Personalized neoantigen hydrogel vaccine combined with PD-1 and CTLA-4 double blockade elicits antitumor response in liver metastases by activating intratumoral CD8+CD69+ T cells

J Immunother Cancer. 2024 Dec 18;12(12):e009543. doi: 10.1136/jitc-2024-009543.

Abstract

Background: Liver metastasis is highly aggressive and immune tolerant, and lacks effective treatment strategies. This study aimed to develop a neoantigen hydrogel vaccine (NPT-gels) with high clinical feasibility and further investigate its efficacy and antitumor molecular mechanisms in combination with immune checkpoint inhibitors (ICIs) for the treatment of liver metastases.

Methods: The effects of liver metastasis on survival and intratumor T-cell subpopulation infiltration in patients with advanced tumors were investigated using the Surveillance, Epidemiology, and End Results Program (SEER) database and immunofluorescence staining, respectively. NPT-gels were prepared using hyaluronic acid, screened neoantigen peptides, and dual clinical adjuvants [Poly(I:C) and thymosin α-1]. Then, the efficacy and corresponding antitumor molecular mechanisms of NPT-gels combined with programmed death receptor 1 and cytotoxic T-lymphocyte-associated protein 4 double blockade (PCDB) for the treatment of liver metastases were investigated using various preclinical liver metastasis models.

Results: Liver metastases are associated with poorer 5-year overall survival, characterized by low infiltration of cytotoxic CD8+ T cells and high infiltration of regulatory T cells (Tregs). NPT-gels overcame the challenges faced by conventional neoantigen peptide vaccines by sustaining a durable, high-intensity immune response with a single injection and significantly improving the infiltration of neoantigen-specific T-cell subpopulations in different mice subcutaneous tumor models. Importantly, NPT-gels further combined with PCDB could enhance neoantigen-specific T-cell infiltration and effectively unlock the immunosuppressive microenvironment of liver metastases, showing superior antitumor efficacy and inducing long-term immune memory in various preclinical liver metastasis models without obvious toxicity. Mechanistically, the combined strategy can inhibit Tregs, induce the production and infiltration of neoantigen-specific CD8+CD69+ T cells to enhance the immune response, and potentially elicit antigen-presenting effects in Naïve B_Ighd+ cells and M1-type macrophages.

Conclusions: This study demonstrated that NPT-gels combined with PCDB could exert a durable and powerful antitumor immunity by enhancing the recruitment and activation of CD8+CD69+ T cells, which supports the rationale and clinical translation of this combination strategy and provides important evidence for further improving the immunotherapy efficacy of liver metastases in the future.

Keywords: T cell; T regulatory cell - Treg; immune checkpoint inhibitor; immunotherapy; vaccine.

MeSH terms

  • Animals
  • Antigens, Neoplasm / immunology
  • CD8-Positive T-Lymphocytes* / immunology
  • CTLA-4 Antigen* / antagonists & inhibitors
  • CTLA-4 Antigen* / immunology
  • Cancer Vaccines* / administration & dosage
  • Cancer Vaccines* / immunology
  • Cancer Vaccines* / therapeutic use
  • Female
  • Humans
  • Hydrogels / therapeutic use
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Liver Neoplasms* / immunology
  • Liver Neoplasms* / secondary
  • Male
  • Mice
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / immunology

Substances

  • Cancer Vaccines
  • Programmed Cell Death 1 Receptor
  • CTLA-4 Antigen
  • Immune Checkpoint Inhibitors
  • Hydrogels
  • Antigens, Neoplasm