Composition Dependence of Water Permeation Across Multicomponent Gel-Phase Bilayers

Hartkamp, Remco; Moore, Timothy C.; Iacovella, Christopher R.; Thompson, Michael A.; Bulsara, Pallav A.; Moore, David J.; McCabe, Clare

doi:10.1021/acs.jpcb.8b00747

Composition Dependence of Water Permeation Across Multicomponent Gel-Phase Bilayers

Journal Article · Sun Mar 04 23:00:00 EST 2018 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI:https://doi.org/10.1021/acs.jpcb.8b00747· OSTI ID:1480431

^[1]; Moore, Timothy C. ^[2]; Iacovella, Christopher R. ^[2]; Thompson, Michael A. ^[3]; Bulsara, Pallav A. ^[3]; Moore, David J. ^[3]; ^[2]

Vanderbilt Univ., Nashville, TN (United States); Delft Univ. of Technology, Delft (The Netherlands)
Vanderbilt Univ., Nashville, TN (United States)
GlaxoSmithKline Consumer Healthcare, Warren, NJ (United States)

The permeability of multicomponent phospholipid bilayers in the gel phase is investigated via molecular dynamics simulation. The physical role of the different molecules is probed by comparing multiple mixed-component bilayers containing distearylphosphatidylcholine (DSPC) with varying amounts of either the emollient isostearyl isostearate or long-chain alcohol (dodecanol, octadecanol, or tetracosanol) molecules. Permeability is found to depend on both the tail packing density and hydrogen bonding between lipid headgroups and water. Whereas the addition of emollient or alcohol molecules to a gel-phase DSPC bilayer can increase the tail packing density, it also disturbed the hydrogen-bonding network, which in turn can increase interfacial water dynamics. In conclusion, these phenomena have opposing effects on bilayer permeability, which is found to depend on the balance between enhanced tail packing and decreased hydrogen bonding.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

OSTI ID:: 1480431

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Journal Name: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry Journal Issue: 12 Vol. 122; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

