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Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness
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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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MethodPalacios, E., & Racotta, I. S. (2007) · Aquaculture · doi:10.1016/j.aquaculture.2007.04.034 · Cited by 56
Motional Coherence in Fluid Phospholipid Membranes
Rheinstadter, M. C., Das, J., Flenner, E., Brüning, B., Seydel, T., & Kosztin, I. (2008) · Physical Review Letters · doi:10.1103/physrevlett.101.248106 · Cited by 55
Malik, A., & Claoué, C. M. P. (2012) · Contact Lens and Anterior Eye · doi:10.1016/j.clae.2012.07.005 · Cited by 54
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Macro- vs. micromolecular stabilisation of W/O/W-emulsions
Hattrem, M. N., Dille, M. J., Seternes, T., & Draget, K. I. (2013) · Food Hydrocolloids · doi:10.1016/j.foodhyd.2013.10.024 · Cited by 53
Gallová, J., Uhrı́ková, D., Islamov, A. K., Kuklin, A. I., & Balgavý, P. (2004) · PubMed · Cited by 52
A membrane transporter for tryptophan composed of RNA
Janas, T., Janas, T., & Yarus, M. (2004) · RNA · doi:10.1261/rna.7112704 · Cited by 53
“There is experimental evidence of the existence of transient, aqueous defects in membranes (Smith et al. 1984; Paula et al. 1996; Sandre et al. 1999), as well as evidence that polar molecules must traverse such routes crossing the bilayer (Paula et al. 1996).”
BackgroundKausik, R., & Han, S. (2011) · Physical Chemistry Chemical Physics · doi:10.1039/c0cp02512g · Cited by 52
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“Paula et al. (1996) examined the effect of bilayer thickness on proton permeation and concluded that transient pores could explain proton permeation behavior for lipid bilayers having up to 18 carbon acyl chains but that solubility-diffusion better predicted longer chain phospholipids.”
BackgroundProton leak and CFTR in regulation of Golgi pH in respiratory epithelial cells
Chandy, G., Grabe, M., Moore, H.-P. H., & Machen, T. E. (2001) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2001.281.3.c908 · Cited by 50
“However, our estimates of PH1 compare favorably with PH1 in lipid bilayers and liposomes: 1027-1022 cm/s (8, 21, 37 , 40).”
BackgroundResultBiomedical Implants with Charge‐Transfer Monitoring and Regulating Abilities
Wang, D., Tan, J., Zhu, H., Mei, Y., & Liu, X. (2021) · Advanced Science · doi:10.1002/advs.202004393 · Cited by 49
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Natural polyphenols: Influence on membrane transporters
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“It represents a tough barrier for most polar molecules, while enables passage of hydrophobic molecules only through passive diffusion [24].”
BackgroundUbiquinone-10 alters mechanical properties and increases stability of phospholipid membranes
Hernández, V. A., Eriksson, E. K., & Edwards, K. (2015) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2015.05.002 · Cited by 49
Electrostatics of Deformable Lipid Membranes
Vorobyov, I. V., Bekker, B., & Allen, T. W. (2010) · Biophysical Journal · doi:10.1016/j.bpj.2010.03.046 · Cited by 49
Influence of Diffusive Transport on the Structural Evolution of W/O/W Emulsions
Herzi, S., Essafi, W., Bellagha, S., & Leal‐Calderon, F. (2012) · Langmuir · doi:10.1021/la303469j · Cited by 48
Peterlin, P., & Arrigler, V. (2008) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2008.01.004 · Cited by 47
Strong Differential Monovalent Anion Selectivity in Narrow Diameter Carbon Nanotube Porins
Li, Z., Li, Y., Yao, Y., Aydin, F., Zhan, C., Chen, Y., Elimelech, M., Pham, T. A., & Noy, A. (2020) · ACS Nano · doi:10.1021/acsnano.0c02423 · Cited by 49
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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