References
- Allen, M. P., & Tildesley, D. J. (1989). Computer simulation of liquids (p. 385). Clarendon Press.
- Awoonor-Williams, E., & Rowley, C. N. (2016). Molecular simulation of nonfacilitated membrane permeation. Biochimica et Biophysica Acta, 1858(7 Pt B), 1672–1687. https://doi.org/https://doi.org/10.1016/j.bbamem.2015.12.014
- Bassolino-Klimas, D., Alper, H. E., & Stouch, T. R. (1993). Solute diffusion in lipid bilayer membranes: An atomic level study by molecular dynamics simulation. Biochemistry, 32(47), 12624–12637. https://doi.org/https://doi.org/10.1021/bi00210a010
- Bassolino-Klimas, D., Alper, H. E., & Stouch, T. R. (1995). Mechanism of solute diffusion through lipid bilayer membranes by molecular dynamics simulation. Journal of the American Chemical Society, 117(14), 4118–4129. https://doi.org/https://doi.org/10.1021/ja00119a028
- Bicout, D. J., & Szabo, A. (1998). Electron transfer reaction dynamics in non-Debye solvents. Journal of Chemical Physics, 109(6), 2325–2338. https://doi.org/https://doi.org/10.1063/1.476800
- Bonhenry, D., Tarek, M., & Dehez, F. (2013). Effects of phospholipid composition on the transfer of a small cationic peptide across a model biological membrane. Journal of Chemical Theory and Computation, 9 (12), 5675–5684. https://doi.org/https://doi.org/10.1021/ct400576e
- Brooks, B. R., Brooks, C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., … Karplus, M. (2009). CHARMM: The biomolecular simulation program. Journal of Computational Chemistry, 30 (10), 1545–1614. https://doi.org/https://doi.org/10.1002/jcc.21287
- Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. The Journal of Chemical Physics, 126 (1), 14101. https://doi.org/https://doi.org/10.1063/1.2408420
- Cardenas, A. E., & Elber, R. (2013). Computational study of peptide permeation through membrane: Searching for hidden slow variables. Molecular Physics, 111(22–23), 3565–3578. https://doi.org/https://doi.org/10.1080/00268976.2013.842010
- Cardenas, A. E., & Elber, R. (2014). Modeling kinetics and equilibrium of membranes with fields: Milestoning analysis and implication to permeation. The Journal of Chemical Physics, 141(5), 54101. https://doi.org/https://doi.org/10.1063/1.4891305
- Cardenas, A. E., Jas, G. S., DeLeon, K. Y., Hegefeld, W. A., Kuczera, K., & Elber, R. (2012). Unassisted transport of N-Acetyl-L-tryptophanamide through membrane: Experiment and simulation of kinetics. The Journal of Physical Chemistry. B, 116(9), 2739–2750. https://doi.org/https://doi.org/10.1021/jp2102447
- Carpenter, T. S., Kirshner, D. A., Lau, E. Y., Wong, S. E., Nilmeier, J. P., & Lightstone, F. C. (2014). A method to predict blood-brain barrier permeability of drug-like compounds using molecular dynamics simulations. Biophysical Journal, 107(3), 630–641. https://doi.org/https://doi.org/10.1016/j.bpj.2014.06.024
- Cohen, B. E., & Bangham, A. D. (1972). Diffusion of small non-electrolytes across liposome membranes. Nature, 236(5343), 173–174. https://doi.org/https://doi.org/10.1038/236173a0
- Comer, J., Phillips, J. C., Schulten, K., & Chipot, C. (2014). Multiple-replica strategies for free-energy calculations in NAMD: Multiple-walker adaptive biasing force and walker selection rules. Journal of Chemical Theory and Computation, 10(12), 5276–5285. https://doi.org/https://doi.org/10.1021/ct500874p
- Comer, J., Schulten, K., & Chipot, C. (2014). Calculation of Lipid-bilayer permeabilities using an average force. Journal of Chemical Theory and Computation, 10(2), 554–564. https://doi.org/https://doi.org/10.1021/ct400925s
- Corti, G., Maestrelli, F., Cirri, M., Zerrouk, N., & Mura, P. (2006). Development and evaluation of an in vitro method for prediction of human drug absorption II. Demonstration of the method suitability. European Journal of Pharmaceutical Sciences: Official Journal of the European Federation for Pharmaceutical Sciences, 27(4), 354–362. https://doi.org/https://doi.org/10.1016/j.ejps.2005.11.005
