The type 2 cytokine Fc-IL-4 revitalizes exhausted CD8+ T cells against cancer

Nature. 2024 Oct;634(8034):712-720. doi: 10.1038/s41586-024-07962-4. Epub 2024 Sep 25.

Abstract

Current cancer immunotherapy predominately focuses on eliciting type 1 immune responses fighting cancer; however, long-term complete remission remains uncommon1,2. A pivotal question arises as to whether type 2 immunity can be orchestrated alongside type 1-centric immunotherapy to achieve enduring response against cancer3,4. Here we show that an interleukin-4 fusion protein (Fc-IL-4), a typical type 2 cytokine, directly acts on CD8+ T cells and enriches functional terminally exhausted CD8+ T (CD8+ TTE) cells in the tumour. Consequently, Fc-IL-4 enhances antitumour efficacy of type 1 immunity-centric adoptive T cell transfer or immune checkpoint blockade therapies and induces durable remission across several syngeneic and xenograft tumour models. Mechanistically, we discovered that Fc-IL-4 signals through both signal transducer and activator of transcription 6 (STAT6) and mammalian target of rapamycin (mTOR) pathways, augmenting the glycolytic metabolism and the nicotinamide adenine dinucleotide (NAD) concentration of CD8+ TTE cells in a lactate dehydrogenase A-dependent manner. The metabolic modulation mediated by Fc-IL-4 is indispensable for reinvigorating intratumoural CD8+ TTE cells. These findings underscore Fc-IL-4 as a potent type 2 cytokine-based immunotherapy that synergizes effectively with type 1 immunity to elicit long-lasting responses against cancer. Our study not only sheds light on the synergy between these two types of immune responses, but also unveils an innovative strategy for advancing next-generation cancer immunotherapy by integrating type 2 immune factors.

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes* / drug effects
  • CD8-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes* / metabolism
  • Cell Line, Tumor
  • Female
  • Glycolysis / drug effects
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Immunoglobulin Fc Fragments* / genetics
  • Immunoglobulin Fc Fragments* / immunology
  • Immunoglobulin Fc Fragments* / metabolism
  • Immunotherapy* / methods
  • Immunotherapy, Adoptive
  • Interleukin-4* / genetics
  • Interleukin-4* / immunology
  • Interleukin-4* / pharmacology
  • Interleukin-4* / therapeutic use
  • Lactate Dehydrogenase 5 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • NAD / metabolism
  • Neoplasms* / drug therapy
  • Neoplasms* / immunology
  • Neoplasms* / therapy
  • Recombinant Fusion Proteins* / genetics
  • Recombinant Fusion Proteins* / immunology
  • Recombinant Fusion Proteins* / pharmacology
  • Recombinant Fusion Proteins* / therapeutic use
  • STAT6 Transcription Factor / metabolism
  • Signal Transduction / drug effects
  • TOR Serine-Threonine Kinases / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Immune Checkpoint Inhibitors
  • Immunoglobulin Fc Fragments
  • Interleukin-4
  • Lactate Dehydrogenase 5
  • NAD
  • Recombinant Fusion Proteins
  • STAT6 Transcription Factor
  • TOR Serine-Threonine Kinases