Chimeric antigen receptor dendritic cells targeted delivery of a single tumoricidal factor for cancer immunotherapy

Cancer Immunol Immunother. 2024 Aug 6;73(10):203. doi: 10.1007/s00262-024-03788-1.

Abstract

Background: Chimeric antigen receptor (CAR)-T cells have been used to treat blood cancers by producing a wide variety of cytokines. However, they are not effective in treating solid cancers and can cause severe side-effects, including cytokine release syndrome. TNFα is a tumoricidal cytokine, but it markedly increases the protein levels of cIAP1 and cIAP2, the members of inhibitor of apoptosis protein (IAP) family of E3 ubiquitin ligase that limits caspase-induced apoptosis. Degradation of IAP proteins by an IAP antagonist does not effectively kill cancer cells but enables TNFα to strongly induce cancer cell apoptosis. It would be a promising approach to treat cancers by targeted delivery of TNFα through an inactive adoptive cell in combination with an IAP antagonist.

Methods: Human dendritic cells (DCs) were engineered to express a single tumoricidal factor, TNFα, and a membrane-anchored Mucin1 antibody scFv, named Mucin 1 directed DCs expressing TNFα (M-DCsTNF). The efficacy of M-DCsTNF in recognizing and treating breast cancer was tested in vitro and in vivo.

Results: Mucin1 was highly expressed on the surface of a wide range of human breast cancer cell lines. M-DCsTNF directly associated with MDA-MB-231 cells in the bone of NSG mice. M-DCsTNF plus an IAP antagonist, SM-164, but neither alone, markedly induce MDA-MB-231 breast cancer cell apoptosis, which was blocked by TNF antibody. Importantly, M-DCsTNF combined with SM-164, but not SM-164 alone, inhibited the growth of patient-derived breast cancer in NSG mice.

Conclusion: An adoptive cell targeting delivery of TNFα combined with an IAP antagonist is a novel effective approach to treat breast cancer and could be expanded to treat other solid cancers. Unlike CAR-T cell, this novel adoptive cell is not activated to produce a wide variety of cytokines, except for additional overexpressed TNF, and thus could avoid the severe side effects such as cytokine release syndrome.

Keywords: Breast cancer; Chimeric antigen receptor (CAR) cell therapy; Dendritic cell (DC); IAP antagonist; Inhibitor of apoptosis proteins (IAPs); Mucin1; Patient-derived xenograft (PDX) model; Tumor necrosis factor-α (TNF).

MeSH terms

  • Animals
  • Apoptosis
  • Breast Neoplasms / immunology
  • Breast Neoplasms / therapy
  • Cell Line, Tumor
  • Dendritic Cells* / immunology
  • Dendritic Cells* / metabolism
  • Female
  • Humans
  • Immunotherapy / methods
  • Immunotherapy, Adoptive / methods
  • Inhibitor of Apoptosis Proteins / antagonists & inhibitors
  • Inhibitor of Apoptosis Proteins / metabolism
  • Mice
  • Mice, SCID
  • Mucin-1 / immunology
  • Mucin-1 / metabolism
  • Neoplasms / immunology
  • Neoplasms / therapy
  • Receptors, Chimeric Antigen* / immunology
  • Tumor Necrosis Factor-alpha* / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Receptors, Chimeric Antigen
  • Tumor Necrosis Factor-alpha
  • Mucin-1
  • Inhibitor of Apoptosis Proteins
  • MUC1 protein, human