On the permeability of water molecules across vesicular lipid bilayers Lawaczeck, Rüdiger The Journal of Membrane Biology, Vol. 51, Issue 3-4 https://doi.org/10.1007/bf01869086	journal	September 1979
Behaviour of small solutes and large drugs in a lipid bilayer from computer simulations Bemporad, D.; Luttmann, C.; Essex, J. W. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1718, Issue 1-2 https://doi.org/10.1016/j.bbamem.2005.07.009	journal	December 2005
FTIR studies show lipophilic moisturizers to interact with stratum corneum lipids, rendering the more densely packed Caussin, Julia; Gooris, Gert S.; Bouwstra, Joke A. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 6 https://doi.org/10.1016/j.bbamem.2008.03.006	journal	June 2008
Permeability across lipid membranes Shinoda, Wataru Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 10 https://doi.org/10.1016/j.bbamem.2016.03.032	journal	October 2016
Local Partition Coefficients Govern Solute Permeability of Cholesterol-Containing Membranes Zocher, Florian; van der Spoel, David; Pohl, Peter Biophysical Journal, Vol. 105, Issue 12 https://doi.org/10.1016/j.bpj.2013.11.003	journal	December 2013
A Method to Predict Blood-Brain Barrier Permeability of Drug-Like Compounds Using Molecular Dynamics Simulations Carpenter, Timothy S.; Kirshner, Daniel A.; Lau, Edmond Y. Biophysical Journal, Vol. 107, Issue 3 https://doi.org/10.1016/j.bpj.2014.06.024	journal	August 2014
Investigating the Structure of Multicomponent Gel-Phase Lipid Bilayers Hartkamp, Remco; Moore, Timothy C.; Iacovella, Christopher R. Biophysical Journal, Vol. 111, Issue 4 https://doi.org/10.1016/j.bpj.2016.07.016	journal	August 2016
A Universal Correlation Predicts Permeability Coefficients of Fluid- and Gel-Phase Phospholipid and Phospholipid-Cholesterol Bilayers for Arbitrary Solutes Nitsche, Johannes M.; Kasting, Gerald B. Journal of Pharmaceutical Sciences, Vol. 105, Issue 5 https://doi.org/10.1016/j.xphs.2016.02.012	journal	May 2016
Incorporation of surface tension into molecular dynamics simulation of an interface: a fluid phase lipid bilayer membrane Chiu, S. W.; Clark, M.; Balaji, V. Biophysical Journal, Vol. 69, Issue 4 https://doi.org/10.1016/s0006-3495(95)80005-6	journal	October 1995
A comparative study of diffusive and osmotic water permeation across bilayers composed of phospholipids with different head groups and fatty acyl chains Jansen, M.; Blume, A. Biophysical Journal, Vol. 68, Issue 3 https://doi.org/10.1016/s0006-3495(95)80275-4	journal	March 1995
Structure of gel phase saturated lecithin bilayers: temperature and chain length dependence Sun, W. J.; Tristram-Nagle, S.; Suter, R. M. Biophysical Journal, Vol. 71, Issue 2 https://doi.org/10.1016/s0006-3495(96)79290-1	journal	August 1996
Simulation-Based Approaches for Determining Membrane Permeability of Small Compounds Lee, Christopher T.; Comer, Jeffrey; Herndon, Conner Journal of Chemical Information and Modeling, Vol. 56, Issue 4 https://doi.org/10.1021/acs.jcim.6b00022	journal	March 2016
Molecular Simulation of the DPPE Lipid Bilayer Gel Phase: Coupling between Molecular Packing Order and Tail Tilt Angle Uppulury, Karthik; Coppock, Patrick S.; Kindt, James T. The Journal of Physical Chemistry B, Vol. 119, Issue 28 https://doi.org/10.1021/acs.jpcb.5b05720	journal	July 2015
Effects of Acyl Chain Unsaturation on Activation Energy of Water Permeability across Droplet Bilayers of Homologous Monoglycerides: Role of Cholesterol Lopez, Maria; Denver, Jacqueline; Evangelista, Sue Ellen Langmuir, Vol. 34, Issue 5 https://doi.org/10.1021/acs.langmuir.7b03590	journal	January 2018
Accelerating Convergence in Molecular Dynamics Simulations of Solutes in Lipid Membranes by Conducting a Random Walk along the Bilayer Normal Neale, Chris; Madill, Chris; Rauscher, Sarah Journal of Chemical Theory and Computation, Vol. 9, Issue 8 https://doi.org/10.1021/ct301005b	journal	July 2013
Reparameterized United Atom Model for Molecular Dynamics Simulations of Gel and Fluid Phosphatidylcholine Bilayers Tjörnhammar, Richard; Edholm, Olle Journal of Chemical Theory and Computation, Vol. 10, Issue 12 https://doi.org/10.1021/ct500589z	journal	November 2014
The Strength of Hydrogen Bonds in Liquid Water and Around Nonpolar Solutes Silverstein, Kevin A. T.; Haymet, A. D. J.; Dill, Ken A. Journal of the American Chemical Society, Vol. 122, Issue 33 https://doi.org/10.1021/ja000459t	journal	August 2000
Molecular Dynamics Study of the Behavior of Selected Nanoscale Building Blocks in a Gel-Phase Lipid Bilayer Redmill, Patrick S.; McCabe, Clare The Journal of Physical Chemistry B, Vol. 114, Issue 28 https://doi.org/10.1021/jp1039942	journal	June 2010
Unassisted Transport of N -Acetyl- l -tryptophanamide through Membrane: Experiment and Simulation of Kinetics Cardenas, Alfredo E.; Jas, Gouri S.; DeLeon, Kristine Y. The Journal of Physical Chemistry B, Vol. 116, Issue 9 https://doi.org/10.1021/jp2102447	journal	February 2012
