Landscape of tumoral ecosystem for enhanced anti-PD-1 immunotherapy by gut Akkermansia muciniphila

Cell Rep. 2024 Jun 25;43(6):114306. doi: 10.1016/j.celrep.2024.114306. Epub 2024 May 30.

Abstract

Gut Akkermansia muciniphila (Akk) has been implicated in impacting immunotherapy or oncogenesis. This study aims to dissect the Akk-associated tumor immune ecosystem (TIME) by single-cell profiling coupled with T cell receptor (TCR) sequencing. We adopted mouse cancer models under anti-PD-1 immunotherapy, combined with oral administration of three forms of Akk, including live Akk, pasteurized Akk (Akk-past), or its membrane protein Amuc_1100 (Amuc). We show that live Akk is most effective in activation of CD8 T cells by rescuing the exhausted type into cytotoxic subpopulations. Remarkably, only live Akk activates MHC-II-pDC pathways, downregulates CXCL3 in Bgn(+)Dcn(+) cancer-associated fibroblasts (CAFs), blunts crosstalk between Bgn(+)Dcn(+) CAFs and PD-L1(+) neutrophils by a CXCL3-PD-L1 axis, and further suppresses the crosstalk between PD-L1(+) neutrophils and CD8 T cells, leading to the rescue of exhausted CD8 T cells. Together, this comprehensive picture of the tumor ecosystem provides deeper insights into immune mechanisms associated with gut Akk-dependent anti-PD-1 immunotherapy.

Keywords: CP: Cancer; CP: Immunology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Akkermansia*
  • Animals
  • B7-H1 Antigen / metabolism
  • CD8-Positive T-Lymphocytes* / immunology
  • Gastrointestinal Microbiome / drug effects
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Immunotherapy* / methods
  • Mice
  • Mice, Inbred C57BL
  • Neoplasms* / immunology
  • Neoplasms* / therapy
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / metabolism
  • Receptors, CXCR3 / metabolism
  • Tumor Microenvironment

Substances

  • B7-H1 Antigen
  • Immune Checkpoint Inhibitors
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • Receptors, CXCR3

Supplementary concepts

  • Akkermansia muciniphila