<p>Cell cycle-inhibiting chemotherapeutics are widely used in cancer treatment. Although the primary aim is to block tumor cell proliferation, their clinical efficacy also involves specific effector CD8<sup>+</sup> T cells that undergo synchronized proliferation and differentiation. How CD8<sup>+</sup> T cells are programmed when these processes are uncoupled, as occurs during cell cycle inhibition, is unclear. Here, we show that activated CD8<sup>+</sup> T cells arrested in their cell cycle can still undergo effector differentiation. Cell cycle-arrested CD8<sup>+</sup> T cells become metabolically reprogrammed into a highly energized state, enabling rapid and enhanced proliferation upon release from arrest. This metabolic imprinting is driven by increased nutrient uptake, storage and processing, leading to enhanced glycolysis in cell cycle-arrested cells. The nutrient sensible mTORC1 pathway, however, was not crucial. Instead, elevated interleukin-2 production during arrest activates STAT5 signaling, which supports expansion of the energized CD8<sup>+</sup> T cells following arrest. Transient arrest in vivo enables superior CD8<sup>+</sup> T cell-mediated tumor control across models of immune checkpoint blockade, adoptive cell transfer and therapeutic vaccination. Thus, transient uncoupling of CD8<sup>+</sup> T cell differentiation from cell cycle progression programs a favorable metabolic state that supports the efficacy of effector T cell-mediated immunotherapies.</p>

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Cell cycle arrest enhances CD8+ T cell effector function by potentiating glucose metabolism and IL-2 signaling

  • Floortje J. van Haften,
  • Tetje C. van der Sluis,
  • Hanna S. Hepp,
  • Nils Mülling,
  • Reza Nadafi,
  • Bharath Sampadi,
  • Suzanne van Duikeren,
  • J. Shirin Mostert,
  • Rosemarijn van der Sterre,
  • Peter A. van Veelen,
  • Graham A. Heieis,
  • Dominique M. B. Veerkamp,
  • Thomas H. Wesselink,
  • Ward Vleeshouwers,
  • Macha Beijnes,
  • Iris N. Pardieck,
  • Eralin L. F. van Horssen,
  • Anne F. de Groot,
  • Manon van der Ploeg,
  • Judith R. Kroep,
  • Noel F. C. C. de Miranda,
  • Sabina Y. van der Zanden,
  • Jacques Neefjes,
  • Hailiang Mei,
  • Alfred C. O. Vertegaal,
  • Bart Everts,
  • Sjoerd H. van der Burg,
  • Ramon Arens

摘要

Cell cycle-inhibiting chemotherapeutics are widely used in cancer treatment. Although the primary aim is to block tumor cell proliferation, their clinical efficacy also involves specific effector CD8+ T cells that undergo synchronized proliferation and differentiation. How CD8+ T cells are programmed when these processes are uncoupled, as occurs during cell cycle inhibition, is unclear. Here, we show that activated CD8+ T cells arrested in their cell cycle can still undergo effector differentiation. Cell cycle-arrested CD8+ T cells become metabolically reprogrammed into a highly energized state, enabling rapid and enhanced proliferation upon release from arrest. This metabolic imprinting is driven by increased nutrient uptake, storage and processing, leading to enhanced glycolysis in cell cycle-arrested cells. The nutrient sensible mTORC1 pathway, however, was not crucial. Instead, elevated interleukin-2 production during arrest activates STAT5 signaling, which supports expansion of the energized CD8+ T cells following arrest. Transient arrest in vivo enables superior CD8+ T cell-mediated tumor control across models of immune checkpoint blockade, adoptive cell transfer and therapeutic vaccination. Thus, transient uncoupling of CD8+ T cell differentiation from cell cycle progression programs a favorable metabolic state that supports the efficacy of effector T cell-mediated immunotherapies.