Neurotransmitter signalling via NMDA receptors leads to decreased T helper type 1-like and enhanced T helper type 2-like immune balance in humans

Immunology. 2018 Mar;153(3):368-379. doi: 10.1111/imm.12846. Epub 2017 Nov 3.

Abstract

Given the pivotal roles that CD4+ T cell imbalance plays in human immune disorders, much interest centres on better understanding influences that regulate human helper T-cell subset dominance in vivo. Here, using primary CD4+ T cells and short-term T helper type 1 (Th1) and Th2-like lines, we investigated roles and mechanisms by which neurotransmitter receptors may influence human type 1 versus type 2 immunity. We hypothesized that N-methyl-d-aspartate receptors (NMDA-R), which play key roles in memory and learning, can also regulate human CD4+ T cell function through induction of excitotoxicity. Fresh primary CD4+ T cells from healthy donors express functional NMDA-R that are strongly up-regulated upon T cell receptor (TCR) mediated activation. Synthetic and physiological NMDA-R agonists elicited Ca2+ flux and led to marked inhibition of type 1 but not type 2 or interleukin-10 cytokine responses. Among CD4+ lines, NMDA and quinolinic acid preferentially reduced cytokine production, Ca2+ flux, proliferation and survival of Th1-like cells through increased induction of cell death whereas Th2-like cells were largely spared. Collectively, the findings demonstrate that (i) NMDA-R is rapidly up-regulated upon CD4+ T cell activation in humans and (ii) Th1 versus Th2 cell functions such as proliferation, cytokine production and cell survival are differentially affected by NMDA-R agonists. Differential cytokine production and proliferative capacity of Th1 versus Th2 cells is attributable in part to increased physiological cell death among fully committed Th1 versus Th2 cells, leading to increased Th2-like dominance. Hence, excitotoxicity, beyond its roles in neuronal plasticity, may contribute to ongoing modulation of human T cell responses.

Keywords: NMDA; CD4+ T cells; NMDA-R; Th1, Th2; glutamate; glutamic acid; human; immune regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • Cell Death / immunology
  • Cell Line
  • Cell Proliferation / physiology
  • Cytokines / immunology
  • Cytokines / metabolism
  • Humans
  • Interleukin-10 / immunology
  • Lymphocyte Activation / immunology
  • Neurotransmitter Agents / immunology
  • Neurotransmitter Agents / metabolism*
  • Receptors, Antigen, T-Cell / immunology
  • Receptors, N-Methyl-D-Aspartate / immunology
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • T-Lymphocytes, Helper-Inducer / immunology
  • T-Lymphocytes, Helper-Inducer / metabolism*
  • Th1 Cells / immunology
  • Th2 Cells / immunology
  • Th2 Cells / metabolism*
  • Up-Regulation / immunology

Substances

  • Cytokines
  • Neurotransmitter Agents
  • Receptors, Antigen, T-Cell
  • Receptors, N-Methyl-D-Aspartate
  • Interleukin-10

Grants and funding