Anti-metabolite chemotherapy increases LAG-3 expressing tumor-infiltrating lymphocytes which can be targeted by combination immune checkpoint blockade

J Immunother Cancer. 2024 Sep 28;12(9):e008568. doi: 10.1136/jitc-2023-008568.

Abstract

Background: Antibodies that target immune checkpoints such as cytotoxic T lymphocyte antigen 4 (CTLA-4), programmed cell death protein/ligand 1 (PD-1/PD-L1) are approved for treatment of multiple cancer types. Chemotherapy is often administered with immune checkpoint blockade (ICB) therapies that target CTLA-4 and/or PD-(L)1. ICB targeting other immune checkpoints such as lymphocyte activating gene-3 (LAG-3) has the potential to improve antitumor responses when combined with chemotherapy. Response to anti-PD-1 ICB is dependent on progenitor exhausted CD8+ T cells (TPEX) in the tumor, but it is unclear how chemotherapy alters TPEX proportions and phenotype.

Methods: Here we investigated whether sequential chemotherapy altered TPEX frequency and immune checkpoint expression in multiple murine tumor models.

Results: Two doses of two different anti-metabolite chemotherapies increased tumor infiltrating CD4+, and CD8+ TPEX expressing LAG-3 in multiple mouse models, which was not restricted to tumor antigen specific CD8+ T cells. To determine if LAG-3+tumor infiltrating lymphocytes (TILs) could be targeted to improve tumor control, we administered anti-LAG-3 and anti-PD-1 ICB after two doses of chemotherapy and found combination therapy generated robust antitumor responses compared with each agent alone. Both anti-LAG-3 and anti-PD-1 ICB with chemotherapy were required for the complete tumor regression observed.

Conclusions: Changes in immune checkpoint expression on TILs during chemotherapy administration informs selection of ICB therapies to combine with.

Keywords: Chemotherapy; Combination therapy; Immune checkpoint inhibitors; T-lymphocytes.

MeSH terms

  • Animals
  • Antigens, CD* / metabolism
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Cell Line, Tumor
  • Female
  • Humans
  • Immune Checkpoint Inhibitors* / pharmacology
  • Immune Checkpoint Inhibitors* / therapeutic use
  • Lymphocyte Activation Gene 3 Protein*
  • Lymphocytes, Tumor-Infiltrating* / drug effects
  • Lymphocytes, Tumor-Infiltrating* / immunology
  • Lymphocytes, Tumor-Infiltrating* / metabolism
  • Mice

Substances

  • Lymphocyte Activation Gene 3 Protein
  • Immune Checkpoint Inhibitors
  • Antigens, CD
  • Lag3 protein, mouse
  • Lag3 protein, human