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Measuring Lipid Bilayer Permeability with Biomimetic Membranes

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Carbon Nanomaterials for Biomedical Applications

Part of the book series: Springer Series in Biomaterials Science and Engineering ((SSBSE,volume 5))

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Abstract

While there are numerous active mechanisms controlling which molecules cross a cell’s plasma membrane to enter the cytoplasm, these are not the only routes by which molecules can enter cells. In fact, transport by passive diffusion across the lipid bilayer of the plasma membrane represents a nearly universal mechanism of molecular entry. Passive transport represents a key route by which both drugs and environmental toxins can cross biological barriers. Understanding the barrier properties of the lipid bilayer and what molecular characteristics control its permeability is therefore of fundamental interest to toxicology and drug development. Methods of measuring and predicting this permeability have been the topics of research for decades. Today, sophisticated biomimetic cell membranes, coupled with advanced analytical tools and computer modeling, allow new insight into this important biological property.

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References

  1. P. Artursson, J. Karlsson, Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells. Biochem. Biophys. Res. Commun. 175(3), 880–885 (1991)

    Article  Google Scholar 

  2. D.F. Veber, S.R. Johnson, H.-Y. Cheng et al., Molecular properties that influence the oral bioavailability of drug candidates. J. Med. Chem. 45(12), 2615–2623 (2002)

    Article  Google Scholar 

  3. V. Pade, S. Stavchansky, Link between drug absorption solubility and permeability measurements in Caco-2 cells. J. Pharm. Sci. 87(12), 1604–1607 (1998)

    Article  Google Scholar 

  4. C.A. Lipinski, F. Lombardo, B.W. Dominy et al., Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Delivery Rev. 23(1), 3–25 (1997)

    Article  Google Scholar 

  5. R.A. Conradi, A.R. Hilgers, N.F. Ho et al., The influence of peptide structure on transport across Caco-2 cells. II. Peptide bond modification which results in improved permeability. Pharm. Res. 9(3), 435–439 (1992)

    Article  Google Scholar 

  6. P.S. Burton, R.A. Conradi, N.F. Ho et al., How structural features influence the biomembrane permeability of peptides. J. Pharm. Sci. 85(12), 1336–1340 (1996)

    Article  Google Scholar 

  7. M.A. Navia, P.R. Chaturvedi, Design principles for orally bioavailable drugs. Drug Discov. Today 1(5), 179–189 (1996)

    Article  Google Scholar 

  8. K. Palm, P. Stenberg, K. Luthman et al., Polar molecular surface properties predict the intestinal absorption of drugs in humans. Pharm. Res. 14(5), 568–571 (1997)

    Article  Google Scholar 

  9. J. Kelder, P.D. Grootenhuis, D.M. Bayada et al., Polar molecular surface as a dominating determinant for oral absorption and brain penetration of drugs. Pharm. Res. 16(10), 1514–1519 (1999)

    Article  Google Scholar 

  10. Y.C. Martin, A bioavailability score. J. Med. Chem. 48(9), 3164–3170 (2005)

    Article  Google Scholar 

  11. M.J. Waring, Defining optimum lipophilicity and molecular weight ranges for drug candidates—Molecular weight dependent lower log D limits based on permeability. Bioorg. Med. Chem. Lett. 19(10), 2844–2851 (2009)

    Article  Google Scholar 

  12. E. Perola, An analysis of the binding efficiencies of drugs and their leads in successful drug discovery programs. J. Med. Chem. 53(7), 2986–2997 (2010)

    Article  Google Scholar 

  13. R. O’Shea, H.E. Moser, Physicochemical properties of antibacterial compounds: Implications for drug discovery. J. Med. Chem. 51(10), 2871–2878 (2008)

    Article  Google Scholar 

  14. M.-Q. Zhang, B. Wilkinson, Drug discovery beyond the ‘rule-of-five’. Curr. Opin. Biotechnol. 18(6), 478–488 (2007)

    Article  Google Scholar 

  15. G.W. Burton, M.G. Traber, Vitamin E, antioxidant activity, biokinetics, and bioavailability. Annu. Rev. Nutr. 10(1), 357–382 (1990)

    Article  Google Scholar 

  16. R.L. Lipnick, Base-line toxicity predicted by quantitative structure-activity relationships as a probe for molecular mechanism of toxicity. Probi. Bioact. Mech. 413, 366–389 (1989)

    Article  Google Scholar 

  17. E. Foulkes, Transport of toxic heavy metals across cell membranes. Proc. Soc. Exp. Biol. Med. 223(3), 234–240 (2000)

    Article  Google Scholar 

  18. J. Sikkema, J. De Bont, B. Poolman, Mechanisms of membrane toxicity of hydrocarbons. Microbiol. Rev. 59(2), 201–222 (1995)

