A microbiota-modulated checkpoint directs immunosuppressive intestinal T cells into cancers

Science. 2023 Jun 9;380(6649):eabo2296. doi: 10.1126/science.abo2296. Epub 2023 Jun 9.

Abstract

Antibiotics (ABX) compromise the efficacy of programmed cell death protein 1 (PD-1) blockade in cancer patients, but the mechanisms underlying their immunosuppressive effects remain unknown. By inducing the down-regulation of mucosal addressin cell adhesion molecule 1 (MAdCAM-1) in the ileum, post-ABX gut recolonization by Enterocloster species drove the emigration of enterotropic α4β7+CD4+ regulatory T 17 cells into the tumor. These deleterious ABX effects were mimicked by oral gavage of Enterocloster species, by genetic deficiency, or by antibody-mediated neutralization of MAdCAM-1 and its receptor, α4β7 integrin. By contrast, fecal microbiota transplantation or interleukin-17A neutralization prevented ABX-induced immunosuppression. In independent lung, kidney, and bladder cancer patient cohorts, low serum levels of soluble MAdCAM-1 had a negative prognostic impact. Thus, the MAdCAM-1-α4β7 axis constitutes an actionable gut immune checkpoint in cancer immunosurveillance.

MeSH terms

  • Animals
  • Anti-Bacterial Agents* / adverse effects
  • Bacteria / immunology
  • Cell Adhesion Molecules* / metabolism
  • Cell Movement
  • Drug Resistance, Neoplasm*
  • Fecal Microbiota Transplantation
  • Gastrointestinal Microbiome* / immunology
  • Gastrointestinal Tract / immunology
  • Gastrointestinal Tract / microbiology
  • Humans
  • Immune Checkpoint Inhibitors* / therapeutic use
  • Immune Tolerance* / drug effects
  • Immunologic Surveillance*
  • Integrins* / metabolism
  • Interleukin-17 / metabolism
  • Mice
  • Mucoproteins* / metabolism
  • Neoplasms* / immunology
  • Neoplasms* / therapy
  • Th17 Cells / immunology

Substances

  • Anti-Bacterial Agents
  • Cell Adhesion Molecules
  • Immune Checkpoint Inhibitors
  • integrin alpha4beta7
  • Integrins
  • Interleukin-17
  • MADCAM1 protein, human
  • Mucoproteins