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J. Biol. Chem., Vol. 280, Issue 5, 3590-3596, February 4, 2005

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cAMP Has Distinct Acute and Chronic Effects on Aquaporin-5 in Lung Epithelial Cells^*

Venkataramana Sidhaye, Jason D. Hoffert, and Landon S. King¶||

From the Department of Medicine, Division of Pulmonary and Critical Care Medicine, and the ^¶Department of Biological Chemistry, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21224 and the Laboratory of Kidney and Electrolyte Metabolism, NHLBI, National Institutes of Health, Bethesda, Maryland 20892

Aquaporin-5 (AQP5) is present on the apical membrane of epithelial cells in various secretory glands as well as on the apical membrane of the airway epithelium, airway submucosal glands, and type 1 pneumocytes, where it can participate in respiratory tract water homeostasis. We examined the effects of cAMP on AQP5 distribution and abundance. When AQP5-expressing mouse lung epithelial cells were treated with cAMP or the -adrenergic agonist terbutaline, a biphasic AQP5 response was observed. Short term (minutes) exposure to cAMP produced internalization of AQP5 off of the membrane and a decrease in protein abundance. Both of these responses were blocked by inhibition of protein kinase A and the decrease in abundance was blocked by chloroquine, indicating lysosome-mediated degradation. Sustained cAMP exposure (hours) produced an increase in membrane localization and increased abundance; these effects were also blocked by protein kinase A inhibition. The -adrenergic agonist terbutaline produced changes in AQP5 abundance in mouse trachea and lung, consistent with our findings in cultured epithelial cells. Purified AQP5 protein was phosphorylated by protein kinase A but not protein kinase C or casein kinase II, and aquaporin-5 was phosphorylated in cultured cells after long term (but not short term) exposure to cAMP. These studies indicate that cAMP and -adrenergic agonists produce distinct short and long term effects on AQP5 distribution and abundance that may contribute to regulation of lung water homeostasis.

Received for publication, September 24, 2004 , and in revised form, November 5, 2004.

^* This work was supported by NHLBI, National Institutes of Health Grants F32-HL074515 (National Research Service Award) (to V. S.) and R01-HL70217 and by American Heart Association Grant-in-aid AHA-0255234N (to L. S. K.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| To whom correspondence should be addressed: Johns Hopkins Asthma and Allergy Center 4B.64, 5501 Hopkins Bayview Circle, Baltimore, MD 21224. Tel.: 410-550-1224; Fax: 410-550-2612; E-mail: lsking{at}jhmi.edu.

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