    Google Scholar 

  19. S. Li, N. Malmstadt, Deformation and poration of lipid bilayer membranes by cationic nanoparticles. Soft Matter 9(20), 4969–4976 (2013)

    Article  Google Scholar 

  20. N.R. Yacobi, N. Malmstadt, F. Fazolallahi et al., Mechanisms of alveolar epithelial translocation of a defined population of nanoparticles. Am. J. Respir. Cell Mol. Biol. 42(5), 604–614 (2010)

    Article  Google Scholar 

  21. D. Bedrov, G.D. Smith, H. Davande et al., Passive transport of C-60 fullerenes through a lipid membrane: A molecular dynamics simulation study. J. Phys. Chem. B. 112(7), 2078–2084 (2008)

    Article  Google Scholar 

  22. T. Wang, J. Bai, X. Jiang et al., Cellular uptake of nanoparticles by membrane penetration: A study combining confocal microscopy with FTIR spectroelectrochemistry. ACS Nano 6(2), 1251–1259 (2012)

    Article  Google Scholar 

  23. A. Verma, O. Uzun, Y.H. Hu et al., Surface-structure-regulated cell-membrane penetration by monolayer-protected nanoparticles. Nat. Mater. 7(7), 588–595 (2008)

    Article  Google Scholar 

  24. M. Jackson, Drug transport across gastrointestinal epithelia. Physiol. Gastrointest. Tract. 2, 1597 (1987)

    Google Scholar 

  25. S. Yee, In vitro permeability across Caco-2 cells (colonic) can predict in vivo (small intestinal) absorption in man—Fact or myth. Pharm. Res. 14(6), 763–766 (1997)

    Article  Google Scholar 

  26. I.J. Hidalgo, T.J. Raub, R.T. Borchardt, Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96(3), 736–749 (1989)

    Google Scholar 

  27. E.H. Kerns, L. Di, S. Petusky et al., Combined application of parallel artificial membrane permeability assay and Caco-2 permeability assays in drug discovery. J. Pharm. Sci. 93(6), 1440–1453 (2004)

    Article  Google Scholar 

  28. G. Wilson, I. Hassan, C. Dix et al., Transport and permeability properties of human Caco-2 cells: An in vitro model of the intestinal epithelial cell barrier. J. Control. Release 11(1), 25–40 (1990)

    Article  Google Scholar 

  29. J. Karlsson, P. Artursson, A method for the determination of cellular permeability coefficients and aqueous boundary layer thickness in monolayers of intestinal epithelial (Caco-2) cells grown in permeable filter chambers. Int. J. Pharm. 71, 55–64 (1991)

    Article  Google Scholar 

  30. J. Karlsson, P. Artursson, A new diffusion chamber system for the determination of drug permeability coefficients across the human intestinal epithelium that are independent of the unstirred water layer. Biochim. Biophys. Acta. 1111, 204–210 (1992)

    Article  Google Scholar 

  31. I. Behrens, W. Kamm, A.H. Dantzig et al., Variation of peptide transporter (PepT1 and HPT1) expression in Caco-2 cells as a function of cell origin. J. Pharm. Sci. 93(7), 1743–1754 (2004)

    Article  Google Scholar 

  32. D.A. Volpe, Variability in Caco-2 and MDCK cell-based intestinal permeability assays. J. Pharm. Sci. 97(2), 712–725 (2008)

    Article  Google Scholar 

  33. A. Kleinzeller, Ernest Overton’s contribution to the cell membrane concept: A centennial appreciation. Physiology 12(4), 49–52 (1997)

    Google Scholar 

  34. A. Missner, P. Pohl, 110 years of the Meyer-Overton rule: Predicting membrane permeability of gases and other small compounds. Chemphyschem 10(9–10), 1405–1414 (2009)

    Article  Google Scholar 

  35. C.E. Overton, in Studies of Narcosis, ed. and trans. by R. L. Lipnick (Chapman and Hall Ltd. and The Wood Library-Museum of Anesthesiology, New York, 1991). (Original Published in 1901)

    Google Scholar 

  36. A. Finkelstein, Water and nonelectrolyte permeability of lipid bilayer membranes. J. Gen. Physiol. 68(2), 127–135 (1976)

    Article  Google Scholar 

  37. J.D. Seader, E.J. Henley, D.K. Roper, Separation Process Principles, 3rd edn. (Wiley, New Jersey, 2010)

    Google Scholar 

  38. J.M. Wolosin, H. Ginsburg, Permeation of organic-acids through lecithin bilayers resemblance to diffusion in polymers. Biochim. Biophys. Acta. 389(1), 20–33 (1975)

    Article  Google Scholar 

  39. A. Walter, J. Gutknecht, Permeability of small nonelectrolyes through lipid bilayer membranes. J. Membr. Biol. 90, 207–217 (1986)