- Di, L., Kerns, E. H., Fan, K., McConnell, O. J., & Carter, G. T. (2003). High throughput artificial membrane permeability assay for blood-brain barrier. European Journal of Medicinal Chemistry, 38(3), 223–232. https://doi.org/https://doi.org/10.1016/s0223-5234(03)00012-6
- Diamond, J. M., & Katz, Y. (1974). Interpretation of nonelectrolyte partition coefficients between dimyristoyl lecithin and water. The Journal of Membrane Biology, 17(2), 121–154. https://doi.org/https://doi.org/10.1007/BF01870176
- Dobson, P. D., & Kell, D. B. (2008). Carrier-mediated cellular uptake of pharmaceutical drugs: An exception or the rule? Nature Reviews. Drug Discovery, 7(3), 205–220. https://doi.org/https://doi.org/10.1038/nrd2438
- Dobson, P. D., Lanthaler, K., Oliver, S. G., & Kell, D. B. (2009). Implications of the dominant role of transporters in drug uptake by cells. Current Topics in Medicinal Chemistry, 9(2), 163–181. https://doi.org/https://doi.org/10.2174/156802609787521616
- Faulkner, C., Santos-Carballal, D., Plant, D. F., & de Leeuw, N. H. (2020). Atomistic molecular dynamics simulations of propofol and fentanyl in phosphatidylcholine lipid bilayers. ACS Omega, 5(24), 14340–14353. https://doi.org/https://doi.org/10.1021/acsomega.0c00813
- Fredriksson, R., Nordstrom, K. J., Stephansson, O., Hagglund, M. G., & Schioth, H. B. (2008). The solute carrier (SLC) complement of the human genome: Phylogenetic classification reveals four major families. FEBS Letters, 582(27), 3811–3816. https://doi.org/https://doi.org/10.1016/j.febslet.2008.10.016
- Giacomini, K. M., Huang, S.-M., Tweedie, D. J., Benet, L. Z., Brouwer, K. L. R., Chu, X., Dahlin, A., Evers, R., Fischer, V., Hillgren, K. M., Hoffmaster, K. A., Ishikawa, T., Keppler, D., Kim, R. B., Lee, C. A., Niemi, M., Polli, J. W., Sugiyama, Y., Swaan, P. W., … Zhang, L. (2010). Membrane transporters in drug development. Nature Reviews. Drug Discovery, 9(3), 215–236. https://doi.org/https://doi.org/10.1038/nrd3028
- Hogben, C. A., Tocco, D. J., Brodie, B. B., & Schanker, L. S. (1959). On the mechanism of intestinal absorption of drugs. The Journal of Pharmacology and Experimental Therapeutics, 125(4), 275–282. PMID: 13642268
- Högerle, M. L., & Winne, D. (1983). Drug absorption by the rat jejunum perfused in situ. Dissociation from the pH-partition theory and role of microclimate-pH and unstirred layer. Naunyn-Schmiedeberg's Archives of Pharmacology, 322(4), 249–255. https://doi.org/https://doi.org/10.1007/BF00508339
- Hu, Y., Ou, S. C., & Patel, S. (2013). Free energetics of arginine permeation into model DMPC lipid bilayers: Coupling of effective counterion concentration and lateral bilayer dimensions. The Journal of Physical Chemistry. B, 117 (39), 11641–11653. https://doi.org/https://doi.org/10.1021/jp404829y
- Hummer, G. (2005). Position-dependent diffusion coefficients and free energies from Bayesian analysis of equilibrium and replica molecular dynamics simulations. New Journal of Physics, 7(34), 34–14. https://doi.org/https://doi.org/10.1088/1367-2630/7/1/034
- Irvine, J. D., Takahashi, L., Lockhart, K., Cheong, J., Tolan, J. W., Selick, H. E., & Grove, J. R. (1999). MDCK (Madin-Darby canine kidney) cells: A tool for membrane permeability screening. Journal of Pharmaceutical Sciences, 88(1), 28–33. https://doi.org/https://doi.org/10.1021/js9803205
- Jämbeck, J. P. M., & Lyubartsev, A. P. (2013). Exploring the free energy landscape of solutes embedded in lipid bilayers. The Journal of Physical Chemistry Letters, 4(11), 1781–1787. https://doi.org/https://doi.org/10.1021/jz4007993
- Jo, S., Kim, T., & Im, W. (2007). Automated builder and database of protein/membrane complexes for molecular dynamics simulations. PLoS One, 2(9), e880. https://doi.org/https://doi.org/10.1371/journal.pone.0000880
