Opposing Effects of cAMP and T259 Phosphorylation on Plasma Membrane Diffusion of the Water Channel Aquaporin-5 in Madin-Darby Canine Kidney Cells

PLoS One. 2015 Jul 28;10(7):e0133324. doi: 10.1371/journal.pone.0133324. eCollection 2015.

Abstract

Aquaporin-5 (AQP5) facilitates passive water transport in glandular epithelia in response to secretory stimuli via intracellular pathways involving calcium release, cAMP and protein kinase A (PKA). In epithelial plasma membranes, AQP5 may be acutely regulated to facilitate water transport in response to physiological stimuli by changes in protein modifications, interactions with proteins and lipids, nanoscale membrane domain organization, and turnover rates. Such regulatory mechanisms could potentially be associated with alteration of diffusion behavior, possibly resulting in a change in the plasma membrane diffusion coefficient of AQP5. We aimed to test the short-term regulatory effects of the above pathways, by measuring lateral diffusion of AQP5 and an AQP5 phospho-mutant, T259A, using k-space Image Correlation Spectroscopy of quantum dot- and EGFP-labeled AQP5. Elevated cAMP and PKA inhibition significantly decreased lateral diffusion of AQP5, whereas T259A mutation showed opposing effects; slowing diffusion without stimulation and increasing diffusion to basal levels after cAMP elevation. Thus, lateral diffusion of AQP5 is significantly regulated by cAMP, PKA, and T259 phosphorylation, which could be important for regulating water flow in glandular secretions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Aquaporin 5 / genetics
  • Aquaporin 5 / metabolism*
  • Cyclic AMP / genetics
  • Cyclic AMP / metabolism*
  • Cyclic AMP-Dependent Protein Kinases / genetics
  • Cyclic AMP-Dependent Protein Kinases / metabolism*
  • Dogs
  • Madin Darby Canine Kidney Cells
  • Membrane Microdomains / genetics
  • Membrane Microdomains / metabolism*
  • Mutation, Missense
  • Phosphorylation / physiology

Substances

  • Aquaporin 5
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases

Grants and funding

This work was supported by a Lundbeck Junior Group Leader Fellowship to LNN from the Lundbeck Foundation (http://www.lundbeckfoundation.com/). Additionally, this work was funded by the Graduate School of Science and Technology (GSST), AU, to JSK and SM (http://talent.au.dk/phd/scienceandtechnology/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.