Human neonatal naive CD4+ T cells have enhanced activation-dependent signaling regulated by the microRNA miR-181a

J Immunol. 2013 Mar 15;190(6):2682-91. doi: 10.4049/jimmunol.1202534. Epub 2013 Feb 13.

Abstract

Compared with older children and adults, human neonates have reduced and delayed CD4(+) T cell immunity to certain pathogens, but the mechanisms for these developmental differences in immune function remain poorly understood. We investigated the hypothesis that impaired human neonatal CD4(+) T cell immunity was due to reduced signaling by naive CD4(+) T cells following engagement of the αβ-TCR/CD3 complex and CD28. Surprisingly, calcium flux following engagement of CD3 was significantly higher in neonatal naive CD4(+) T cells from umbilical cord blood (CB) compared with naive CD4(+) T cells from adult peripheral blood. Enhanced calcium flux was also observed in adult CD4(+) recent thymic emigrants. Neonatal naive CD4(+) T cells also had higher activation-induced Erk phosphorylation. The microRNA miR-181a, which enhances activation-induced calcium flux in murine thymocytes, was expressed at significantly higher levels in CB naive CD4(+) T cells compared with adult cells. Overexpression of miR-181a in adult naive CD4(+) T cells increased activation-induced calcium flux, implying that the increased miR-181a levels of CB naive CD4(+) T cells contributed to their enhanced signaling. In contrast, AP-1-dependent transcription, which is downstream of Erk and required for full T cell activation, was decreased in CB naive CD4(+) T cells compared with adult cells. Thus, CB naive CD4(+) T cells have enhanced activation-dependent calcium flux, indicative of the retention of a thymocyte-like phenotype. Enhanced calcium signaling and Erk phosphorylation are decoupled from downstream AP-1-dependent transcription, which is reduced and likely contributes to limitations of human fetal and neonatal CD4(+) T cell immunity.

Publication types

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

MeSH terms

  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism*
  • Calcium Signaling / genetics
  • Calcium Signaling / immunology
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Humans
  • Infant, Newborn
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology*
  • MicroRNAs / biosynthesis
  • MicroRNAs / blood*
  • MicroRNAs / genetics
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • Up-Regulation / genetics
  • Up-Regulation / immunology*

Substances

  • MIrn181 microRNA, human
  • MicroRNAs