- Jo, S., Lim, J. B., Klauda, J. B., & Im, W. (2009). CHARMM-GUI membrane builder for mixed bilayers and its application to yeast membranes. Biophysical Journal, 97(1), 50–58. https://doi.org/https://doi.org/10.1016/j.bpj.2009.04.013
- Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics, 79(2), 926–935. https://doi.org/https://doi.org/10.1063/1.445869
- Kansy, M., Senner, F., & Gubernator, K. (1998). Physicochemical high throughput screening: Parallel artificial membrane permeation assay in the description of passive absorption processes. Journal of Medicinal Chemistry, 41(7), 1007–1010. https://doi.org/https://doi.org/10.1021/jm970530e
- Kästner, J. (2011). Umbrella sampling. Wiley Interdisciplinary Reviews: Computational Molecular Science, 1(6), 932–942. https://doi.org/https://doi.org/10.1002/wcms.66
- Khuntawee, W., Wolschann, P., Rungrotmongkol, T., Wong-Ekkabut, J., & Hannongbua, S. (2015). Molecular dynamics simulations of the interaction of beta cyclodextrin with a lipid bilayer. Journal of Chemical Information and Modeling, 55(9), 1894–1902. https://doi.org/https://doi.org/10.1021/acs.jcim.5b00152
- Klauda, J. B., Roberts, M. F., Redfield, A. G., Brooks, B. R., & Pastor, R. W. (2008). Rotation of lipids in membranes: Molecular dynamics simulation, 31P spin-lattice relaxation, and rigid-body dynamics. Biophysical Journal, 94(8), 3074–3083. https://doi.org/https://doi.org/10.1529/biophysj.107.121806
- Kuczera, K., Unruh, J., Johnson, C. K., & Jas, G. S. (2010). Reorientations of aromatic amino acids and their side chain models: Anisotropy measurements and molecular dynamics simulations. The Journal of Physical Chemistry A, 114(1), 133–142. https://doi.org/https://doi.org/10.1021/jp907382h
- Kumar, S., Bouzida, D., Swendsen, R., Kollman, P., & Rosenberg, J. (1992). The weighted histogram analysis method for free-energy calculations on biomolecules.1. The method. Journal of Computational Chemistry, 13(8), 1011–1021. https://doi.org/https://doi.org/10.1002/jcc.540130812
- Lee, B. L., & Kuczera, K. (2018). Simulating the free energy of passive membrane permeation for small molecules. Molecular Simulation, 44 (13–14), 1147–1157. https://doi.org/https://doi.org/10.1080/08927022.2017.1407029
- Lee, B. L., Kuczera, K., Middaugh, C. R., & Jas, G. S. (2016). Permeation of the three aromatic dipeptides through lipid bilayers: Experimental and computational study. The Journal of Chemical Physics, 144(24), 245103. https://doi.org/https://doi.org/10.1063/1.4954241
- Leftin, A., Molugu, T. R., Job, C., Beyer, K., & Brown, M. F. (2014). Area per lipid and cholesterol interactions in membranes from separated local-field (13)C NMR spectroscopy. Biophysical Journal, 107(10), 2274–2286. https://doi.org/https://doi.org/10.1016/j.bpj.2014.07.044
- Liu, Y., & Nagle, J. F. (2004). Diffuse scattering provides material parameters and electron density profiles of biomembranes. Physical Review E, 69(4), 40901. https://doi.org/https://doi.org/10.1103/PhysRevE.69.040901
- Marrink, S.-J., & Berendsen, H. J. C. (1994). Simulation of water transport through a lipid membrane. The Journal of Physical Chemistry, 98(15), 4155–4168. https://doi.org/https://doi.org/10.1021/j100066a040
- Marrink, S. J., & Berendsen, H. J. C. (1996). Permeation process of small molecules across lipid membranes studied by molecular dynamics simulations. The Journal of Physical Chemistry, 100 (41), 16729–16738. https://doi.org/https://doi.org/10.1021/jp952956f
- Meier, M., Blatter, X. L., Seelig, A., & Seelig, J. (2006). Interaction of verapamil with lipid membranes and P-glycoprotein: Connecting thermodynamics and membrane structure with functional activity. Biophysical Journal, 91(8), 2943–2955. https://doi.org/https://doi.org/10.1529/biophysj.106.089581
