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Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness
Open accessAbstract
Two mechanisms have been proposed to account for solute permeation of lipid bilayers. Partitioning into the hydrophobic phase of the bilayer, followed by diffusion, is accepted by many for the permeation of water and other small neutral solutes, but transient pores have also been proposed to account for both water and ionic solute permeation. These two mechanisms make distinctively different predictions about the permeability coefficient as a function of bilayer thickness. Whereas the solubility-diffusion mechanism predicts only a modest variation related to bilayer thickness, the pore model predicts an exponential relationship. To test these models, we measured the permeability of phospholipid bilayers to protons, potassium ions, water, urea, and glycerol. Bilayers were prepared as liposomes, and thickness was varied systematically by using unsaturated lipids with chain lengths ranging from 14 to 24 carbon atoms. The permeability coefficient of water and neutral polar solutes displayed a modest dependence on bilayer thickness, with an approximately linear fivefold decrease as the carbon number varied from 14 to 24 atoms. In contrast, the permeability to protons and potassium ions decreased sharply by two orders of magnitude between 14 and 18 carbon atoms, and leveled off, when the chain length was further extended to 24 carbon atoms. The results for water and the neutral permeating solutes are best explained by the solubility-diffusion mechanism. The results for protons and potassium ions in shorter-chain lipids are consistent with the transient pore model, but better fit the theoretical line predicted by the solubility-diffusion model at longer chain lengths.
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“Paula et al. [66] showed that the number of defects increased with decreasing membrane thickness, as might be expected.”
From The Role of Lipid Membranes in Life’s Origin (2017) · cites this paper as [66]
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“Phospholipids having 14 carbon chains were much leakier to protons and potassium ions that those with 16 and 18 carbon chains, which is the chain length that is optimal for today’s cells living at moderate temperature ranges.”
From The Role of Lipid Membranes in Life’s Origin (2017) · cites this paper as [66]
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“According to Deamer’s study (Paula et al. 1996), the permeability of vehicles was controlled by both thickness and tightness of the membranes.”
BackgroundRainsford, P., Sarre, B. R., Falavigna, M., Brandsdal, B. O., Flaten, G. E., Jakubec, M., & Isaksson, J. M. (2022) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2022.183911 · Cited by 3
Morales-Bonilla, S., Mota-Díaz, I. I., Douda, J., HERNANDEZ, A. F., Campos-López, J. P., & Torres-Torres, C. (2023) · Symmetry · doi:10.3390/sym15030775 · Cited by 3
Zhang, H.-Y., Xu, Q., & Wei, D. (2022) · Journal of Molecular Liquids · doi:10.1016/j.molliq.2022.119339 · Cited by 3
MEMBRANE BENDING IS CRITICAL FOR ASSESSING THE THERMODYNAMIC STABILITY OF PROTEINS IN THE MEMBRANE
Callenberg, K. M. (2013) · D-Scholarship@Pitt (University of Pittsburgh) · Cited by 3
Mechanism of Passive Permeation of Ions and Molecules Through Plant Membranes
Volkov, A. G., Murphy, V. A., & Markin, V. S. (2012) · Springer eBooks · doi:10.1007/978-3-642-29119-7_14 · Cited by 3
Self-citationBlume, A. (2004) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-7853-1_3 · Cited by 3
Barta, T., Sandtner, W., Wachlmayr, J., Hannesschlaeger, C., Ebert, A., Speletz, A., & Hörner, A. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.874472 · Cited by 3
Bootsveld, A., Degenhardt, R., Kamp, D., & Haest, C. W. M. (2004) · Molecular Membrane Biology · doi:10.1080/09687860400003917 · Cited by 3
Metadata
- Authors
- Paula, S., Volkov, A. G., Van Hoek, A. N., Haines, T. H., & Deamer, D. W.
- Affiliations
- City University of New York (US)
- Corresponding author
- Paula, S.
- Venue
- Biophysical Journal
- Publisher
- Elsevier BV
- Published
- 1996-01
- Volume
- 70
- Issue
- 1
- Pages
- 339-348
- ISSN
- 0006-3495 (ISSN-L)
- PMC
- PMC1224932
- OpenAlex
- W2019036104
- Cited by
- 578
- References
- 44
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 20 · 2023: 15 · 2022: 20 · 2021: 21 · 2020: 17 · 2019: 31 · 2018: 23 · 2017: 30 · 2016: 23 · 2015: 27 · 2014: 26 · 2013: 15 · 2012: 22
- FWCI
- 5.16
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biophysical Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Aeronautics and Space Administration
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Physical Sciences › Engineering › Biomedical Engineering › Nanopore and Nanochannel Transport Studies
- Keywords
- membrane permeability, phospholipid bilayers, membrane thickness, proton permeation, potassium ion permeation, water permeation, urea, glycerol, unsaturated lipids, chain length, liposomes, permeability coefficient
- MeSH terms
- Biophysics, Diffusion, Glycerol, Lipid Bilayers, Models, Chemical, Permeability, Phospholipids, Potassium, Protons, Solubility, Urea, Water, Biophysical Phenomena
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