Permeability of Small Molecules through a Lipid Bilayer: A Multiscale Simulation Study Orsi, Mario; Sanderson, Wendy E.; Essex, Jonathan W. The Journal of Physical Chemistry B, Vol. 113, Issue 35 https://doi.org/10.1021/jp903248s	journal	August 2009
Permeation Process of Small Molecules across Lipid Membranes Studied by Molecular Dynamics Simulations Marrink, Siewert J.; Berendsen, Herman J. C. The Journal of Physical Chemistry, Vol. 100, Issue 41 https://doi.org/10.1021/jp952956f	journal	January 1996
Exploring the Free Energy Landscape of Solutes Embedded in Lipid Bilayers Jämbeck, Joakim P. M.; Lyubartsev, Alexander P. The Journal of Physical Chemistry Letters, Vol. 4, Issue 11 https://doi.org/10.1021/jz4007993	journal	May 2013
Driving Force for Water Permeation Across Lipid Membranes Qiao, Baofu; Olvera de la Cruz, Monica The Journal of Physical Chemistry Letters, Vol. 4, Issue 19 https://doi.org/10.1021/jz401730s	journal	September 2013
Rationalization of Reduced Penetration of Drugs through Ceramide Gel Phase Membrane Paloncýová, Markéta; DeVane, Russell H.; Murch, Bruce P. Langmuir, Vol. 30, Issue 46 https://doi.org/10.1021/la503289v	journal	November 2014
Strain-induced room-temperature ferroelectricity in SrTiO3 membranes Xu, Ruijuan; Huang, Jiawei; Barnard, Edward S. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16912-3	journal	June 2020
Water permeation through stratum corneum lipid bilayers from atomistic simulations Das, Chinmay; Olmsted, Peter D.; Noro, Massimo G. Soft Matter, Vol. 5, Issue 22 https://doi.org/10.1039/b911257j	journal	January 2009
Aberrant Lipid Organization in Stratum Corneum of Patients with Atopic Dermatitis and Lamellar Ichthyosis Pilgram, Gonneke S. K.; Vissers, Debby C. J.; van der Meulen, Hans Journal of Investigative Dermatology, Vol. 117, Issue 3 https://doi.org/10.1046/j.0022-202x.2001.01455.x	journal	September 2001
Barrier Function of the Skin: “La Raison d'Être” of the Epidermis Madison, Kathi C. Journal of Investigative Dermatology, Vol. 121, Issue 2 https://doi.org/10.1046/j.1523-1747.2003.12359.x	journal	August 2003
A molecular-dynamics study of lipid bilayers: Effects of the hydrocarbon chain length on permeability Sugii, Taisuke; Takagi, Shu; Matsumoto, Yoichiro The Journal of Chemical Physics, Vol. 123, Issue 18 https://doi.org/10.1063/1.2102900	journal	November 2005
Structure and transport of aqueous electrolytes: From simple halides to radionuclide ions Hartkamp, Remco; Coasne, Benoit The Journal of Chemical Physics, Vol. 141, Issue 12 https://doi.org/10.1063/1.4896380	journal	September 2014
Polarity and permeation profiles in lipid membranes Marsh, D. Proceedings of the National Academy of Sciences, Vol. 98, Issue 14 https://doi.org/10.1073/pnas.131023798	journal	July 2001
Position-dependent diffusion coefficients and free energies from Bayesian analysis of equilibrium and replica molecular dynamics simulations Hummer, Gerhard New Journal of Physics, Vol. 7 https://doi.org/10.1088/1367-2630/7/1/034	journal	January 2005
Interaction of Lipophilic Moisturizers on Stratum Corneum Lipid Domains in vitro and in vivo Caussin, J.; Gooris, G. S.; Groenink, H. W. W. Skin Pharmacology and Physiology, Vol. 20, Issue 4 https://doi.org/10.1159/000101387	journal	January 2007
Computer Simulation of Small Molecule Permeation across a Lipid Bilayer: Dependence on Bilayer Properties and Solute Volume, Size, and Cross-Sectional Area Bemporad, D.; Luttmann, C.; Essex, J. W. Biophysical Journal, Vol. 87, Issue 1 https://doi.org/10.1529/biophysj.103.030601	journal	July 2004
Lipid-based nano-delivery systems for skin delivery of drugs and bioactives Hua, Susan Frontiers in Pharmacology, Vol. 6 https://doi.org/10.3389/fphar.2015.00219	journal	September 2015
A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6 Oostenbrink, Chris; Villa, Alessandra; Mark, Alan E. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20090	journal	January 2004
Fast Parallel Algorithms for Short-Range Molecular Dynamics Plimpton, Steve Journal of Computational Physics, Vol. 117, Issue 1 https://doi.org/10.1006/jcph.1995.1039	journal	March 1995
On the permeability of water molecules across vesicular lipid bilayers Lawaczeck, Rüdiger The Journal of Membrane Biology, Vol. 51, Issue 3-4 https://doi.org/10.1007/BF01869086	journal	September 1979
A method for measuring nonelectrolyte partition coefficients between liposomes and water Katz, Yehuda; Diamond, Jared M. The Journal of Membrane Biology, Vol. 17, Issue 1 https://doi.org/10.1007/BF01870173	journal	December 1974
A Novel in Vitro Percutaneous Penetration Model: Evaluation of Barrier Properties with P-Aminobenzoic Acid and Two of Its Derivatives de Jager, Miranda; Groenink, Wouter; Bielsa i. Guivernau, Ruth Pharmaceutical Research, Vol. 23, Issue 5 https://doi.org/10.1007/s11095-006-9909-1	journal	May 2006
