Glycogenesis and glyconeogenesis from glutamine, lactate and glycerol support human macrophage functions

EMBO Rep. 2024 Dec;25(12):5383-5407. doi: 10.1038/s44319-024-00278-4. Epub 2024 Oct 18.

Abstract

Macrophages fight infection and ensure tissue repair, often operating at nutrient-poor wound sites. We investigated the ability of human macrophages to metabolize glycogen. We observed that the cytokines GM-CSF and M-CSF plus IL-4 induced glycogenesis and the accumulation of glycogen by monocyte-derived macrophages. Glyconeogenesis occurs in cells cultured in the presence of the inflammatory cytokines GM-CSF and IFNγ (M1 cells), via phosphoenolpyruvate carboxykinase 2 (PCK2) and fructose-1,6-bisphosphatase 1 (FBP1). Enzyme inhibition with drugs or gene silencing techniques and 13C-tracing demonstrate that glutamine (metabolized by the TCA cycle), lactic acid, and glycerol were substrates of glyconeogenesis only in M1 cells. Tumor-associated macrophages (TAMs) also store glycogen and can perform glyconeogenesis. Finally, macrophage glycogenolysis and the pentose phosphate pathway (PPP) support cytokine secretion and phagocytosis regardless of the availability of extracellular glucose. Thus, glycogen metabolism supports the functions of human M1 and M2 cells, with inflammatory M1 cells displaying a possible dependence on glyconeogenesis.

Keywords: Cytokine secretion; Glycogenolysis; Glyconeogenesis; Macrophages; Phagocytosis.

MeSH terms

  • Cytokines / metabolism
  • Fructose-Bisphosphatase / genetics
  • Fructose-Bisphosphatase / metabolism
  • Gluconeogenesis
  • Glutamine* / metabolism
  • Glycerol* / metabolism
  • Glycogen* / metabolism
  • Glycogenolysis
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism
  • Humans
  • Interferon-gamma / metabolism
  • Interferon-gamma / pharmacology
  • Interleukin-4 / metabolism
  • Lactic Acid* / metabolism
  • Macrophage Colony-Stimulating Factor / metabolism
  • Macrophages* / metabolism
  • Pentose Phosphate Pathway
  • Phagocytosis
  • Phosphoenolpyruvate Carboxykinase (ATP)
  • Phosphoenolpyruvate Carboxykinase (GTP) / genetics
  • Phosphoenolpyruvate Carboxykinase (GTP) / metabolism

Substances

  • Glutamine
  • Glycogen
  • Glycerol
  • Lactic Acid
  • PCK2 protein, human
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Phosphoenolpyruvate Carboxykinase (GTP)
  • Fructose-Bisphosphatase
  • Interleukin-4
  • Macrophage Colony-Stimulating Factor
  • Interferon-gamma
  • Cytokines
  • Phosphoenolpyruvate Carboxykinase (ATP)