Tumor methionine metabolism drives T-cell exhaustion in hepatocellular carcinoma

Nat Commun. 2021 Mar 5;12(1):1455. doi: 10.1038/s41467-021-21804-1.

Abstract

T-cell exhaustion denotes a hypofunctional state of T lymphocytes commonly found in cancer, but how tumor cells drive T-cell exhaustion remains elusive. Here, we find T-cell exhaustion linked to overall survival in 675 hepatocellular carcinoma (HCC) patients with diverse ethnicities and etiologies. Integrative omics analyses uncover oncogenic reprograming of HCC methionine recycling with elevated 5-methylthioadenosine (MTA) and S-adenosylmethionine (SAM) to be tightly linked to T-cell exhaustion. SAM and MTA induce T-cell dysfunction in vitro. Moreover, CRISPR-Cas9-mediated deletion of MAT2A, a key SAM producing enzyme, results in an inhibition of T-cell dysfunction and HCC growth in mice. Thus, reprogramming of tumor methionine metabolism may be a viable therapeutic strategy to improve HCC immunity.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Biomarkers, Tumor
  • CD8-Positive T-Lymphocytes
  • CRISPR-Cas Systems
  • Carcinogenesis / genetics
  • Carcinogenesis / metabolism
  • Carcinoma, Hepatocellular / genetics
  • Carcinoma, Hepatocellular / immunology
  • Carcinoma, Hepatocellular / metabolism*
  • Carcinoma, Hepatocellular / pathology
  • Cell Line, Tumor
  • Female
  • Gene Expression Regulation, Neoplastic
  • Gene Knockout Techniques
  • Humans
  • Liver / metabolism
  • Liver / pathology
  • Liver Neoplasms / genetics
  • Liver Neoplasms / immunology
  • Liver Neoplasms / metabolism*
  • Methionine / metabolism*
  • Methionine Adenosyltransferase / blood
  • Methionine Adenosyltransferase / genetics
  • Methionine Adenosyltransferase / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • S-Adenosylmethionine / metabolism
  • T-Lymphocytes / metabolism*
  • Transcriptome

Substances

  • Biomarkers, Tumor
  • S-Adenosylmethionine
  • Methionine
  • Mat2a protein, mouse
  • Methionine Adenosyltransferase