Incorporation of surface tension into molecular dynamics simulation of an interface: a fluid phase lipid bilayer membrane Chiu, S. W.; Clark, M.; Balaji, V. Biophysical Journal, Vol. 69, Issue 4 https://doi.org/10.1016/S0006-3495(95)80005-6	journal	October 1995
A comparative study of diffusive and osmotic water permeation across bilayers composed of phospholipids with different head groups and fatty acyl chains Jansen, M.; Blume, A. Biophysical Journal, Vol. 68, Issue 3 https://doi.org/10.1016/S0006-3495(95)80275-4	journal	March 1995
Structure of gel phase saturated lecithin bilayers: temperature and chain length dependence Sun, W. J.; Tristram-Nagle, S.; Suter, R. M. Biophysical Journal, Vol. 71, Issue 2 https://doi.org/10.1016/S0006-3495(96)79290-1	journal	August 1996
Molecular simulation of nonfacilitated membrane permeation Awoonor-Williams, Ernest; Rowley, Christopher N. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 7 https://doi.org/10.1016/j.bbamem.2015.12.014	journal	July 2016
Molecular Dynamics Simulation Study of Permeation of Molecules through Skin Lipid Bilayer Gupta, Rakesh; Sridhar, D. B.; Rai, Beena The Journal of Physical Chemistry B, Vol. 120, Issue 34 https://doi.org/10.1021/acs.jpcb.6b05451	journal	August 2016
Molecular Dynamics Simulation of Skin Lipids: Effect of Ceramide Chain Lengths on Bilayer Properties Gupta, Rakesh; Dwadasi, Balarama Sridhar; Rai, Beena The Journal of Physical Chemistry B, Vol. 120, Issue 49 https://doi.org/10.1021/acs.jpcb.6b08059	journal	November 2016
Structural Properties of Phospholipid-based Bilayers with Long-Chain Alcohol Molecules in the Gel Phase Hartkamp, Remco; Moore, Timothy C.; Iacovella, Christopher R. The Journal of Physical Chemistry B, Vol. 120, Issue 50 https://doi.org/10.1021/acs.jpcb.6b10192	journal	December 2016
Membrane Permeability of Fatty Acyl Compounds Studied via Molecular Simulation Vermaas, Josh V.; Beckham, Gregg T.; Crowley, Michael F. The Journal of Physical Chemistry B, Vol. 121, Issue 50 https://doi.org/10.1021/acs.jpcb.7b08233	journal	November 2017
An Automated Force Field Topology Builder (ATB) and Repository: Version 1.0 Malde, Alpeshkumar K.; Zuo, Le; Breeze, Matthew Journal of Chemical Theory and Computation, Vol. 7, Issue 12 https://doi.org/10.1021/ct200196m	journal	October 2011
Calculating Position-Dependent Diffusivity in Biased Molecular Dynamics Simulations Comer, Jeffrey; Chipot, Christophe; González-Nilo, Fernando D. Journal of Chemical Theory and Computation, Vol. 9, Issue 2 https://doi.org/10.1021/ct300867e	journal	December 2012
Passive Membrane Permeability: Beyond the Standard Solubility-Diffusion Model Parisio, Giulia; Stocchero, Matteo; Ferrarini, Alberta Journal of Chemical Theory and Computation, Vol. 9, Issue 12 https://doi.org/10.1021/ct400690t	journal	November 2013
Simulation of water transport through a lipid membrane Marrink, Siewert-Jan; Berendsen, Herman J. C. The Journal of Physical Chemistry, Vol. 98, Issue 15 https://doi.org/10.1021/j100066a040	journal	April 1994
Cholesterol Effect on Water Permeability through DPPC and PSM Lipid Bilayers: A Molecular Dynamics Study Saito, Hiroaki; Shinoda, Wataru The Journal of Physical Chemistry B, Vol. 115, Issue 51 https://doi.org/10.1021/jp201611p	journal	December 2011
Orientational Dynamics of Water in Phospholipid Bilayers with Different Hydration Levels Zhang, Zhancheng; Berkowitz, Max L. The Journal of Physical Chemistry B, Vol. 113, Issue 21 https://doi.org/10.1021/jp900873d	journal	May 2009
Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations Zhernenkov, Mikhail; Bolmatov, Dima; Soloviov, Dmitry Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11575	journal	May 2016
Molecular dynamics simulation of the effect of bond flexibility on the transport properties of water Raabe, Gabriele; Sadus, Richard J. The Journal of Chemical Physics, Vol. 137, Issue 10 https://doi.org/10.1063/1.4749382	journal	September 2012
Seeking better topical delivery technologies of moisturizing agents for enhanced skin moisturization Kim, Hyeongmin; Kim, Jeong Tae; Barua, Sonia Expert Opinion on Drug Delivery, Vol. 15, Issue 1 https://doi.org/10.1080/17425247.2017.1306054	journal	March 2017
Permeability and Electrical Properties of Thin Lipid Membranes Finkelstein, Alan; Cass, Albert Journal of General Physiology, Vol. 52, Issue 1 https://doi.org/10.1085/jgp.52.1.145	journal	July 1968
Calculating diffusion and permeability coefficients with the oscillating forward-reverse method Holland, Bryan W.; Gray, Chris G.; Tomberli, Bruno Physical Review E, Vol. 86, Issue 3 https://doi.org/10.1103/PhysRevE.86.036707	journal	September 2012
Superior effect of isostearyl isostearate on improvement in stratum corneum water permeability barrier function as examined by the plastic occlusion stress test: Superior effect of isostearyl isostearate Pennick, G.; Harrison, S.; Jones, D. International Journal of Cosmetic Science, Vol. 32, Issue 4 https://doi.org/10.1111/j.1468-2494.2010.00604.x	journal	April 2010

