Rapid aquaporin translocation regulates cellular water flow: the mechanism of hypotonicity-induced sub-cellular localization of the aquaporin 1 water channel

Matthew T. Conner, Alex C. Conner, Charlotte E. Bland, Luke H.J. Taylor, James Brown, H. Rheinallt Parri, Roslyn M. Bill

Research output: Contribution to journalArticle

Abstract

The control of cellular water flow is mediated by the aquaporin (AQP) family of membrane proteins. The family's structural features and the mechanism of selective water passage through the AQP pore are established, but there remains a gap in our knowledge of how water transport is regulated. Two broad possibilities exist. One is controlling the passage of water through the AQP pore, but this has only been observed as a phenomenon in some plant and microbial AQPs. An alternative is controlling the number of AQPs in the cell membrane. Here we describe a novel pathway in mammalian cells whereby a hypotonic stimulus directly induces intracellular calcium elevations, through transient receptor potential channels, that trigger AQP1 translocation. This translocation, which has a direct role in cell volume regulation, occurs within 30s and is dependent on calmodulin activation and phosphorylation of AQP1 at two threonine residues by protein kinase C. This direct mechanism provides a rationale for the changes in water transport that are required in response to constantly-changing local cellular water availability. Moreover, since calcium is a pluripotent and ubiquitous second messenger in biological systems, the discovery of its role in the regulation of AQP translocation has ramifications for diverse physiological and pathophysiological processes, as well as providing an explanation for the rapid regulation of water flow that is necessary for cell homeostasis.
LanguageEnglish
Pages11516-11525
Number of pages10
JournalJournal of Biological Chemistry
Volume287
Issue number14
Early online date9 Feb 2012
DOIs
Publication statusPublished - 30 Mar 2012

Fingerprint

Aquaporin 1
Aquaporins
Water
Calcium
Transient Receptor Potential Channels
Phosphorylation
Flow of water
Physiological Phenomena
Second Messenger Systems
Biological systems
Threonine
Calmodulin
Cell membranes
Protein Kinase C
Cell Size
Membrane Proteins
Chemical activation
Cells
Availability
Homeostasis

Bibliographical note

Author Choice Articles - Creative Commons Attribution Non-Commercial License

Keywords

  • aquaporins
  • calcium channels
  • cellular regulation
  • membrane trafficking
  • phosphorylation
  • water channel
  • homeostasis
  • hypotonicity

Cite this

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Rapid aquaporin translocation regulates cellular water flow : the mechanism of hypotonicity-induced sub-cellular localization of the aquaporin 1 water channel. / Conner, Matthew T.; Conner, Alex C.; Bland, Charlotte E.; Taylor, Luke H.J.; Brown, James; Parri, H. Rheinallt; Bill, Roslyn M.

In: Journal of Biological Chemistry, Vol. 287, No. 14, 30.03.2012, p. 11516-11525.

Research output: Contribution to journalArticle

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