metabolic activation and pro-inflammatory polarization of macrophages while it decreases macrophages' support for survival of lymphoma cells empowering anti-lymphoma function. As a mechanism of macrophage repolarization, the link between PPP and immune regulation was identified. PPP inhibition causes decreased glycogen level and subsequent modulation of the immune modulatory uridine diphosphate glucose (UDPG)-Stat1-Irg1-itaconate axis. Thus, we hypothesize the PPP as a key regulator and targetable modulator of macrophage activity in lymphoma to improve efficacy of immunotherapies and prolong survival.

Keywords: ADCP; Irg1; immunotherapy; itaconate; lymphoma; macrophage; metabolic modulation; pentose phosphate pathway; phagocytosis; polarization.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Humans
  • Leukemia, Lymphocytic, Chronic, B-Cell / drug therapy
  • Leukemia, Lymphocytic, Chronic, B-Cell / immunology
  • Leukemia, Lymphocytic, Chronic, B-Cell / metabolism
  • Leukemia, Lymphocytic, Chronic, B-Cell / pathology
  • Macrophage Activation / drug effects
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Mice
  • Pentose Phosphate Pathway* / drug effects
  • Phagocytosis*
  • Tumor Microenvironment / immunology