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J. Biol. Chem., Vol. 283, Issue 37, 25340-25347, September 12, 2008

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Carbon Dioxide Transport through Membranes^*

Andreas Missner, Philipp Kügler^¶, Sapar M. Saparov, Klaus Sommer, John C. Mathai^||, Mark L. Zeidel^||, and Peter Pohl¹

From the Institut für Biophysik and Institut für Industriemathematik, Johannes Kepler Universität, Linz A-4040, Austria, ^¶Johan Radon Institute for Computational and Applied Mathematics, Austrian Academy of Sciences, Linz A-4040, Austria, and ^||Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts 02215

Several membrane channels, like aquaporin-1 (AQP1) and the RhAG protein of the rhesus complex, were hypothesized to be of physiological relevance for CO₂ transport. However, the underlying assumption that the lipid matrix imposes a significant barrier to CO₂ diffusion was never confirmed experimentally. Here we have monitored transmembrane CO₂ flux (J_CO2) by imposing a CO₂ concentration gradient across planar lipid bilayers and detecting the resulting small pH shift in the immediate membrane vicinity. An analytical model, which accounts for the presence of both carbonic anhydrase and buffer molecules, was fitted to the experimental pH profiles using inverse problems techniques. At pH 7.4, the model revealed that J_CO2 was entirely rate-limited by near-membrane unstirred layers (USL), which act as diffusional barriers in series with the membrane. Membrane tightening by sphingomyelin and cholesterol did not alter J_CO2 confirming that membrane resistance was comparatively small. In contrast, a pH-induced shift of the CO₂ hydration-dehydration equilibrium resulted in a relative membrane contribution of about 15% to the total resistance (pH 9.6). Under these conditions, a membrane CO₂ permeability (3.2 ± 1.6 cm/s) was estimated. It indicates that cellular CO₂ uptake (pH 7.4) is always USL-limited, because the USL size always exceeds 1 µm. Consequently, facilitation of CO₂ transport by AQP1, RhAG, or any other protein is highly unlikely. The conclusion was confirmed by the observation that CO₂ permeability of epithelial cell monolayers was always the same whether AQP1 was overexpressed in both the apical and basolateral membranes or not.

Received for publication, January 4, 2008 , and in revised form, June 27, 2008.

^* This work was supported, in whole or in part, by National Institutes of Health Grants DK43955 and DK048217 (to M. Z. L. and J. C. M.). This work was also supported by Austrian Science Fund FWF W1201-N13 (to P. P.). 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.

¹ To whom correspondence should be addressed: Altenbergerstr. 69, A-4040 Linz, Austria. Fax: 43-732-2468-9269; E-mail: peter.pohl{at}jku.at.

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