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

Author:

Takano Takahiro1,Wahl Amanda M1,Huang Kai-Ting1,Narita Takanori2ORCID,Rugis John3ORCID,Sneyd James3,Yule David I1ORCID

Affiliation:

1. Department of Pharmacology and Physiology, University of Rochester, Rochester, United States

2. Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, Fujisawa, Japan

3. Department of Mathematics, University of Auckland, Auckland, New Zealand

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.

Funder

National Institute of Dental and Craniofacial Research

Marsden Fund

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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