Water Permeability of Asymmetric Planar Lipid Bilayers

Krylov, Andrey V.; Pohl, Peter; Zeidel, Mark L.; Hill, Warren G.

doi:10.1085/jgp.118.4.333

Cited by 75 publications

(42 citation statements)

References 26 publications

(48 reference statements)

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“…This approach has been used for water flux measurements through peptide channels (9, 10), water channels (11,12), lipid bilayers (13,14), and epithelial cells (15). Now we report that osmotic volume flow depletes K ϩ out of the KcsA protein.…”

mentioning

confidence: 72%

Beyond the diffusion limit: Water flow through the empty bacterial potassium channel

Saparov

Pohl

2004

Proc. Natl. Acad. Sci. U.S.A.

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100

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Water molecules are constrained to move with K ؉ ions through the narrow part of the Streptomyces lividans K ؉ channel because of the single-file nature of transport. In the presence of an osmotic gradient, a water molecule requires <10 ps to cross the purified protein reconstituted into planar bilayers. Rinsing K ؉ out of the channel, water may be 1,000 times faster than the fastest experimentally observed K ؉ ion and 20 times faster than the onedimensional bulk diffusion of water. Both the anomalously high water mobility and its inhibition observed at high K ؉ concentrations are consistent with the view that liquid-vapor oscillations occur because of geometrical confinements of water in the selectivity filter. These oscillations, where the chain of molecules imbedded in the channel (the ''liquid'') cooperatively exits the channel, leaving behind a near vacuum (the ''vapor''), thus far have only been discovered in hydrophobic nanopores by molecular dynamics simulations

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mentioning

confidence: 72%

Beyond the diffusion limit: Water flow through the empty bacterial potassium channel

Saparov

Pohl

2004

Proc. Natl. Acad. Sci. U.S.A.

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100

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“…Because membrane tightening by cholesterol and SM does not reduce membrane CO 2 permeability below 3.2 cm/s, facilitation of CO 2 membrane transport by proteinaceous molecules is virtually impossible. Here, CO 2 transport differs fundamentally from ammonia and water transport, which, in the absence of specific membrane channels, exhibit permeabilities that are orders of magnitude smaller (2,9,22).…”

Section: Discussionmentioning

confidence: 97%

“…Thus, in contrast to membrane permeabilities of water (21,22) and ammonia (2, 9, 23), membrane tightening by cholesterol and SM should not alter the apparent CO 2 permeability of 3.2 cm/s. At least three effects contribute to the reduction in membrane microviscosity (24,25).…”

mentioning

confidence: 91%

Carbon Dioxide Transport through Membranes

Missner

Kügler

Saparov

et al. 2008

Journal of Biological Chemistry

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149

212

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Several membrane channels, like aquaporin-1 (AQP1) and the RhAG protein of the rhesus complex, were hypothesized to be of physiological relevance for CO 2 transport. However, the underlying assumption that the lipid matrix imposes a significant barrier to CO 2 diffusion was never confirmed experimentally. Here we have monitored transmembrane CO 2 flux (J CO2 ) by imposing a CO 2 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 CO 2 hydration-dehydration equilibrium resulted in a relative membrane contribution of about 15% to the total resistance (pH 9.6). Under these conditions, a membrane CO 2 permeability (3.2 ؎ 1.6 cm/s) was estimated. It indicates that cellular CO 2 uptake (pH 7.4) is always USL-limited, because the USL size always exceeds 1 m. Consequently, facilitation of CO 2 transport by AQP1, RhAG, or any other protein is highly unlikely. The conclusion was confirmed by the observation that CO 2 permeability of epithelial cell monolayers was always the same whether AQP1 was overexpressed in both the apical and basolateral membranes or not.The widely accepted model that gases like NH 3 , CO 2 , and O 2 pass biological membranes by diffusion through the lipid matrix has been recently called into question. For example, the membrane protein channels AmtB and aquaporin-8 have been identified to transport NH 3 (1, 2). Protein channels such as the human aquaporin-1, the plant aquaporin NtAQP1, and the RhAG protein of the rhesus complex were reported to provide a pathway for CO 2 transport (3-5). The similarity in the findings for NH 3 and CO 2 is very surprising because Overtone's rule predicts that their permeabilities, P M , across the lipid phase of biological membranes differ 750-fold. The number was calculated assuming that NH 3 and CO 2 have comparable membrane diffusivities and that neither one of them belongs to those extremely rare exceptions from Overtone's rule (6, 7) so that the proportionality between P M and the biphasic partition coefficient (water/organic solvent) applies as shown in Equation 1,where K CO2 ϳ 1.5 (8), K NH3 ϳ 0.002 (6), and P M,NH3 ϭ 0.016 cm/s (9).A P M , CO2 of 12 cm/s suggests that the lipid matrix of biological membranes cannot act as a barrier to CO 2 diffusion. In fact, a stagnant water layer adjacent to the membrane that has the same thickness (␦) as the membrane would generate the same resistance to CO 2 flow as is caused by the membrane itself. Because these so-called unstirr...

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“…[45] This finding is easy to understand if we assume that the energy barrier offered by these membranes is about 20 kJ mol −1 larger for small molecules (as an upper limit) than of pure phosphatidyl choline membranes. [70] In this case, the aquaporin provides an energetically favourable pathway ( Figure 7). However, for CO 2 transport, the situation does not change.…”

Section: Gas Transport Through Membranes and Membrane Channelsmentioning

confidence: 99%

110 Years of the Meyer–Overton Rule: Predicting Membrane Permeability of Gases and Other Small Compounds

2009

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The transport of gaseous compounds across biological membranes is essential in all forms of life. Although it was generally accepted that gases freely penetrate the lipid matrix of biological membranes, a number of studies challenged this doctrine as they found biological membranes to have extremely low gas-permeability values. These observations led to the identification of several membrane-embedded "gas" channels, which facilitate the transport of biological active gases, such as carbon dioxide, nitric oxide, and ammonia. However, some of these findings are in contrast to the well-established solubility-diffusion model (also known as the Meyer-Overton rule), which predicts membrane permeabilities from the molecule's oil-water partition coefficient. Herein, we discuss recently reported violations of the Meyer-Overton rule for small molecules, including carboxylic acids and gases, and show that Meyer and Overton continue to rule.

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Water Permeability of Asymmetric Planar Lipid Bilayers

Cited by 75 publications

References 26 publications

Beyond the diffusion limit: Water flow through the empty bacterial potassium channel

Beyond the diffusion limit: Water flow through the empty bacterial potassium channel

Carbon Dioxide Transport through Membranes

110 Years of the Meyer–Overton Rule: Predicting Membrane Permeability of Gases and Other Small Compounds

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