    Article  Google Scholar 

  40. C.A. Lipinsky, F. Lobardo, B.W. Dominy et al., Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 46, 3–26 (2001)

    Article  Google Scholar 

  41. F. Wohnsland, B. Faller, High-throughput permeability pH profile and high-throughput alkane/water log P with artificial membranes. J. Med. Chem. 44, 923–930 (2001)

    Article  Google Scholar 

  42. D. Bassolino-Klimas, H.E. Alper, T.R. Stouch, Solute diffusion in lipid bilayer membranes: An atomic level study by molecular dynamics simulation. Biochemistry 32, 12624–12637 (1993)

    Article  Google Scholar 

  43. S.J. Marrink, H.J.C. Berendsen, Simulation of water transport through a lipid membrane. J. Phys. Chem. 98, 4155–4186 (1994)

    Article  Google Scholar 

  44. D. Bemporad, C. Luttmann, J. Essex, Behaviour of small solutes and large drugs in a lipid bilayer from computer simulations. Biochim. Biophys. Acta. 1718(1), 1–21 (2005)

    Article  Google Scholar 

  45. S.J. Marrink, H.J.C. Berendsen, Permeation process of small molecules across lipid membranes studied by molecular dyanmics simulations. J. Phy. Chem. 100, 16729–16738 (1996)

    Article  Google Scholar 

  46. D. Bemporad, C. Luttmann, J.W. Essex, Computer simulation of small molecule permeation across a lipid bilayer: Dependence on bilayer properties and solute volume, size, and cross-sectional area. Biophys. J. 87(1), 1–13 (2004)

    Article  Google Scholar 

  47. D. Bemporad, J.W. Essex, C. Luttmann, Permeation of small molecules through a lipid bilayer: A computer simulation study. J. Phy. Chem. B. 108, 4975–4884 (2004)

    Article  Google Scholar 

  48. M. Orsi, W.E. Sanderson, J.W. Essex, Permeability of small molecules through a lipid bilayer: A multiscale simulation study. J. Phy. Chem. B. 113, 12019–12029 (2009)

    Article  Google Scholar 

  49. M. Orsi, J.W. Essex, Permeability of drugs and hormones through a lipid bilayer: Insights from dual-resolution molecular dynamics. Soft Matter 6(16), 3797 (2010)

    Article  Google Scholar 

  50. R. Vacha, M.L. Berkowitz, P. Jungwirth, Molecular model of a cell plasma membrane with an asymmetric multicomponent composition: Water permeation and ion effects. Biophys. J. 96(11), 4493–4501 (2009)

    Article  Google Scholar 

  51. K. Shinoda, W. Shinoda, M. Mikami, Efficient free energy calculation of water across lipid membranes. J. Comput. Chem. 29(12), 1912–1918 (2008)

    Article  Google Scholar 

  52. H. Träuble, The movement of molecules across lipid membranes: A molecular theory. J. Membr. Biol. 4(1), 193–208 (1971)

    Article  Google Scholar 

  53. R. Kimmich, A. Peters, K. Spohn, Solubility of oxygen in lecithin bilayers and other hydrocarbon lamellae as a probe for free volume and transport properties. J. Membr. Sci. 9(3), 313–336 (1981)

    Article  Google Scholar 

  54. F. Zocher, D. van der Spoel, P. Pohl et al., Local partition coefficients govern solute permeability of cholesterol-containing membranes. Biophys. J. 105(12), 2760–2770 (2013)

    Article  Google Scholar 

  55. J.F. Nagle, J.C. Mathai, M.L. Zeidel et al., Theory of passive permeability through lipid bilayers. J. Gen. Physiol. 131(1), 77–85 (2008)

    Article  Google Scholar 

  56. S. Mitragotri, M.E. Johnson, D. Blankschtein et al., An analysis of size selectivity of solute partitioning, diffusion, and permeation across lipid bilayers. Biophys. J. 77, 1268–1283 (1999)

    Article  Google Scholar 

  57. J.M. Nitsche, G.B. Kasting, Permeability of fluid-phase phospholipid bilayers: Assessment and useful correlations for permeability screening and other applications. J. Pharm. Sci. 102(6), 2005–2032 (2013)

    Article  Google Scholar 

  58. P. Mueller, D.O. Rudin, H. Ti Tien et al., Reconstitution of cell membrane structure in vitro and its transformation into an excitable system. Nature 194, 979–980 (1962)

    Article  Google Scholar 

  59. A. Bangham, M. Standish, J. Watkins, Diffusion of univalent ions across the lamellae of swollen phospholipids. J. Mol. Biol. 13(1), 238–252 (1965)

