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CD8+ T cell priming that is required for curative intratumorally anchored anti-4-1BB immunotherapy is constrained by Tregs

Joseph R. Palmeri, Brianna M. Lax, Joshua M. Peters, Lauren Duhamel, Jordan A. Stinson, Luciano Santollani, Emi A. Lutz, William Pinney, Bryan D. Bryson, K. Dane Wittrup

2024Nature Communications19 citationsDOIOpen Access PDF

Abstract

Although co-stimulation of T cells with agonist antibodies targeting 4-1BB (CD137) improves antitumor immune responses in preclinical studies, clinical success has been limited by on-target, off-tumor activity. Here, we report the development of a tumor-anchored ɑ4-1BB agonist (ɑ4-1BB-LAIR), which consists of a ɑ4-1BB antibody fused to the collagen-binding protein LAIR. While combination treatment with an antitumor antibody (TA99) shows only modest efficacy, simultaneous depletion of CD4+ T cells boosts cure rates to over 90% of mice. Mechanistically, this synergy depends on ɑCD4 eliminating tumor draining lymph node regulatory T cells, resulting in priming and activation of CD8+ T cells which then infiltrate the tumor microenvironment. The cytotoxic program of these newly primed CD8+ T cells is then supported by the combined effect of TA99 and ɑ4-1BB-LAIR. The combination of TA99 and ɑ4-1BB-LAIR with a clinically approved ɑCTLA-4 antibody known for enhancing T cell priming results in equivalent cure rates, which validates the mechanistic principle, while the addition of ɑCTLA-4 also generates robust immunological memory against secondary tumor rechallenge. Thus, our study establishes the proof of principle for a clinically translatable cancer immunotherapy.

Topics & Concepts

Priming (agriculture)CD137Cytotoxic T cellImmunotherapyT cellCancer immunotherapyCD8Cancer researchTumor microenvironmentMedicineAntibodyImmunologyImmune systemChemistryBiologyIn vitroBiochemistryGerminationBotanyCAR-T cell therapy researchImmunotherapy and Immune ResponsesImmune Cell Function and Interaction