Determining small-molecule permeation through lipid membranes

Jacopo Frallicciardi, Matteo Gabba, Bert Poolman

Published: 2022-08-23 DOI: 10.1038/s41596-022-00734-2

membrane permeability

stopped-flow fluorimetry

lipid vesicles

osmotic permeability

pH-sensitive probes

AI 解读

Author Correction: Full-length sequencing of circular DNA viruses and extrachromosomal circular DNA using CIDER-Seq

Generation of heart-forming organoids from human pluripotent stem cells

Design and fabrication of wearable electronic textiles using twisted fiber-based threads

Activation of mechanoluminescent nanotransducers by focused ultrasound enables light delivery to deep-seated tissue in vivo

Chromatin accessibility profiling by ATAC-seq

Deoxyfluorination of phenols for chemoselective18F-labeling of peptides

Author Correction: cfSNV: a software tool for the sensitive detection of somatic mutations from cell-free DNA

Human primordial germ cell-like cells specified from resetting precursors develop in human hindgut organoids

An inexpensive semi-automated sample processing pipeline for cell-free RNA extraction

Application of CHyMErA Cas9-Cas12a combinatorial genome-editing platform for genetic interaction mapping and gene fragment deletion screening

查看全部

Sections

Figures

References

The passive permeability of cell membranes is of key importance in biology, biomedical research and biotechnology as it determines the extent to which various molecules such as drugs, products of metabolism, and toxins can enter or leave the cell unaided
Introduction
Materials
Procedure
Troubleshooting
Timing
Anticipated results
- References
- References
References
ACKNOWLEDGMENTS