    Article  Google Scholar 

  60. P.H. Barry, J.M. Diamond, Effects of unstirred layers on membrane phenomena. Am. Physiol. Soc. 64(3), 763–872 (1984)

    Google Scholar 

  61. F. Burczynski, Z. Cai, J. Moran et al., Palmitate uptake by cultured hepatocytes: Albumin binding and stagnant layer phenomena. Am. J. Physiol. 257(4), G584–G593 (1989)

    Google Scholar 

  62. J. Dainty, C. House, Unstirred layers in frog skin. J. Physiol. 182(1), 66 (1966)

    Article  Google Scholar 

  63. C.U. Cotton, L. Reuss, Measurement of the effective thickness of the mucosal unstirred layer in Necturus gallbladder epithelium. J. Gen. Physiol. 93(4), 631–647 (1989)

    Article  Google Scholar 

  64. T.-X. Xiang, B.D. Anderson, Diffusion of ionizable solutes across planar lipid bilayer membranes: Boundary-layer pH gradients and the effect of buffers. Pharm. Res. 10(11), 1654–1661 (1993)

    Article  Google Scholar 

  65. M. Levitt, T. Aufderheide, C. Fetzer et al., Use of carbon monoxide to measure luminal stirring in the rat gut. J. Clin. Invest. 74(6), 2056 (1984)

    Article  Google Scholar 

  66. L.J. Jensen, J.N. Sørensen, E.H. Larsen et al., Proton pump activity of mitochondria-rich cells: The interpretation of external proton-concentration gradients. J. Gen. Physiol. 109(1), 73–91 (1997)

    Article  Google Scholar 

  67. A. Strocchi, G. Corazza, J. Furne et al., Measurements of the jejunal unstirred layer in normal subjects and patients with celiac disease. Am. J. Physiol. 270(3), G487–G491 (1996)

    Google Scholar 

  68. P. Pohl, E. Rosenfelt, R. Millner, Effects of ultrasound on the steady state transmembrane pH gradient and permeability of acetic acid through bilayer lipid membranes. Biochim. Biophysica. Acta. 1145, 279–283 (1993)

    Article  Google Scholar 

  69. Y.N. Antonenko, G.A. Denisov, P. Pohl, Weak acid transport across bilayer lipid membrane in the presence of buffers. Biophys. J. 64, 1701–1710 (1993)

    Article  Google Scholar 

  70. Y.N. Antonenko, P. Pohl, G.A. Denisov, Permeation of ammonia across bilayer lipid membranes studied by ammonium ion selective microelectrodes. Biophys. J. 72, 2187–2195 (1997)

    Article  Google Scholar 

  71. T. Pedley, The interaction between stirring and osmosis. Part 1. J. Fluid Mech. 101(04), 843–861 (1980)

    Article  Google Scholar 

  72. V.G. Levich, D.B. Spalding, Physicochemical Hydrodynamics (Prentice-Hall, Englewood Cliffs, 1962)

    Google Scholar 

  73. P. Pohl, S.M. Saparov, Y.N. Antonenko, The size of the unstirred layer as a function of the solute diffusion coefficient. Biophy. J. 75, 1403–1409 (1998)

    Article  Google Scholar 

  74. C.A. Berry, A. Verkman, Osmotic gradient dependence of osmotic water permeability in rabbit proximal convoluted tubule. J. Membrane Biol. 105(1), 33–43 (1988)

    Article  Google Scholar 

  75. B. Flourie, N. Vidon, C. Florent et al., Effect of pectin on jejunal glucose absorption and unstirred layer thickness in normal man. Gut 25(9), 936–941 (1984)

    Article  Google Scholar 

  76. E. Guyon, Physical Hydrodynamics (Oxford University Press, New York, 2001)

    Google Scholar 

  77. M. Poznansky, S. Tong, P.C. White et al., Nonelectrolyte diffusion across lipid bilayer systems. J. Gen. Physiol. 67(1), 45–66 (1976)

    Article  Google Scholar 

  78. L. Escuder-Gilabert, J.J. Martínez-Pla, S. Sagrado et al., Biopartitioning micellar separation methods: Modelling drug absorption. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci. 797(1–2), 21–35 (2003)

    Article  Google Scholar 

  79. C. Zhu, L. Jiang, T.-M. Chen et al., A comparative study of artificial membrane permeability assay for high throughput profiling of drug absorption potential. Eur. J. Med. Chem. 37(5), 399–407 (2002)

    Article  Google Scholar 

  80. M. Kansy, F. Senner, K. Gubernator, Physicochemical high throughput screening: Parallel artificial membrane permeation assay in the description of passive absorption processes. J. Med. Chem. 41(7), 1007–1010 (1998)

