Acidity suppresses CD8 + T-cell function by perturbing IL-2, mTORC1, and c-Myc signaling

EMBO J. 2024 Nov;43(21):4922-4953. doi: 10.1038/s44318-024-00235-w. Epub 2024 Sep 16.

Abstract

CD8 + T cells have critical roles in tumor control, but a range of factors in their microenvironment such as low pH can suppress their function. Here, we demonstrate that acidity restricts T-cell expansion mainly through impairing IL-2 responsiveness, lowers cytokine secretion upon re-activation, and reduces the cytolytic capacity of CD8 + T cells expressing low-affinity TCR. We further find decreased mTORC1 signaling activity and c-Myc levels at low pH. Mechanistically, nuclear/cytoplasmic acidification is linked to mTORC1 suppression in a Rheb-, Akt/TSC2/PRAS40-, GATOR1- and Lkb1/AMPK-independent manner, while c-Myc levels drop due to both decreased transcription and higher levels of proteasome-mediated degradation. In addition, lower intracellular levels of glutamine, glutamate, and aspartate, as well as elevated proline levels are observed with no apparent impact on mTORC1 signaling or c-Myc levels. Overall, we suggest that, due to the broad impact of acidity on CD8 + T cells, multiple interventions will be required to restore T-cell function unless intracellular pH is effectively controlled.

Keywords: Acidity; CD8+ T cell; IL-2; c-Myc; mTOR.

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes* / immunology
  • CD8-Positive T-Lymphocytes* / metabolism
  • Humans
  • Hydrogen-Ion Concentration
  • Interleukin-2* / metabolism
  • Mechanistic Target of Rapamycin Complex 1* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Proto-Oncogene Proteins c-myc* / genetics
  • Proto-Oncogene Proteins c-myc* / metabolism
  • Signal Transduction*

Substances

  • Mechanistic Target of Rapamycin Complex 1
  • Proto-Oncogene Proteins c-myc
  • Interleukin-2
  • Myc protein, mouse