Vitali, V., Sutka, M., Amodeo, G., Chara, O. & Ozu, M. The water to solute permeability ratio governs the osmotic volume dynamics in beetroot vacuoles. Front. Plant Sci. 7, 1388 (2016).
Massari, S., Frigeri, L. & Azzone, G. F. Permeability to water, dimension of surface, and structural changes during swelling in rat liver mitochondria. J. Membr. Biol. 9, 57–70 (1972).
Brahm, J. Diffusional water permeability of human erythrocytes and their ghosts. J. Gen. Physiol. 79, 791–819 (1982).
Mathai, J. C. et al. Functional analysis of aquaporin-1 deficient red cells. J. Biol. Chem. 271, 1309–1313 (1996).
Foctave & Scilab. MINUIT—a Binding to Minuit for Matlab (1996).
Krämer, S. D. et al. When barriers ignore the “rule-of-five”. Adv. Drug Deliv. Rev. 101, 62–74 (2016).
Drew, D., North, R. A., Nagarathinam, K. & Tanabe, M. Structures and general transport mechanisms by the major facilitator superfamily (MFS). Chem. Rev. 121, 5289–5335 (2021).
Henderson, R. K., Fendler, K. & Poolman, B. Coupling efficiency of secondary active transporters. Curr. Opin. Biotechnol. 58, 62–71 (2019).
Fricke, W. Water transport and energy. Plant. Cell Environ. 40, 977–994 (2017).
Hannesschlaeger, C., Horner, A. & Pohl, P. Intrinsic membrane permeability to small molecules. Chem. Rev. 119, 5922–5953 (2019).
Kerns, E. H. & Li, D. Drug-like Properties: Concepts, Structure Optimization, Design and Methods from ADME to Toxicity (Academic, 2008).
Bangham, A. D., De Gier, J. & Greville, G. D. Osmotic properties and water permeability of phospholipid liquid crystals. Chem. Phys. Lipids 1, 225–246 (1967).
Gabba, M. et al. Weak acid permeation in synthetic lipid vesicles and across the yeast plasma membrane. Biophys. J. 118, 422–434 (2020).
Neijssel, O. M., Buurman, E. T. & de Mattos, M. J. T. The role of futile cycles in the energetics of bacterial growth. Biochim. Biophys. Acta 1018, 252–255 (1990).
Poolman, B. & Konings, W. N. Relation of growth of Streptococcus lactis and Streptococcus cremoris to amino acid transport. J. Bacteriol. 170, 700–707 (1988).
Borgnia, M. J., Kozono, D., Calamita, G., Maloney, P. C. & Agre, P. Functional reconstitution and characterization of AqpZ, the E. coli water channel protein. J. Mol. Biol. 291, 1169–1179 (1999).
Hill, W. G. & Zeidel, M. L. Reconstituting the barrier properties of a water-tight epithelial membrane by design of leaflet-specific liposomes. J. Biol. Chem. 275, 30176–30185 (2000).
Krylov, A. V., Pohl, P., Zeidel, M. L. & Hill, W. G. Water permeability of asymmetric planar lipid bilayers. J. Gen. Physiol. 118, 333–340 (2001).
Frallicciardi, J., Melcr, J., Siginou, E., Marrink, S. J. & Poolman, B. Membrane thickness, lipid phase and sterol type are determining factors in the permeability of membranes to small solutes. Nat. Commum. 13, 1605 (2022).
Chen, P. Y., Pearce, D. & Verkman, A. S. Membrane water and solute permeability determined quantitatively by self-quenching of an entrapped fluorophore. Biochemistry 27, 5713–5718 (1988).
Sha’afi, R. I., Rich, G. T., Sidel, V. W., Bossert, W. & Solomon, A. K. The effect of the unstirred layer on human red cell water permeability. J. Gen. Physiol. 50, 1377–1399 (1967).
Zeidel, M. L., Ambudkar, S. V., Smith, B. L. & Agre, P. Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 31, 7436–7440 (1992).
Tsunoda, S. P., Wiesner, B., Lorenz, D., Rosenthal, W. & Pohl, P. Aquaporin-1, nothing but a water channel. J. Biol. Chem. 279, 11364–11367 (2004).
Preston, G. M., Carroll, T. P., Guggino, W. B. & Agre, P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256, 385–387 (1992).
Mlekoday, H. J., Moore, R. & Levitt, D. G. Osmotic water permeability of the human red cell. Dependence on direction of water flow and cell volume. J. Gen. Physiol. 81, 213–220 (1983).
Mathai, J. C., Sprott, G. D. & Zeidel, M. L. Molecular mechanisms of water and solute transport across archaebacterial lipid membranes. J. Biol. Chem. 276, 27266–27271 (2001).
Verkman, A. S. Water permeability measurement in living cells and complex tissues. J. Membr. Biol. 173, 73–87 (2000).
Saparov, S. M., Antonenko, Y. N., Koeppe, R. E. & Pohl, P. Desformylgramicidin: a model channel with an extremely high water permeability. Biophys. J. 79, 2526–2534 (2000).
Shatil-cohen, A. et al. Measuring the osmotic water permeability coefficient (Pf) of spherical cells: isolated plant protoplasts as an example. J. Vis. Exp. 92, e51652 (2014).
Pfeuffer, J. et al. Expression of aquaporins in Xenopus laevis oocytes and glial cells as detected by diffusion-weighted 1H NMR spectroscopy and photometric swelling assay. Biochim. Biophys. Acta 1448, 27–36 (1998).
Ye, R. & Verkman, A. S. Simultaneous optical measurement of osmotic and diffusional water permeability in cells and liposomes. Biochemistry 28, 824–829 (1989).