    Article  Google Scholar 

  81. R. Ano, Y. Kimura, M. Shima et al., Relationships between structure and high-throughput screening permeability of peptide derivatives and related compounds with artificial membranes: Application to prediction of Caco-2 cell permeability. Bioorg. Med. Chem. 12, 257–264 (2004)

    Article  Google Scholar 

  82. K. Sugano, H. Hamada, M. Machida et al., Optimized conditions of bio-mimetic artificial membrane permeation assay. Int. J. Pharm. 228, 181–188 (2001)

    Article  Google Scholar 

  83. T. Rezai, J.E. Bock, M.V. Zhou et al., Conformational flexibility, internal hydrogen bonding, and passive membrane permeability: Successful in silico prediction of the relative permeabilities of cyclic peptides. J. Am. Chem. Soc. 128, 14073–14080 (2006)

    Article  Google Scholar 

  84. P.R. Seo, Z.S. Teksin, J.P. Kao et al., Lipid composition effect on permeability across PAMPA. Eur. J. Pharm. Sci. 29(3–4), 259–268 (2006)

    Article  Google Scholar 

  85. S.S. Leung, J. Mijalkovic, K. Borrelli et al., Testing physical models of passive membrane permeation. J. Chem. Inf. Model. 52(6), 1621–1636 (2012)

    Article  Google Scholar 

  86. M. Thompson, R.B. Lennox, R. McClelland, Structure and electrochemical properties of microfiltration filter-lipid membrane systems. Anal. Chem. 54(1), 76–81 (1982)

    Article  Google Scholar 

  87. P.V. Balimane, E. Pace, S. Chong et al., A novel high-throughput automated chip-based nanoelectrospray tandem mass spectrometric method for PAMPA sample analysis. J. Pharm. Biomed. Anal. 39(1), 8–16 (2005)

    Article  Google Scholar 

  88. J. Gutknecht, A. Walter, Transport of protons and hydrochloric acid through lipid bilayer membranes. Biochim. Biophys. Acta. 641, 183–188 (1981)

    Article  Google Scholar 

  89. Y.N. Antonenko, A.A. Bulychev, Measurements of local pH changes near bilayer lipid membrane by means of a pH microelectrode and a protonophore-dependent membrane potential. Comparison of the methods. Biochim. Biophys. Acta. 1070(1), 279–282 (1991)

    Article  Google Scholar 

  90. S.M. Dzekunov, Y.N. Antonenko, Dynamics of formation and dissipation of local pH gradients in the unstirred layers near bilayer lipid membranes. Bioelectrochem. Bioenerg. 41, 187–190 (1996)

    Article  Google Scholar 

  91. S. Ohki, Membrane Potential and ion permeability of lipid bilayer membranes. Bioelectrochem. Bioenerg. 7, 487–501 (1980)

    Article  Google Scholar 

  92. R. Sandeaux, J. Sandeaux, C. Gavach et al., Transport of Na+ by monensin across biomolecular lipid membranes. Biochim. Biophys. Acta. 684, 127–132 (1982)

    Article  Google Scholar 

  93. J. Gutknecht, A. Walter, Hydroxyl ion permeability of lipid bilayer membranes. Biochim. Biophys. Acta. 645, 161–162 (1981)

    Article  Google Scholar 

  94. J. Gutknecht, A. Walter, Hydrofluoric and nitric acid transport through lipid bilayer membranes. Biochim. Biophys. Acta. 644(1), 153–156 (1981)

    Article  Google Scholar 

  95. A. Walter, J. Gutknecht, Monocarboxylic acid permeation through lipid bilayer membranes. J. Membrane Biol. 77(3), 255–264 (1984)

    Article  Google Scholar 

  96. Y.N. Antonenko, L. Yaguzhinsky, Generation of potential in lipid bilayer membranes as a result of proton-transfer reactions in the unstirred layers. J. Bioenerg. Biomembr. 14(5–6), 457–465 (1982)

    Article  Google Scholar 

  97. Y.N. Antonenko, L.S. Yaguzhinsky, The role of pH gradient in the unstirred layers in the transport of weak acids and bases through bilayer lipid membranes. Bioelectrochem. Bioenerg. 13(1), 85–91 (1984)

    Article  Google Scholar 

  98. Y.N. Antonenko, P. Pohl, Steady-state nonmonotonic concentration profiles in the unstirred layers of bilayer lipid membranes. Biochim. Biophys. Acta. 1235(1), 57–61 (1995)

    Article  Google Scholar 

  99. A.V. Krylov, P. Pohl, M.L. Zeidel et al., Water permeability of asymmetric planar lipid bilayers: Leaflets of different composition offer independent and additive resistances to permeation. J. Gen. Physiol. 118, 333–339 (2001)

