Critical roles of the miR-17∼92 family in thymocyte development, leukemogenesis, and autoimmunity

Cell Rep. 2024 Jun 25;43(6):114261. doi: 10.1016/j.celrep.2024.114261. Epub 2024 May 22.

Abstract

Thymocyte development requires precise control of PI3K-Akt signaling to promote proliferation and prevent leukemia and autoimmune disorders. Here, we show that ablating individual clusters of the miR-17∼92 family has a negligible effect on thymocyte development, while deleting the entire family severely impairs thymocyte proliferation and reduces thymic cellularity, phenocopying genetic deletion of Dicer. Mechanistically, miR-17∼92 expression is induced by Myc-mediated pre-T cell receptor (TCR) signaling, and miR-17∼92 promotes thymocyte proliferation by suppressing the translation of Pten. Retroviral expression of miR-17∼92 restores the proliferation and differentiation of Myc-deficient thymocytes. Conversely, partial deletion of the miR-17∼92 family significantly delays Myc-driven leukemogenesis. Intriguingly, thymocyte-specific transgenic miR-17∼92 expression does not cause leukemia or lymphoma but instead aggravates skin inflammation, while ablation of the miR-17∼92 family ameliorates skin inflammation. This study reveals intricate roles of the miR-17∼92 family in balancing thymocyte development, leukemogenesis, and autoimmunity and identifies those microRNAs (miRNAs) as potential therapeutic targets for leukemia and autoimmune diseases.

Keywords: CP: Cancer; CP: Immunology; leukemogenesis; miR-17∼92; skin inflammation; thymocyte development.

MeSH terms

  • Animals
  • Autoimmunity* / genetics
  • Carcinogenesis / genetics
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Cell Differentiation / genetics
  • Cell Proliferation
  • Leukemia* / genetics
  • Leukemia* / pathology
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • PTEN Phosphohydrolase / genetics
  • PTEN Phosphohydrolase / metabolism
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism
  • Receptors, Antigen, T-Cell / metabolism
  • Signal Transduction
  • Thymocytes* / metabolism
  • Thymocytes* / pathology

Substances

  • MicroRNAs
  • MIRN17-92 microRNA, mouse
  • PTEN Phosphohydrolase
  • Proto-Oncogene Proteins c-myc
  • Receptors, Antigen, T-Cell