Activation of MAT2A-RIP1 signaling axis reprograms monocytes in gastric cancer

J Immunother Cancer. 2021 Feb;9(2):e001364. doi: 10.1136/jitc-2020-001364.

Abstract

Background: The activation of tumor-associated macrophages (TAMs) facilitates the progression of gastric cancer (GC). Cell metabolism reprogramming has been shown to play a vital role in the polarization of TAMs. However, the role of methionine metabolism in function of TAMs remains to be explored.

Methods: Monocytes/macrophages were isolated from peripheral blood, tumor tissues or normal tissues from healthy donors or patients with GC. The role of methionine metabolism in the activation of TAMs was evaluated with both in vivo analyses and in vitro experiments. Pharmacological inhibition of the methionine cycle and modulation of key metabolic genes was employed, where molecular and biological analyses were performed.

Results: TAMs have increased methionine cycle activity that are mainly attributed to elevated methionine adenosyltransferase II alpha (MAT2A) levels. MAT2A modulates the activation and maintenance of the phenotype of TAMs and mediates the upregulation of RIP1 by increasing the histone H3K4 methylation (H3K4me3) at its promoter regions.

Conclusions: Our data cast light on a novel mechanism by which methionine metabolism regulates the anti-inflammatory functions of monocytes in GC. MAT2A might be a potential therapeutic target for cancer cells as well as TAMs in GC.

Keywords: immune evation; immunomodulation; macrophages; tumor escape; tumor microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Case-Control Studies
  • Cell Line, Tumor
  • Cell Polarity
  • Cellular Reprogramming
  • Gene Expression Regulation, Neoplastic
  • Histones / metabolism
  • Humans
  • Methionine / metabolism*
  • Methionine Adenosyltransferase / metabolism*
  • Methylation
  • Mice
  • Monocytes / metabolism*
  • Neoplasm Transplantation
  • Promoter Regions, Genetic
  • Receptor-Interacting Protein Serine-Threonine Kinases / genetics*
  • Receptor-Interacting Protein Serine-Threonine Kinases / metabolism
  • Signal Transduction
  • Stomach Neoplasms / metabolism
  • Stomach Neoplasms / pathology*
  • Tumor-Associated Macrophages / metabolism
  • Up-Regulation*

Substances

  • Histones
  • Methionine
  • MAT2A protein, human
  • Methionine Adenosyltransferase
  • RIPK1 protein, human
  • Receptor-Interacting Protein Serine-Threonine Kinases