Na+ influx via Orai1 inhibits intracellular ATP-induced mTORC2 signaling to disrupt CD4 T cell gene expression and differentiation

Elife. 2017 May 11:6:e25155. doi: 10.7554/eLife.25155.

Abstract

T cell effector functions require sustained calcium influx. However, the signaling and phenotypic consequences of non-specific sodium permeation via calcium channels remain unknown. α-SNAP is a crucial component of Orai1 channels, and its depletion disrupts the functional assembly of Orai1 multimers. Here we show that α-SNAP hypomorph, hydrocephalus with hopping gait, Napahyh/hyh mice harbor significant defects in CD4 T cell gene expression and Foxp3 regulatory T cell (Treg) differentiation. Mechanistically, TCR stimulation induced rapid sodium influx in Napahyh/hyh CD4 T cells, which reduced intracellular ATP, [ATP]i. Depletion of [ATP]i inhibited mTORC2 dependent NFκB activation in Napahyh/hyh cells but ablation of Orai1 restored it. Remarkably, TCR stimulation in the presence of monensin phenocopied the defects in Napahyh/hyh signaling and Treg differentiation, but not IL-2 expression. Thus, non-specific sodium influx via bonafide calcium channels disrupts unexpected signaling nodes and may provide mechanistic insights into some divergent phenotypes associated with Orai1 function.

Keywords: ATP; Foxp3 T cell; Orai; calcium channel; immunology; mTORC; mouse; sodium influx.

Publication types

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

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Animals
  • CD4 Antigens / biosynthesis*
  • CD4-Positive T-Lymphocytes / physiology
  • Cations / metabolism
  • Cell Differentiation
  • Gene Expression*
  • Mechanistic Target of Rapamycin Complex 2 / metabolism*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Signal Transduction*
  • Sodium / metabolism*
  • Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins / metabolism*
  • T-Lymphocytes, Regulatory / physiology

Substances

  • CD4 Antigens
  • Cations
  • Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins
  • Adenosine Triphosphate
  • Sodium
  • Mechanistic Target of Rapamycin Complex 2