Karan, D. M. & Macey, R. I. The permeability of the human red cell to deuterium oxide (heavy water). J. Cell. Physiol. 104, 209–214 (1980).
Zhang, R. B. & Verkman, A. S. Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder. Am. J. Physiol. Physiol. 260, C26–C34 (1991).
Lande, M. B., Priver, N. A. & Zeidel, M. L. Determinants of apical membrane permeabilities of barrier epithelia. Am. J. Physiol. Physiol. 267, C367–C374 (1994).
Levitt, D. G. & Mlekoday, H. J. Reflection coefficient and permeability of urea and ethylene glycol in the human red cell membrane. J. Gen. Physiol. 81, 239–253 (1983).
Gabba, M. & Poolman, B. Physiochemical modeling of vesicle dynamics upon osmotic upshift. Biophys. J. 118, 435–447 (2020).
Frallicciardi, J., Gabba, M. & Poolman, B. Determining small molecule permeation through lipid membranes. GitHub https://doi.org/10.5281/zenodo.6511116 (2022).
Rawicz, W., Smith, B. A., McIntosh, T. J., Simon, S. A. & Evans, E. Elasticity, strength, and water permeability of bilayers that contain raft microdomain-forming lipids. Biophys. J. 94, 4725–4736 (2008).
Lindahl, L., Genheden, S., Eriksson, L. A., Olsson, L. & Bettiga, M. Sphingolipids contribute to acetic acid resistance in Zygosaccharomyces bailii. Biotechnol. Bioeng. 113, 744–753 (2016).
Di, L. et al. The critical role of passive permeability in designing successful drugs. ChemMedChem 15, 1862–1874 (2020).
Dahan, A. & Miller, J. M. The solubility–permeability interplay and its implications in formulation design and development for poorly soluble drugs. AAPS J. 14, 244–251 (2012).
Pols, T. et al. A synthetic metabolic network for physicochemical homeostasis. Nat. Commun. 10, 4239 (2019).
Costa, A. P., Xu, X. & Burgess, D. J. Freeze–anneal–thaw cycling of unilamellar liposomes: effect on encapsulation efficiency. Pharm. Res. 31, 97–103 (2014).
Llu, L. & Yonetani, T. Preparation and characterization of liposome-encapsulated haemoglobin by a freeze–thaw method. J. Microencapsul. 11, 409–421 (1994).
Geertsma, E. R., Nik Mahmood, N. A. B., Schuurman-Wolters, G. K. & Poolman, B. Membrane reconstitution of ABC transporters and assays of translocator function. Nat. Protoc. 3, 256–266 (2008).
Lee, C. et al. A two-domain elevator mechanism for sodium/proton antiport. Nature 501, 573–577 (2013).
Herget, M. et al. Purification and reconstitution of the antigen transport complex TAP. J. Biol. Chem. 284, 33740–33749 (2009).
Sacerdote, M. G. & Szostak, J. W. Semipermeable lipid bilayers exhibit diastereoselectivity favoring ribose. Proc. Natl Acad. Sci. USA 102, 6004–6008 (2005).
Hannesschlaeger, C., Barta, T., Pechova, H. & Pohl, P. The effect of buffers on weak acid uptake by vesicles. Biomolecules 9, 63 (2019).
Shi, S. et al. Hidden complexity in membrane permeabilization behavior of antimicrobial polycations. Phys. Chem. Chem. Phys. 23, 1475–1488 (2021).
Dutta, S., Watson, B., Mattoo, S. & Rochet, J.-C. Calcein release assay to measure membrane permeabilization by recombinant alpha-synuclein. Bio Protoc. 10, e3690 (2020).
Allen, T. M. & Cleland, L. G. Serum-induced leakage of liposome contents. Biochim. Biophys. Acta 597, 418–426 (1980).
De Gier, J., Mandersloot, J. G. & Van Deenen, L. L. M. Lipid composition and permeability of liposomes. Biochim. Biophys. Acta 150, 666–675 (1968).
De Gier, J., Mandersloot, J. G., Hupkes, J. V., McElhaney, R. N. & Van Beek, W. P. On the mechanism of non-electrolyte permeation through lipid bilayers and through biomembranes. Biochim. Biophys. Acta 233, 610–618 (1971).
Allen, T. M., Hong, K. & Papahadjopoulos, D. Membrane contact, fusion and hexagonal (HII) transitions in phosphatidylethanolamine liposomes. Biochemistry 29, 2976–2985 (1990).
D'Souza, G. G. M. Liposomes 1522 (Springer, 2017).
Hamann, S. et al. Measurement of cell volume changes by fluorescence self-quenching. J. Fluoresc. 12, 139–145 (2002).
Blicher, A., Wodzinska, K., Fidorra, M., Winterhalter, M. & Heimburg, T. The temperature dependence of lipid membrane permeability, its quantized nature, and the influence of anesthetics. Biophys. J. 96, 4581–4591 (2009).
James, F. Minuit: Function Minimization and Error Analysis Version 94.1 (CERN, 1994).
El Tayar, N., Tsai, R.-S., Carrupt, P.-A. & Testa, B. Octan-1-ol–water partition coefficients of zwitterionic α-amino acids. Determination by centrifugal partition chromatography and factorization into steric/hydrophobic and polar components. J. Chem. Soc. Perkin Trans. 2, 79–84 (1992).
Perkins, R. & Vaida, V. Phenylalanine increases membrane permeability. J. Am. Chem. Soc. 139, 14388–14391 (2017).

Determining small-molecule permeation through lipid membranes

Supplementary information

推荐阅读