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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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Collective Dynamics of Lipid Membranes Studied by Inelastic Neutron Scattering
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Saito, H., & Shinoda, W. (2011) · The Journal of Physical Chemistry B · doi:10.1021/jp201611p · Cited by 134
Jash, A., Ubeyitogullari, A., & Rizvi, S. S. H. (2021) · Journal of Materials Chemistry B · doi:10.1039/d1tb00126d · Cited by 139
Paula, S., Volkov, A. G., & Deamer, D. W. (1998) · Biophysical Journal · doi:10.1016/s0006-3495(98)77789-6 · Cited by 135
“…characteristics correctly by accounting for the dependence ofP on bilayer thickness and by explaining how an increase in the unhydrated ionic radius effectsP. study, we will also consider earlier results obtained for potassium permeation in identical bilayer systems (Paula et al., 1996).”
BackgroundMethodResultInfluentialSelf-citationBennett, W. F., & Tieleman, D. P. (2011) · Journal of Chemical Theory and Computation · doi:10.1021/ct200291v · Cited by 135
Komatsu, H., & Chong, P. L. (1998) · Biochemistry · doi:10.1021/bi972163e · Cited by 130
Pathways and Challenges for Biomimetic Desalination Membranes with Sub-Nanometer Channels
Porter, C. J., Werber, J. R., Zhong, M., Wilson, C. J., & Elimelech, M. (2020) · ACS Nano · doi:10.1021/acsnano.0c05753 · Cited by 129
Membrane Transport in Primitive CellsPreprint
Mansy, S. S. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002188 · Cited by 130
“Permeability coefficients versus membrane thickness data for Naþ and Kþwere consistent with a transient pore model rather than a solubility-diffusion model for phospholipids with short acyl chains, whereas acyl chains "18 carbons, showed permeation consistent with the solubility-diffusion model, particularly for anion…”
BackgroundMethodGuo, Y., Terazzi, E., Seemann, R., Fleury, J., & Baulin, V. A. (2016) · Science Advances · doi:10.1126/sciadv.1600261 · Cited by 125
Shinoda, W., Mikami, M., Baba, T., & Hato, M. (2004) · The Journal of Physical Chemistry B · doi:10.1021/jp035998+ · Cited by 123
Gurtovenko, A. A., & Vattulainen, I. (2007) · Biophysical Journal · doi:10.1529/biophysj.106.094797 · Cited by 123
A lipocentric view of peptide-induced pores
Fuertes, G., Giménez, D., Esteban-Martín, S., Sánchez‐Muñoz, O. L., & Salgado, J. (2011) · European Biophysics Journal · doi:10.1007/s00249-011-0693-4 · Cited by 123
Hauß, T., Dante, S., Dencher, N. A., & Haines, T. H. (2002) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(02)00346-8 · Cited by 121
“Paula et al., [ 21 ] have demonstrated, using bilayers made of phosphatidyl choline lipids with chains varying from C12 to C22, that the proton leakage is exponentially inversely proportional to the thickness of the bilayer.”
BackgroundSelf-citationConstructing vesicle-based artificial cells with embedded living cells as organelle-like modules
Elani, Y., Trantidou, T., Wylie, D., Dekker, L., Polizzi, K. M., Law, R. V., & Ces, O. (2018) · Scientific Reports · doi:10.1038/s41598-018-22263-3 · Cited by 117
Sarwar, C. M. S., Papadimitriou, L., Pitt, B., Piña, I. L., Zannad, F. M., Anker, S. D., Gheorghiade, M., & Butler, J. (2016) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2016.06.060 · Cited by 117
Osmotically Induced Shape Changes of Large Unilamellar Vesicles Measured by Dynamic Light Scattering
Pencer, J., White, G. F., & Hallett, F. R. (2001) · Biophysical Journal · doi:10.1016/s0006-3495(01)75914-0 · Cited by 114
“, 1996, 1998) and one-membrane permeant osmolyte, urea (Paula et al., 1996) as a control.”
BackgroundMethodElectrical double layers at the oil/water interface
Volkov, A. G., Deamer, D. W., Tanelian, D. L., & Markin, V. S. (1996) · Progress in Surface Science · doi:10.1016/s0079-6816(97)82876-6 · Cited by 113
Self-citationSampling errors in free energy simulations of small molecules in lipid bilayers
Neale, C., & Pomès, R. (2016) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2016.03.006 · Cited by 112
ATP synthase: Evolution, energetics, and membrane interactions
Nirody, J. A., Budin, I., & Rangamani, P. (2020) · The Journal of General Physiology · doi:10.1085/jgp.201912475 · Cited by 122
“In contrast, ion permeation in pure phospholipid membranes is mediated by direct ion partitioning or formation of transient pores in the bilayer (Paula et al., 1996).”
BackgroundTejuca, M., Serra, M. D., Potrich, C., Álvarez, C., & Menestrina, G. (2001) · The Journal of Membrane Biology · doi:10.1007/s00232-001-0060-y · Cited by 110
“For example, the single-channel water permeability of the S. aureus a-toxin pore was measured to be around 1.5 ◊1 0 9 nm3/sec [ 45 ].”
BackgroundInfluentialA Genomic View of Sugar Transport inMycobacterium smegmatisandMycobacterium tuberculosis
Titgemeyer, F., Amon, J., Parche, S., Mahfoud, M., Bail, J., Schlicht, M., Rehm, N., Hillmann, D., Stephan, J., Walter, B., et al. (2007) · Journal of Bacteriology · doi:10.1128/jb.00257-07 · Cited by 110
“tuberculosis grows with a generation time of 24 h, and it has been shown that glycerol can directly diffuse through lipid membranes both in vitro (50) and in vivo (22), it is conceivable that the rate of glycerol intake by passive diffusion may be sufficient for growth.”
BackgroundIon-Induced Defect Permeation of Lipid Membranes
Vorobyov, I. V., Olson, T. E., Kim, J. H., Koeppe, R. E., Andersen, O. S., & Allen, T. W. (2014) · Biophysical Journal · doi:10.1016/j.bpj.2013.12.027 · Cited by 110
Collective Dynamics in Fully Hydrated Phospholipid Bilayers Studied by Inelastic X-Ray Scattering
Chen, S. H., Liao, C. Y., Huang, H. W., Weiss, T. M., Bellissent‐Funel, M., & Sette, F. (2001) · Physical Review Letters · doi:10.1103/physrevlett.86.740 · Cited by 104
Accelerated interleaflet transport of phosphatidylcholine molecules in membranes under deformation
Raphael, R. M., & Waugh, R. E. (1996) · Biophysical Journal · doi:10.1016/s0006-3495(96)79340-2 · Cited by 102
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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