NAD+ levels control Ca2+ store replenishment and mitogen-induced increase of cytosolic Ca2+ by Cyclic ADP-ribose-dependent TRPM2 channel gating in human T lymphocytes

J Biol Chem. 2012 Jun 15;287(25):21067-81. doi: 10.1074/jbc.M111.324269. Epub 2012 Apr 30.

Abstract

Intracellular NAD(+) levels ([NAD(+)](i)) are important in regulating human T lymphocyte survival, cytokine secretion, and the capacity to respond to antigenic stimuli. NAD(+)-derived Ca(2+)-mobilizing second messengers, produced by CD38, play a pivotal role in T cell activation. Here we demonstrate that [NAD(+)](i) modifications in T lymphocytes affect intracellular Ca(2+) homeostasis both in terms of mitogen-induced [Ca(2+)](i) increase and of endoplasmic reticulum Ca(2+) store replenishment. Lowering [NAD(+)](i) by FK866-mediated nicotinamide phosphoribosyltransferase inhibition decreased the mitogen-induced [Ca(2+)](i) rise in Jurkat cells and in activated T lymphocytes. Accordingly, the Ca(2+) content of thapsigargin-sensitive Ca(2+) stores was greatly reduced in these cells in the presence of FK866. When NAD(+) levels were increased by supplementing peripheral blood lymphocytes with the NAD(+) precursors nicotinamide, nicotinic acid, or nicotinamide mononucleotide, the Ca(2+) content of thapsigargin-sensitive Ca(2+) stores as well as cell responsiveness to mitogens in terms of [Ca(2+)](i) elevation were up-regulated. The use of specific siRNA showed that the changes of Ca(2+) homeostasis induced by NAD(+) precursors are mediated by CD38 and the consequent ADPR-mediated TRPM2 gating. Finally, the presence of NAD(+) precursors up-regulated important T cell functions, such as proliferation and IL-2 release in response to mitogens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acrylamides / pharmacology
  • Calcium / metabolism*
  • Calcium Signaling / drug effects*
  • Calcium Signaling / physiology
  • Cell Proliferation / drug effects
  • Cyclic ADP-Ribose / genetics
  • Cyclic ADP-Ribose / metabolism*
  • Cytokines / antagonists & inhibitors
  • Cytokines / genetics
  • Cytokines / metabolism
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Interleukin-2 / genetics
  • Interleukin-2 / metabolism
  • Ion Channel Gating / drug effects*
  • Ion Channel Gating / physiology
  • Jurkat Cells
  • Mitogens / pharmacology*
  • NAD / genetics
  • NAD / metabolism*
  • Nicotinamide Phosphoribosyltransferase / antagonists & inhibitors
  • Nicotinamide Phosphoribosyltransferase / genetics
  • Nicotinamide Phosphoribosyltransferase / metabolism
  • Piperidines / pharmacology
  • T-Lymphocytes / cytology
  • T-Lymphocytes / metabolism*
  • TRPM Cation Channels / genetics
  • TRPM Cation Channels / metabolism*
  • Thapsigargin / pharmacology

Substances

  • Acrylamides
  • Cytokines
  • Enzyme Inhibitors
  • IL2 protein, human
  • Interleukin-2
  • Mitogens
  • N-(4-(1-benzoylpiperidin-4-yl)butyl)-3-(pyridin-3-yl)acrylamide
  • Piperidines
  • TRPM Cation Channels
  • TRPM2 protein, human
  • NAD
  • Cyclic ADP-Ribose
  • Thapsigargin
  • Nicotinamide Phosphoribosyltransferase
  • nicotinamide phosphoribosyltransferase, human
  • Calcium