    Article  Google Scholar 

  100. J.M. Grime, M.A. Edwards, N.C. Rudd et al., Quantitative visualization of passive transport across bilayer lipid membranes. Proc. Natl. Acad. Sci. U S A 105(38), 14277–14282 (2008)

    Article  Google Scholar 

  101. A. Missner, P. Kügler, Y.N. Antonenko et al., Passive transport across bilayer lipid membranes: Overton continues to rule. Proc. Natl. Acad. Sci. U S A 105(52), E123–E123 (2008)

    Article  Google Scholar 

  102. J.M. Grime, M.A. Edwards, P.R. Unwin, Reply to Missner et al.: Timescale for passive diffusion across bilayer lipid membranes. Proc. Natl. Acad. Sci. U S A 105(52), E124–E124 (2008)

    Article  Google Scholar 

  103. J.T. Groves, N. Ulman, S.G. Boxer, Micropatterning fluid lipid bilayers on solid supports. Science 275(5300), 651–653 (1997)

    Article  Google Scholar 

  104. J.S. Hovis, S.G. Boxer, Patterning and composition arrays of supported lipid bilayers by microcontact printing. Langmuir 17(11), 3400–3405 (2001)

    Article  Google Scholar 

  105. J.T. Groves, S.G. Boxer, Micropattern formation in supported lipid membranes. Acc. Chem. Res. 35(3), 149–157 (2002)

    Article  Google Scholar 

  106. A.M. Brozell, S. Inaba, A.N. Parikh, Lipid bilayers on topochemically structured planar colloidal crystals: A versatile platform for optical recording of membrane-mediated ion transport. Soft Matter 6(21), 5334–5341 (2010)

    Article  Google Scholar 

  107. H. Bayley, B. Cronin, A. Heron et al., Droplet interface bilayers. Mol. BioSyst. 4(12), 1191–1208 (2008)

    Article  Google Scholar 

  108. N. Malmstadt, M.A. Nash, R.F. Purnell et al., Automated formation of lipid-bilayer membranes in a microfluidic device. Nano Lett. 6(9), 1961–1965 (2006)

    Article  Google Scholar 

  109. T. Nisisako, S. Portonovo, J. Schmidt, Microfluidic passive permeability assay using nanoliter droplet interface lipid bilayers. Analyst 138(22), 6793–6800 (2013)

    Article  Google Scholar 

  110. F. Szoka Jr., D. Papahadjopoulos, Comparative properties and methods of preparation of lipid vesicles (liposomes). Annu. Rev. Biophys. Bioeng. 9(1), 467–508 (1980)

    Article  Google Scholar 

  111. T.-X. Xiang, B.D. Anderson, Influence of chain ordering on the selectivity of dipalmitoylphosphatisylcholine bilayer membranes for permeant size and shape. Biophys. J. 75, 13 (1998)

    Article  Google Scholar 

  112. J. Alger, J. Prestegard, Nuclear magnetic resonance study of acetic acid permeation of large unilamellar vesicle membranes. Biophys. J. 28(1), 1–13 (1979)

    Article  Google Scholar 

  113. T.-X. Xiang, J. Chen, B.D., Anderson, A quantitative model for the dependence of solute permeability on peptide and cholesterol content in biomembranes. J. Membr. Biol. 177(2), 137–148 (2000)

    Article  Google Scholar 

  114. T.-X. Xiang, Y.H. Xu, B.D. Anderson, The barrier domain for solute permeation varies with lipid bilayer phase structure. J. Membr. Biol. 165, 77–90 (1998)

    Article  Google Scholar 

  115. M. Wunder, P. Bollert, G. Gros, Mathematical modelling of the role of intra-and extracellular activity of carbonic anhydrase and membrane permeabilities of HCO3-, H2O and CO2 in 18O exchange. Isotopes Environ. Health Stud. 33(1), 197–206 (1997)

    Article  Google Scholar 

  116. M. Wunder, G. Gros, 18O exchange in suspensions of red blood cells: Determination of parameters of mass spectrometer inlet system. Isotopes Environ. Health Stud. 34(3), 303–310 (1998)

    Article  Google Scholar 

  117. V. Endeward, G. Gros, Extra-and intracellular unstirred layer effects in measurements of CO2 diffusion across membranes–a novel approach applied to the mass spectrometric 18O technique for red blood cells. J. Physiol. 587(6), 1153–1167 (2009)

    Article  Google Scholar 

  118. V. Endeward, G. Gros, Low carbon dioxide permeability of the apical epithelial membrane of guinea-pig colon. J. Physiol. 567(1), 253–265 (2005)

    Article  Google Scholar 

  119. F. Itel, S. Al-Samir, F. Oberg et al., CO2 permeability of cell membranes is regulated by membrane cholesterol and protein gas channels. Faseb J. 26(12), 5182–5191 (2012)

