GPR4 promotes immune exclusion in colon cancer through LOXL2-mediated extracellular matrix remodeling

Nat Commun. 2025 Dec 24;17(1):1196. doi: 10.1038/s41467-025-67967-z.

Abstract

Immune exclusion is associated with adverse prognosis in tumors, and this phenomenon may be facilitated by a physical barrier constituted by the extracellular matrix (ECM). Hypoxia and acidity promote immune exclusion, however the detailed mechanism remains unclear. This study demonstrate that G-protein-coupled-receptor-4 (GPR4), as a proton sensor, induces immune exclusion in colon cancer by promoting collagen fiber alignment and deposition. Specifically, GPR4 facilitates collagen alignment via LOXL2 regulation and enhances collagen I by modulating TGF-β, both mediated by the JAK2/STAT3 pathway. We further validate our findings in a male animal model, observing that elevated GPR4 expression in colon cancer results in an immune-excluded microenvironment. Inhibition of the JAK2/STAT3 pathway and LOXL2 function effectively reverse immune exclusion and enhance immunotherapy efficacy. Collectively, our findings elucidate a mechanism of immune exclusion and propose a potential target for improving the therapeutic efficacy of immunotherapy through the remodeling of the tumor ECM.

MeSH terms

  • Amino Acid Oxidoreductases* / genetics
  • Amino Acid Oxidoreductases* / metabolism
  • Animals
  • Cell Line, Tumor
  • Colonic Neoplasms* / genetics
  • Colonic Neoplasms* / immunology
  • Colonic Neoplasms* / metabolism
  • Colonic Neoplasms* / pathology
  • Extracellular Matrix* / immunology
  • Extracellular Matrix* / metabolism
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Immunotherapy
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Receptors, G-Protein-Coupled* / genetics
  • Receptors, G-Protein-Coupled* / metabolism
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction
  • Tumor Microenvironment / immunology

Substances

  • Amino Acid Oxidoreductases
  • Receptors, G-Protein-Coupled
  • LOXL2 protein, human
  • GPR4 protein, human
  • STAT3 Transcription Factor