Enhanced tumor response to adoptive T cell therapy with PHD2/3-deficient CD8 T cells

Nat Commun. 2024 Sep 6;15(1):7789. doi: 10.1038/s41467-024-51782-z.

Abstract

While adoptive cell therapy has shown success in hematological malignancies, its potential against solid tumors is hindered by an immunosuppressive tumor microenvironment (TME). In recent years, members of the hypoxia-inducible factor (HIF) family have gained recognition as important regulators of T-cell metabolism and function. The role of HIF signalling in activated CD8 T cell function in the context of adoptive cell transfer, however, has not been explored in full depth. Here we utilize CRISPR-Cas9 technology to delete prolyl hydroxylase domain-containing enzymes (PHD) 2 and 3, thereby stabilizing HIF-1 signalling, in CD8 T cells that have already undergone differentiation and activation, modelling the T cell phenotype utilized in clinical settings. We observe a significant boost in T-cell activation and effector functions following PHD2/3 deletion, which is dependent on HIF-1α, and is accompanied by an increased glycolytic flux. This improvement in CD8 T cell performance translates into an enhancement in tumor response to adoptive T cell therapy in mice, across various tumor models, even including those reported to be extremely resistant to immunotherapeutic interventions. These findings hold promise for advancing CD8 T-cell based therapies and overcoming the immune suppression barriers within challenging tumor microenvironments.

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes* / metabolism
  • CRISPR-Cas Systems
  • Cell Line, Tumor
  • Female
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit* / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit* / metabolism
  • Hypoxia-Inducible Factor-Proline Dioxygenases* / genetics
  • Hypoxia-Inducible Factor-Proline Dioxygenases* / metabolism
  • Immunotherapy, Adoptive* / methods
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Neoplasms / genetics
  • Neoplasms / immunology
  • Neoplasms / therapy
  • Procollagen-Proline Dioxygenase
  • Tumor Microenvironment* / immunology

Substances

  • Hypoxia-Inducible Factor-Proline Dioxygenases
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Egln1 protein, mouse
  • PHD3 protein, mouse
  • Hif1a protein, mouse
  • Procollagen-Proline Dioxygenase