    Article  Google Scholar 

  120. J.W. Nichols, D.W. Deamer, Net proton-hydroxyl permeability of large unilamellar liposomes measured by an acid-base titration technique. Proc. Natl. Acad. Sci. U S A 77(4), 2038–2042 (1980)

    Article  Google Scholar 

  121. D.W. Deamer, J.W. Nichols, Proton-hydroxide permeability of liposomes. Proc. Natl. Acad. Sci. U S A 80(1), 165–168 (1983)

    Article  Google Scholar 

  122. D.W. Deamer, J.W. Nichols, Proton flux mechanisms in model and biological membranes. J. Membrane Biol. 107(2), 91–103 (1989)

    Article  Google Scholar 

  123. R. Sha’Afi, G. Rich, V.W. Sidel et al., The effect of the unstirred layer on human red cell water permeability. J. Gen. Physiol. 50(5), 1377–1399 (1967)

    Article  Google Scholar 

  124. R. Lawaczeck, Water permeability through biological membranes by isotopic effects of fluorescence and light scattering. Biophys. J. 45(3), 491–494 (1984)

    Article  Google Scholar 

  125. H.J. Mlekoday, R. Moore, D.G. Levitt, Osmotic water permeability of the human red cell. Dependence on direction of water flow and cell volume. J. Gen. Physiol. 81(2), 213–220 (1983)

    Article  Google Scholar 

  126. R. Ye, A.S. Verkman, Simultaneous optical measurement of osmotic and diffusional water permeability in cells and liposomes. BioChemistry 28(2), 824–829 (1989)

    Article  Google Scholar 

  127. C. Dordas, P.H. Brown, Permeability of boric acid across lipid bilayers and factors affecting it. J. Membr. Biol. 175, 95–105 (2000)

    Article  Google Scholar 

  128. J.C. Mathai, G.D. Sprott, M.L. Zeidel, Molecular mechanisms of water and solute transport across archaebacterial lipid membranes. J. Biol. Chem. 276(29), 27266–27271 (2001)

    Article  Google Scholar 

  129. R. Holland, H. Shibata, P. Scheid et al., Kinetics of O2 uptake and release by red cells in stopped-flow apparatus: Effects of unstirred layer. Respir. physiol. 59(1), 71–91 (1985)

    Article  Google Scholar 

  130. M. Brändén, S. Dahlin, F. Höök, Label-free measurements of molecular transport across liposome membranes using evanescent-wave sensing. Chemphyschem 9(17), 2480–2485 (2008)

    Article  Google Scholar 

  131. M. Brändén, S.R. Tabaei, G. Fischer et al., Refractive-index-based screening of membrane-protein-mediated transfer across biological membranes. Biophys. J. 99(1), 124–133 (2010)

    Article  Google Scholar 

  132. S. Li, P. Hu, N. Malmstadt, Confocal imaging to quantify passive transport across biomimetic lipid membranes. Anal. Chem. 82(18), 7766–7771 (2010)

    Article  Google Scholar 

  133. E.C. Heider, G.A. Myers, J.M. Harris, Spectroscopic microscopy analysis of the interior pH of individual phospholipid vesicles. Anal. Chem. 83(21), 8230–8238 (2011)

    Article  Google Scholar 

  134. K.L. Budzinski, M. Zeigler, B.S. Fujimoto et al., Measurements of the acidification kinetics of single SynaptopHluorin vesicles. Biophys. J. 101(7), 1580–1589 (2011)

    Article  Google Scholar 

  135. S. Li, P.C. Hu, N. Malmstadt, Imaging molecular transport across lipid bilayers. Biophys. J. 101(3), 700–708 (2011)

    Article  Google Scholar 

  136. P. Kuhn, K. Eyer, S. Allner et al., A microfluidic vesicle screening platform: Monitoring the lipid membrane permeability of tetracyclines. Anal. Chem. 83(23), 8877–8885 (2011)

    Article  Google Scholar 

  137. K. Eyer, F. Paech, F. Schuler et al., A liposomal fluorescence assay to study permeation kinetics of drug-like weak bases across the lipid bilayer. J. Control. Release 173, 102–109 (2013)

    Article  Google Scholar 

  138. G. Ohlsson, S.R. Tabaei, J. Beech et al., Solute transport on the sub 100 ms scale across the lipid bilayer membrane of individual proteoliposomes. Lab Chip 12(22), 4635–4643 (2012)

    Article  Google Scholar 

  139. C.L. Kuyper, J.S. Kuo, S.A. Mutch et al., Proton permeation into single vesicles occurs via a sequential two-step mechanism and is heterogeneous. J. Am. Chem. Soc. 128(10), 3233–3240 (2006)

