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Am J Physiol Cell Physiol (August 17, 2005). doi:10.1152/ajpcell.00211.2005
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Submitted on May 3, 2005
Accepted on July 2, 2005

Identification of aquaporin-5 in lipid rafts and its translocation to apical membranes by the activation of M3-muscarinic acetylcholine receptors in the interlobular ducts of rat parotid glands

Yasuko Ishikawa1*, Zhenfang Yuan1, Noriko Inoue1, Mariusz T Skowronski2, Yoshiko Nakae3, Masayuki Shono4, Gota Cho5, Masato Yasui6, Peter Agre6, and Soren Nielsen2

1 Medical Pharmacology, The University of Tokushima Graduate Schoo, Tokushima, Japan
2 The Water and Salt Research Center and Institute of Anatomy, University of Aarhus, Aarhus, Denmark
3 Oral and Maxillofacial Anatomy, The University of Tokushima Graduate Schoo, Tokushima, Japan
4 Support Center for Advanced Medical Sciences, The University of Tokushima Graduate Schoo, Tokushima, Japan
5 Dental Anesthesiology, The University of Tokushima Graduate Schoo, Tokushima, Japan
6 Biological Chemistry and Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA

* To whom correspondence should be addressed. E-mail: isikawa{at}dent.tokushima-u.ac.jp.

Aquaporin 5 (AQP5), an apical plasma membrane (APM) water channel in salivary glands, lacrimal glands, and airway epithelium, has an important role in fluid secretion. M3 muscarinic acetylcholine receptor (mAChR)-induced changes in AQP5 localization in rat parotid glands was investigated using immunofluorescence or immunoelectron microscopy, detergent solubility, and gradient density floatation assays. Confocal microscopy revealed AQP5 localization in intracellular vesicles of interlobular duct cells in rat parotid glands and AQP5 trafficking to the APM 10 min after injection of the mACh agonist cevimeline. Conversely, 60 min after injection, there was a diffuse pattern of AQP5 staining in the cell cytoplasm. The calcium ionophore A23187 mimicked the effects of cevimeline. Immunoelectron microscopic studies confirmed that cevimeline induced AQP5 trafficking from intracellular structures to APMs in the interlobular duct cells of rat parotid glands. Lipid raft markers, flotillin-2 and GM1, co-localized with AQP5 and moved with AQP5 in response to cevimeline. Under control conditions, the majority of AQP5 localized in the Triton X -100-insoluble fraction and floated to the light-density fraction on discontinuous density gradients. After 10-min incubation of parotid tissue slices with cevimeline or A23187, the AQP5 levels decreased in the Triton X-100-insoluble fraction and increased in the Triton X -100-soluble fraction. Thus, AQP5 localizes in the intracellular lipid rafts and M3 mAChR activation induces AQP5 trafficking to the APM with lipid rafts via intracellular calcium signaling and induces AQP5 dissociation from lipid rafts to non-rafts on the APM in the interlobular duct cells of rat parotid glands.




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