Soluble Tim-3 serves as a tumor prognostic marker and therapeutic target for CD8+ T cell exhaustion and anti-PD-1 resistance

Cell Rep Med. 2024 Aug 20;5(8):101686. doi: 10.1016/j.xcrm.2024.101686.

Abstract

Resistance to PD-1 blockade in onco-immunotherapy greatly limits its clinical application. T cell immunoglobulin and mucin domain containing-3 (Tim-3), a promising immune checkpoint target, is cleaved by ADAM10/17 to produce its soluble form (sTim-3) in humans, potentially becoming involved in anti-PD-1 resistance. Herein, serum sTim-3 upregulation was observed in non-small cell lung cancer (NSCLC) and various digestive tumors. Notably, serum sTim-3 is further upregulated in non-responding patients undergoing anti-PD-1 therapy for NSCLC and anti-PD-1-resistant cholangiocarcinoma patients. Furthermore, sTim-3 overexpression facilitates tumor progression and confers anti-PD-1 resistance in multiple tumor mouse models. Mechanistically, sTim-3 induces terminal T cell exhaustion and attenuates CD8+ T cell response to PD-1 blockade through carcinoembryonic antigen-related cell adhesion molecule 1 (CEACAM-1). Moreover, the ADAM10 inhibitor GI254023X, which blocks sTim-3 production, reduces tumor progression in Tim-3 humanized mice and reverses anti-PD-1 resistance in human tumor-infiltrating lymphocytes (TILs). Overall, human sTim-3 holds great predictive and therapeutic potential in onco-immunotherapy.

Keywords: ADAM10; CEACAM-1; HCC; ICC; T cell exhaustion; anti-PD-1 therapy; hepatocellular carcinoma; intrahepatic cholangiocarcinoma; lung cancer; resistance to PD-1 blockade; sTim-3.

MeSH terms

  • ADAM10 Protein / metabolism
  • Animals
  • Biomarkers, Tumor* / metabolism
  • CD8-Positive T-Lymphocytes* / drug effects
  • CD8-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes* / metabolism
  • Carcinoma, Non-Small-Cell Lung / drug therapy
  • Carcinoma, Non-Small-Cell Lung / immunology
  • Carcinoma, Non-Small-Cell Lung / metabolism
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm* / drug effects
  • Female
  • Hepatitis A Virus Cellular Receptor 2* / antagonists & inhibitors
  • Hepatitis A Virus Cellular Receptor 2* / metabolism
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / immunology
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Prognosis
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / immunology
  • Programmed Cell Death 1 Receptor* / metabolism
  • T-Cell Exhaustion

Substances

  • Hepatitis A Virus Cellular Receptor 2
  • HAVCR2 protein, human
  • Programmed Cell Death 1 Receptor
  • Biomarkers, Tumor
  • Immune Checkpoint Inhibitors
  • ADAM10 Protein
  • PDCD1 protein, human