Up-regulation of Store-operated Ca2+ Entry and Nuclear Factor of Activated T Cells Promote the Acinar Phenotype of the Primary Human Salivary Gland Cells

J Biol Chem. 2016 Apr 15;291(16):8709-20. doi: 10.1074/jbc.M115.701607. Epub 2016 Feb 22.

Abstract

The signaling pathways involved in the generation and maintenance of exocrine gland acinar cells have not yet been established. Primary human salivary gland epithelial cells, derived from salivary gland biopsies, acquired an acinar-like phenotype when the [Ca(2+)] in the serum-free medium (keratinocyte growth medium, KGM) was increased from 0.05 mm (KGM-L) to 1.2 mm (KGM-H). Here we examined the mechanism underlying this Ca(2+)-dependent generation of the acinar cell phenotype. Compared with cells in KGM-L, those in KGM-H display enhancement of Orai1, STIM1, STIM2, and nuclear factor of activated T cells 1 (NFAT1) expression together with an increase in store-operated Ca(2+) entry (SOCE), SOCE-dependent nuclear translocation of pGFP-NFAT1, and NFAT-dependent but not NFκB-dependent gene expression. Importantly, AQP5, an acinar-specific protein critical for function, is up-regulated in KGM-H via SOCE/NFAT-dependent gene expression. We identified critical NFAT binding motifs in the AQP5 promoter that are involved in Ca(2+)-dependent up-regulation of AQP5. These important findings reveal that the Ca(2+)-induced switch of salivary epithelial cells to an acinar-like phenotype involves remodeling of SOCE and NFAT signaling, which together control the expression of proteins critically relevant for acinar cell function. Our data provide a novel strategy for generating and maintaining acinar cells in culture.

Keywords: NFAT transcription factor; calcium release-activated calcium channel protein 1 (ORAI1); gene expression; stromal interaction molecule 1 (STIM1); water channel.

MeSH terms

  • Aquaporin 5 / biosynthesis
  • Aquaporin 5 / genetics
  • Calcium / metabolism*
  • Calcium Channels / biosynthesis
  • Calcium Signaling / physiology*
  • Cells, Cultured
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism*
  • Humans
  • NFATC Transcription Factors / genetics
  • NFATC Transcription Factors / metabolism*
  • Salivary Glands / cytology
  • Salivary Glands / metabolism*
  • Up-Regulation / physiology*

Substances

  • AQP5 protein, human
  • Aquaporin 5
  • Calcium Channels
  • NFATC Transcription Factors
  • NFATC2 protein, human
  • Calcium