Suppression of the METTL3-m6A-integrin β1 axis by extracellular acidification impairs T cell infiltration and antitumor activity

Cell Rep. 2024 Feb 27;43(2):113796. doi: 10.1016/j.celrep.2024.113796. Epub 2024 Feb 16.

Abstract

The acidic metabolic byproducts within the tumor microenvironment (TME) hinder T cell effector functions. However, their effects on T cell infiltration remain largely unexplored. Leveraging the comprehensive The Cancer Genome Atlas dataset, we pinpoint 16 genes that correlate with extracellular acidification and establish a metric known as the "tumor acidity (TuAci) score" for individual patients. We consistently observe a negative association between the TuAci score and T lymphocyte score (T score) across various human cancer types. Mechanistically, extracellular acidification significantly impedes T cell motility by suppressing podosome formation. This phenomenon can be attributed to the reduced expression of methyltransferase-like 3 (METTL3) and the modification of RNA N6-methyladenosine (m6A), resulting in a subsequent decrease in the expression of integrin β1 (ITGB1). Importantly, enforced ITGB1 expression leads to enhanced T cell infiltration and improved antitumor activity. Our study suggests that modulating METTL3 activity or boosting ITGB1 expression could augment T cell infiltration within the acidic TME, thereby improving the efficacy of cell therapy.

Keywords: CAR-T cell; CP: Cancer; CP: Immunology; METTL3; RNA m(6)A modification; T cell infiltration; acidic microenvironment; adoptive T cell therapy; cellular immunotherapy; integrin β1; lactic acid; solid tumors.

MeSH terms

  • Cell- and Tissue-Based Therapy
  • Humans
  • Hydrogen-Ion Concentration
  • Integrin beta1* / genetics
  • Methyltransferases / genetics
  • Neoplasms*
  • T-Lymphocytes
  • Tumor Microenvironment

Substances

  • Integrin beta1
  • Methyltransferases
  • METTL3 protein, human
  • Itgb1 protein, human