    Article  Google Scholar 

  140. T. Robinson, P. Kuhn, K. Eyer et al., Microfluidic trapping of giant unilamellar vesicles to study transport through a membrane pore. Biomicrofluidics 7(4), 044105 (2013)

    Article  Google Scholar 

  141. M. Hope, M. Bally, G. Webb et al., Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim. Biophys. Acta. 812(1), 55–65 (1985)

    Article  Google Scholar 

  142. D.J. Needleman, Y. Xu, T.J. Mitchison, Pin-hole array correlation imaging: Highly parallel fluorescence correlation spectroscopy. Biophys. J. 96(12), 5050–5059 (2009)

    Article  Google Scholar 

  143. P. Brissette, D.P. Ballou, V. Massey, Determination of the dead time of a stopped-flow fluorometer. Anal. Biochem. 181(2), 234–238 (1989)

    Article  Google Scholar 

  144. P.C. Hu, S. Li, N. Malmstadt, Microfluidic fabrication of asymmetric giant lipid vesicles. ACS Appl. Mater. Interfaces 3(5), 1434–1440 (2011)

    Article  Google Scholar 

  145. D.L. Richmond, E.M. Schmid, S. Martens et al., Forming giant vesicles with controlled membrane composition, asymmetry, and contents. Proc. Natl. Acad. Sci. U S A 108(23), 9431–9436 (2011)

    Article  Google Scholar 

  146. L.-L. Pontani, J. van der Gucht, G. Salbreux et al., Reconstitution of an actin cortex inside a liposome. Biophys. J. 96(1), 192–198 (2009)

    Article  Google Scholar 

  147. J.S. Hansen, J.R. Thompson, C. Helix-Nielsen et al., Lipid directed intrinsic membrane protein segregation. J. Am. Chem. Soc. 135(46), 17294–17297 (2013)

    Article  Google Scholar 

  148. T. Hamada, Y. Miura, Y. Komatsu et al., Construction of asymmetric cell-sized lipid vesicles from lipid-coated water-in-oil microdroplets. J. Phys. Chem. B. 112(47), 14678–14681 (2008)

    Article  Google Scholar 

  149. S. Hell, E.H. Stelzer, Fundamental improvement of resolution with a 4Pi-confocal fluorescence microscope using two-photon excitation. Opt. Commun. 93(5), 277–282 (1992)

    Article  Google Scholar 

  150. M.G. Gustafsson, Nonlinear structured-illumination microscopy: Wide-field fluorescence imaging with theoretically unlimited resolution. Proc. Natl. Acad. Sci. U S A 102(37), 13081–13086 (2005)

    Article  Google Scholar 

  151. S.W. Hell, J. Wichmann, Breaking the diffraction resolution limit by stimulated emission: Stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19(11), 780–782 (1994)

    Article  Google Scholar 

  152. G.A. Myers, J.M. Harris, Confocal raman microscopy of pH-gradient-based 10,000-fold preconcentration of compounds within individual, optically trapped phospholipid vesicles. Anal. Chem. 83(15), 6098–6105 (2011)

    Article  Google Scholar 

  153. L.M. Freeman, S. Li, Y. Dayani et al., Excitation of Cy5 in self-assembled lipid bilayers using optical microresonators. Appl. Phys. Lett. 98(14), 143703 (2011)

    Article  Google Scholar 

  154. F. Patolsky, G. Zheng, C.M. Lieber, Nanowire-based biosensors. Anal. Chem. 78(13), 4260–4269 (2006)

    Article  Google Scholar 

  155. M. Curreli, R. Zhang, F.N. Ishikawa et al., Real-time, label-free detection of biological entities using nanowire-based FETs. IEEE Trans. Nanotechnol. 7(6), 651–667 (2008)

    Article  Google Scholar 

  156. A.M. El-Arabi, C.S. Salazar, J.J. Schmidt, Ion channel drug potency assay with an artificial bilayer chip. Lab Chip 12(13), 2409–2413 (2012)

    Article  Google Scholar 

  157. B. Lu, G. Kocharyan, J.J. Schmidt, Lipid bilayer arrays: Cyclically formed and measured. Biotech. J. 9(3), 446–451 (2013)

    Article  Google Scholar 

  158. P. Kongsuphol, K.B. Fang, D.Z. Peng, Lipid bilayer technologies in ion channel recordings and their potential in drug screening assay. Sens. Actuators B Chem. 185, 530–542 (2013)

    Article  Google Scholar 

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Runas, K., Malmstadt, N. (2016). Measuring Lipid Bilayer Permeability with Biomimetic Membranes. In: Zhang, M., Naik, R., Dai, L. (eds) Carbon Nanomaterials for Biomedical Applications. Springer Series in Biomaterials Science and Engineering, vol 5. Springer, Cham. https://doi.org/10.1007/978-3-319-22861-7_16

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