miR-143 Regulates Memory T Cell Differentiation by Reprogramming T Cell Metabolism

J Immunol. 2018 Oct 1;201(7):2165-2175. doi: 10.4049/jimmunol.1800230. Epub 2018 Aug 27.

Abstract

MicroRNAs are an important regulator for T cell immune response. In this study, we aimed to identify microRNAs with the potential to regulate T cell differentiation. The influence of miR-143 on differentiation and function of CD8+ T cells from healthy donors were detected, and it was found that miR-143 overexpression could significantly increase the differentiation of central memory T (Tcm) CD8+ cells, decrease cell apoptosis, and increase proinflammatory cytokine secretion. Furthermore, the specific killing of HER2-CAR T cells against esophageal cancer cell line TE-7 was enhanced by miR-143 overexpression. Glucose transporter 1 (Glut-1) was identified as the critical target gene of miR-143 in the role of T cell regulation. By inhibition Glut-1, miR-143 inhibited glucose uptake and glycolysis in T cell to regulated T cell differentiation. Tcm cell populations were also suppressed in parallel with the downregulation of miR-143 in tumor tissues from 13 patients with esophagus cancer. IDO and its metabolite kynurenine in the tumor microenvironment were screened as an upstream regulator of miR-143. IDO small interfering RNA significantly increased the expression of miR-143 and Tcm cell population. In conclusion, our results show that miR-143 enhanced antitumor effects of T cell by promoting memory T cell differentiation and metabolism reprogramming through Glut-1. Our findings will encourage the development of new strategies targeting miR-143 in both cancer cells and T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, Neoplasm / immunology
  • B-Cell Lymphoma 3 Protein
  • Blood Platelets / physiology*
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism*
  • Cell Differentiation
  • Cell Line, Tumor
  • Cellular Reprogramming
  • Cytokines / metabolism
  • Glucose Transporter Type 1 / genetics
  • Glucose Transporter Type 1 / metabolism
  • Humans
  • Immunity / genetics
  • Immunologic Memory
  • Inflammation Mediators / metabolism
  • Interleukin-1beta / metabolism
  • MicroRNAs / genetics*
  • Proto-Oncogene Proteins / metabolism
  • Transcription Factors / metabolism

Substances

  • Antigens, Neoplasm
  • B-Cell Lymphoma 3 Protein
  • BCL3 protein, human
  • Bcl3 protein, mouse
  • Cytokines
  • Glucose Transporter Type 1
  • Inflammation Mediators
  • Interleukin-1beta
  • MIRN143 microRNA, human
  • MicroRNAs
  • MIRN143 microRNA, mouse
  • Proto-Oncogene Proteins
  • Transcription Factors