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J. Biol. Chem., Vol. 278, Issue 50, 50163-50174, December 12, 2003

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Cell Swelling Stimulates Cytosol to Membrane Transposition of ICln^*

Markus Ritter, Andrea Ravasio, Martin Jakab, Sabine Chwatal, Johannes Fürst, Andreas Laich, Martin Gschwentner, Sara Signorelli, Carmen Burtscher, Sonja Eichmüller, and Markus Paulmichl¶||

From the Department of Physiology, University of Innsbruck, Fritz-Pregl-Strasse 3, A-6020 Innsbruck, Austria and the ^¶Department of Biomolecular Science and Biotechnology, Università degli Studi di Milano, Via Celoria 26, I-20133 Milan, Italy

ICln is a multifunctional protein that is essential for cell volume regulation. It can be found in the cytosol and is associated with the cell membrane. Besides its role in the splicing process, ICln is critically involved in the generation of ion currents activated during regulatory volume decrease after cell swelling (RVDC). If reconstituted in artificial bilayers, ICln can form ion channels with biophysical properties related to RVDC. We investigated (i) the cytosol versus cell membrane distribution of ICln in rat kidney tubules, NIH 3T3 fibroblasts, Madin-Darby canine kidney (MDCK) cells, and LLC-PK₁ epithelial cells, (ii) fluorescence resonance energy transfer (FRET) in living fibroblasts between fluorescently tagged ICln and fluorochromes in the cell membrane, and (iii) possible functional consequences of an enhanced ICln presence at the cell membrane. We demonstrate that ICln distribution in rat kidneys depends on the parenchymal localization and functional state of the tubules and that cell swelling causes ICln redistribution from the cytosol to the cell membrane in NIH 3T3 fibroblasts and LLC-PK₁ cells. The addition of purified ICln protein to the extracellular solution or overexpression of farnesylated ICln leads to an increased anion permeability in NIH 3T3 fibroblasts. The swelling-induced redistribution of ICln correlates to altered kinetics of RVDC in NIH 3T3 fibroblasts, LLC-PK₁ cells, and MDCK cells. In these cells, RVDC develops more rapidly, and in MDCK cells the rate of swelling-induced depolarization is accelerated if cells are swollen for a second time. This coincides with an enhanced ICln association with the cell membrane.

Received for publication, January 13, 2003 , and in revised form, September 8, 2003.

^* This article was supported in part by the Austrian Science Foundation (FWF, Grants P12337, P13041, P12467, and P14102Med), the Austrian National Bank (Grants 8444 and 6994), and the Gastein Foundation (Grant FP41/FP46) (to M. P. and M. R.). 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 may be addressed. Tel.: 43-512-507-3766; Fax: 43-512-507-2853; E-mail: markus.ritter{at}uibk.ac.at. || To whom correspondence may be addressed. Tel.: 43-512-507-3756; Fax: 43-512-577-656; E-mail: markus.paulmichl{at}uibk.ac.at.

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