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Rapid aquaporin translocation regulates cellular water flow: Mechanism of hypotonicity-induced subcellular localization of aquaporin 1 water channel

Conner, MT
Conner, AC
Bland, CE
Taylor, LHJ
Brown, JEP
Parri, HR
Bill, RM
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Abstract
The control of cellular water flow is mediated by the aquaporin (AQP) family of membrane proteins. The structural features of the family 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 only has 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, which trigger AQP1 translocation. This translocation, which has a direct role in cell volume regulation, occurs within 30 s 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, because 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. © 2012 by The American Society for Biochemistry and Molecular Biology, Inc.
Citation
Conner, M. T., Conner, Alex C., Bland, C. E., Taylor, Luke H. J., Brown, J. E. P., Parri, H. R. and Bill, R. M. (2012) Rapid aquaporin translocation regulates cellular water flow : Mechanism of hypotonicity-induced subcellular localization of aquaporin 1 water channel. Journal of Biological Chemistry, Vol.287 (No.14). pp. 11516-11525. doi:10.1074/jbc.M111.329219
Research Unit
PubMed ID
22334691 (pubmed)
PubMed Central ID
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Journal article
Language
en
Description
This is an accepted manuscript of an article published by American Society for Biochemistry and Molecular Biology in Journal of Biological Chemistry on 09/02/2012, available online; https://www.jbc.org/content/287/14/11516 The accepted version of the publication may differ from the final published version.
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ISSN
0021-9258
EISSN
1083-351X
ISBN
ISMN
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Sponsors
This work was supported by European Commission Framework Programme 7 Grant 201924 EDICT (to R. M. B.).
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Licence for published version: Creative Commons Attribution-NonCommercial 4.0 International
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