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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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Recent Advances in the Molecular Genetics of Paramecium1
Kung, C., Saimi, Y., Haynes, W. J., Ling, K., & Kissmehl, R. (2000) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.2000.tb00003.x · Cited by 13
Characterization of the role of TMEM175 in an in vitro lysosomal H+ fluxes model
Yang, C., Tian, F., Hu, M. Y., Kang, C., Ping, M., Liu, Y., Hu, M., Xu, H., Ye, Y., Gao, Z., et al. (2023) · FEBS Journal · doi:10.1111/febs.16814 · Cited by 13
Diffusion of gases across lipid membranes with OmpA channel: a molecular dynamics study
Yuan, H., Jameson, C. J., & Murad, S. (2010) · Molecular Physics · doi:10.1080/00268976.2010.484396 · Cited by 12
Castro, O. S., Burri, L., & Nunes, A. J. P. (2017) · Aquaculture Nutrition · doi:10.1111/anu.12577 · Cited by 12
Peterlin, P., Arrigler, V., Diamant, H., & Haleva, E. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-396534-9.00010-6 · Cited by 14
“echnique to the experiment with liposomes as well. A comprehensive review of the use of liposomes in membrane permeability studies is given by de Gier [23]. Using established techniques, Paula et al. [24] did an extensive study in another attempt to resolve the standing debate between the solubility-diffusion mechanism…”
MethodFaster-than-anticipated Na+/Cl− diffusion across lipid bilayers in vesicles
Megens, M. M., Korman, C. E., Ajo-Franklin, C. M., & Horsley, D. A. (2014) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2014.05.010 · Cited by 12
Critical Swelling of Particle-Encapsulating Vesicles
Haleva, E., & Diamant, H. (2008) · Physical Review Letters · doi:10.1103/physrevlett.101.078104 · Cited by 12
Dehydration of Model Membranes Induced by Lectins from Ricinuscommunis and Viscumalbum
Pohl, P., Saparov, S. M., Pohl, E. E., Evtodienko, V. Y., Agapov, I. I., & Tonevitsky, A. (1998) · Biophysical Journal · doi:10.1016/s0006-3495(98)77729-x · Cited by 12
“According to the solubility-diffusion model for water permeation, an enhanced water concentration in the bilayer tends to increase the water permeability (Paula et al., 1996, 1998).”
Gugleva, V., Ahchiyska, K., Georgieva, D., Mihaylova, R., Konstantinov, S., Dimitrov, E., Toncheva-Moncheva, N., Rangelov, S., Foryś, A., Trzebicka, B., et al. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15102414 · Cited by 11
Perspective: Protocells and the Path to Minimal Life
Deamer, D. W. (2024) · Journal of Molecular Evolution · doi:10.1007/s00239-024-10197-6 · Cited by 13
“The primary property of amphiphilic compounds affecting permeability of the membranes they compose is the length of hydrocarbon chains and the components of their mixtures (Paula et al. 1996).”
Self-citationOroskar, P. A., Jameson, C. J., & Murad, S. (2017) · Molecular Simulation · doi:10.1080/08927022.2016.1268259 · Cited by 11
Wilson, K. A., Wang, L., & O’Mara, M. L. (2021) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.1c00395 · Cited by 11
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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