Activation of miR-21-Regulated Pathways in Immune Aging Selects against Signatures Characteristic of Memory T Cells

Cell Rep. 2018 Nov 20;25(8):2148-2162.e5. doi: 10.1016/j.celrep.2018.10.074.

Abstract

Induction of protective vaccine responses, governed by the successful generation of antigen-specific antibodies and long-lived memory T cells, is increasingly impaired with age. Regulation of the T cell proteome by a dynamic network of microRNAs is crucial to T cell responses. Here, we show that activation-induced upregulation of miR-21 biases the transcriptome of differentiating T cells away from memory T cells and toward inflammatory effector T cells. Such a transcriptome bias is also characteristic of T cell responses in older individuals who have increased miR-21 expression and is reversed by antagonizing miR-21. miR-21 targets negative feedback circuits in several signaling pathways. The concerted, sustained activity of these signaling pathways in miR-21high T cells disfavors the induction of transcription factor networks involved in memory cell differentiation. Our data suggest that curbing miR-21 upregulation or activity in older individuals may improve their ability to mount effective vaccine responses.

Keywords: T cell differentiation; T memory cell; immune aging; immunosenescence; microRNA; short-lived T effector cell; vaccination.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Aging / genetics*
  • Aging / immunology*
  • Apoptosis Regulatory Proteins / metabolism
  • Cell Differentiation / genetics
  • Gene Expression Regulation*
  • HEK293 Cells
  • Humans
  • Immunologic Memory / genetics*
  • Lymphocyte Activation / genetics
  • MAP Kinase Signaling System
  • Membrane Proteins / metabolism
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Middle Aged
  • PTEN Phosphohydrolase / metabolism
  • Phosphoproteins / metabolism
  • RNA-Binding Proteins / metabolism
  • T-Lymphocytes / cytology
  • T-Lymphocytes / metabolism*
  • TOR Serine-Threonine Kinases / metabolism
  • Transcription Factor AP-1 / metabolism
  • Young Adult

Substances

  • Apoptosis Regulatory Proteins
  • MIRN21 microRNA, human
  • Membrane Proteins
  • MicroRNAs
  • PDCD4 protein, human
  • Phosphoproteins
  • RNA-Binding Proteins
  • SPRY1 protein, human
  • Transcription Factor AP-1
  • TOR Serine-Threonine Kinases
  • PTEN Phosphohydrolase