Hexokinase 2 senses fructose in tumor-associated macrophages to promote colorectal cancer growth

Cell Metab. 2024 Nov 5;36(11):2449-2467.e6. doi: 10.1016/j.cmet.2024.10.002. Epub 2024 Oct 28.

Abstract

Fructose is associated with colorectal cancer tumorigenesis and metastasis through ketohexokinase-mediated metabolism in the colorectal epithelium, yet its role in the tumor immune microenvironment remains largely unknown. Here, we show that a modest amount of fructose, without affecting obesity and associated complications, promotes colorectal cancer tumorigenesis and growth by suppressing the polarization of M1-like macrophages. Fructose inhibits M1-like macrophage polarization independently of fructose-mediated metabolism. Instead, it serves as a signal molecule to promote the interaction between hexokinase 2 and inositol 1,4,5-trisphophate receptor type 3, the predominant Ca2+ channel on the endoplasmic reticulum. The interaction reduces Ca2+ levels in cytosol and mitochondria, thereby suppressing the activation of mitogen-activated protein kinase (MAPK) and signal transducer and activator of transcription 1 (STAT1) as well as NOD-, LRR- and pyrin domain-containing protein 3 (NLRP3) inflammasome activation. Consequently, this impedes M1-like macrophage polarization. Our study highlights the critical role of fructose as a signaling molecule that impairs the polarization of M1-like macrophages for tumor growth.

Keywords: M1-like macrophage polarization; calcium signaling; fructose; hexokinase 2; inositol 1,4,5-trisphophate receptor type 3.

MeSH terms

  • Animals
  • Cell Proliferation
  • Colorectal Neoplasms* / etiology
  • Colorectal Neoplasms* / metabolism
  • Colorectal Neoplasms* / pathology
  • Fructose* / metabolism
  • Hexokinase* / metabolism
  • Humans
  • Inflammasomes / metabolism
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Tumor-Associated Macrophages* / metabolism
  • Tumor-Associated Macrophages* / pathology

Substances

  • Fructose
  • Hexokinase
  • hexokinase 2, mouse
  • Inflammasomes
  • NLR Family, Pyrin Domain-Containing 3 Protein