Highly localized intracellular Ca2+ signals promote optimal salivary gland fluid secretion

Elife. 2021 Jul 9:10:e66170. doi: 10.7554/eLife.66170.

Abstract

Salivary fluid secretion involves an intricate choreography of membrane transporters to result in the trans-epithelial movement of NaCl and water into the acinus lumen. Current models are largely based on experimental observations in enzymatically isolated cells where the Ca2+ signal invariably propagates globally and thus appears ideally suited to activate spatially separated Cl and K channels, present on the apical and basolateral plasma membrane, respectively. We monitored Ca2+ signals and salivary secretion in live mice expressing GCamp6F, following stimulation of the nerves innervating the submandibular gland. Consistent with in vitro studies, Ca2+ signals were initiated in the apical endoplasmic reticulum. In marked contrast to in vitro data, highly localized trains of Ca2+ transients that failed to fully propagate from the apical region were observed. Following stimuli optimum for secretion, large apical-basal gradients were elicited. A new mathematical model, incorporating these data was constructed to probe how salivary secretion can be optimally stimulated by apical Ca2+ signals.

Keywords: calcium signaling; cell biology; computational biology; exocrine gland; ion channels; mouse; salivary gland secretion; systems biology.

Publication types

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

MeSH terms

  • Acinar Cells / metabolism
  • Animals
  • Calcium / metabolism
  • Calcium Signaling / physiology*
  • Computational Biology
  • Endoplasmic Reticulum / metabolism
  • Female
  • Ion Channels / metabolism
  • Male
  • Mice
  • Saliva / metabolism*
  • Salivary Glands / metabolism*
  • Salivary Glands / pathology
  • Submandibular Gland

Substances

  • Ion Channels
  • Calcium