SHIP-1 regulates the differentiation and function of Tregs via inhibiting mTORC1 activity

Cell Mol Life Sci. 2024 Dec 21;82(1):10. doi: 10.1007/s00018-024-05470-2.

Abstract

Cell metabolism is crucial for orchestrating the differentiation and function of regulatory T cells (Tregs). However, the underlying mechanism that coordinates cell metabolism to regulate Treg activity is not completely understood. As a pivotal molecule in lipid metabolism, the role of SHIP-1 in Tregs remains unknown. In this study, we found SHIP-1 Treg KO mice (SHIP-1 specifically deleted in regulatory T cells) had severe autoimmunity with increased Tregs in the thymus and disrupted peripheral T cell homeostasis. Mechanistically, CD4Cre Ship-1flox/flox mice were found to have increased Treg precursors and SHIP-1 KO Tregs had reduced migration and stability, which caused decreased Tregs in the spleen. Additionally, the suppressive function of Tregs from SHIP-1 KO mice was diminished, along with their promotion of anti-tumor immunity. Interestingly, the PI3K-mTORC1, but not mTORC2, signaling axis was enhanced in SHIP-1 KO Tregs. In vivo treatment of SHIP-1 Treg KO mice with rapamycin rescued the abnormal Treg percentages and peripheral T cell homeostasis, as well as Treg suppressive function. Furthermore, the treatment of wild-type mice with SHIP-1 inhibitor enhanced anti-tumor activity. Our study highlights the SHIP-1-PI3K-mTORC1 axis that regulates Treg differentiation and function, and it is a potential target for cancer treatment.

Keywords: Cell metabolism; SHIP-1; Treg cells; mTOR.

MeSH terms

  • Animals
  • Autoimmunity
  • Cell Differentiation*
  • Mechanistic Target of Rapamycin Complex 1* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases* / genetics
  • Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases* / metabolism
  • Signal Transduction*
  • Sirolimus / pharmacology
  • T-Lymphocytes, Regulatory* / cytology
  • T-Lymphocytes, Regulatory* / immunology
  • T-Lymphocytes, Regulatory* / metabolism

Substances

  • Mechanistic Target of Rapamycin Complex 1
  • Phosphatidylinositol-3,4,5-Trisphosphate 5-Phosphatases
  • Phosphatidylinositol 3-Kinases
  • Sirolimus