Cited By (5)

Role of Oxidized Lipids in Permeation of H2O2 Through a Lipid Membrane: Molecular Mechanism of an Inhibitor to Promoter Switch Ouchi, Yuya; Unoura, Kei; Nabika, Hideki Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-48954-z	journal	August 2019
Cosmetic benefit of a biomimetic lamellar cream formulation on barrier function or the appearance of fine lines and wrinkles in randomized proof-of-concept clinical studies Nisbet, S.; Mahalingam, H.; Gfeller, C. F. International Journal of Cosmetic Science, Vol. 41, Issue 1 https://doi.org/10.1111/ics.12499	journal	February 2019
Effects of Cholesterol on Water Permittivity of Biomimetic Ion Pair Amphiphile Bilayers: Interplay between Membrane Bending and Molecular Packing Tien, Wu-jhao; Chen, Kun-you; Huang, Fong-yin International Journal of Molecular Sciences, Vol. 20, Issue 13 https://doi.org/10.3390/ijms20133252	journal	July 2019
Water desalination using graphene nanopores: influence of the water models used in simulations K., Vishnu Prasad; Kannam, Sridhar Kumar; Hartkamp, Remco Physical Chemistry Chemical Physics, Vol. 20, Issue 23 https://doi.org/10.1039/c8cp00919h	journal	January 2018
Cosmetic benefits of a novel biomimetic lamellar formulation containing niacinamide in healthy females with oily, blemish‐prone skin in a randomized proof‐of‐concept study Santos-Caetano, J. -P.; Gfeller, C. F.; Mahalingam, H. International Journal of Cosmetic Science, Vol. 42, Issue 1 https://doi.org/10.1111/ics.12576	journal	December 2019

Similar Records

Structural Properties of Phospholipid-based Bilayers with Long-Chain Alcohol Molecules in the Gel Phase

Journal Article · Sun Nov 27 23:00:00 EST 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1480279

Charge Regulation Stabilizes the Formation of Ionic Liquid‐Based Amphiphilic Oligomer Droplet Interface Bilayers

Journal Article · Tue Apr 08 00:00:00 EDT 2025 · Macromolecular Chemistry and Physics · OSTI ID:2573238

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Composition Dependence of Water Permeation Across Multicomponent Gel-Phase Bilayers

Citation Formats

References (60)

Cited By (5)

Similar Records

Related Subjects