- Mills, T. T., Toombes, G. E. S., Tristram-Nagle, S., Smilgies, D. M., Feigenson, G. W., & Nagle, J. F. (2008). Order parameters and areas in fluid-phase oriented lipid membranes using wide angle x-ray scattering. Biophysical Journal, 95(2), 669–681. https://doi.org/https://doi.org/10.1529/biophysj.107.127845
- Neale, C., Bennett, W. F. D., Tieleman, D. P., & Pomes, R. (2011). Statistical convergence of equilibrium properties in simulations of molecular solutes embedded in lipid bilayers. Journal of Chemical Theory and Computation, 7 (12), 4175–4188. https://doi.org/https://doi.org/10.1021/ct200316w
- Nitschke, N., Atkovska, K., & Hub, J. S. (2016). Accelerating potential of mean force calculations for lipid membrane permeation: System size, reaction coordinate, solute-solute distance, and cutoffs. The Journal of Chemical Physics, 145 (12), 125101. https://doi.org/https://doi.org/10.1063/1.4963192
- Orsi, M., Sanderson, W. E., & Essex, J. W. (2009). Permeability of small molecules through a lipid bilayer: A multiscale simulation study. The Journal of Physical Chemistry B, 113(35), 12019–12029. https://doi.org/https://doi.org/10.1021/jp903248s
- Parisio, G., Stocchero, M., & Ferrarini, A. (2013). Passive membrane permeability: Beyond the standard solubility-diffusion model. Journal of Chemical Theory and Computation, 9(12), 5236–5246. https://doi.org/https://doi.org/10.1021/ct400690t
- Pastor, R. W., & MacKerell, A. D. (2011). Development of the CHARMM force field for lipids. The Journal of Physical Chemistry Letters, 2(13), 1526–1532. https://doi.org/https://doi.org/10.1021/jz200167q
- Petersen, H. G. (1995). Accuracy and efficiency of the particle mesh Ewald method. Journal of Chemical Physics, 103(9), 3668–3679. https://doi.org/https://doi.org/10.1063/1.470043
- Petrache, H. I., Tristram-Nagle, S., Gawrisch, K., Harries, D., Parsegian, V. A., & Nagle, J. F. (2004). Structure and fluctuations of charged phosphatidylserine bilayers in the absence of salt. Biophysical Journal, 86(3), 1574–1586. https://doi.org/https://doi.org/10.1016/S0006-3495(04)74225-3
- Pronk, S., Pall, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England), 29(7), 845–854. https://doi.org/https://doi.org/10.1093/bioinformatics/btt055
- Ramachandran, G., Ramakrishnan, C., & Sasisekharan, V. (1963). Stereochemistry of polypeptide chain configurations. Journal of Molecular Biology, 7, 95–99. https://doi.org/https://doi.org/10.1016/S0022-2836(63)80023-6
- Roux, B. (1995). The calculation of the potential of mean force using computer-simulations. Computer Physics Communications, 91(1–3), 275–282. https://doi.org/https://doi.org/10.1016/0010-4655(95)00053-I
- Schulten, K., Schulten, Z., & Szabo, A. (1981). Dynamics of reactions involving diffusive barrier crossing. Journal of Chemical Physics, 74(8), 4426–4432. https://doi.org/https://doi.org/10.1063/1.441684
- Seelig, A. (2007). The role of size and charge for blood–brain barrier permeation of drugs and fatty acids. Journal of Molecular Neuroscience, 33(1), 32–41. https://doi.org/https://doi.org/10.1007/s12031-007-0055-y
- Shinoda, W. (2016). Permeability across lipid membranes. Biochimica et Biophysica Acta, 1858(10), 2254–2265. https://doi.org/https://doi.org/10.1016/j.bbamem.2016.03.032
- Snyder, R. G., Tu, K., Klein, M. L., Mendelssohn, R., Strauss, H. L., W., & Sun, W. (2002). Acyl chain conformation and packing in dipalmotoylphosphatidylcholine bilayers from MD simulation and IR spectroscopy. The Journal of Physical Chemistry B, 106(24), 6273–6288. https://doi.org/https://doi.org/10.1021/jp012145d
- Souaille, M., & Roux, B. (2001). Extension to the weighted histogram analysis method: Combining umbrella sampling with free energy calculations. Computer Physics Communications, 135(1), 40–57. https://doi.org/https://doi.org/10.1016/S0010-4655(00)00215-0
- Sugii, T., Takagi, S., & Matsumoto, Y. (2005). A molecular-dynamics study of lipid bilayers: Effects of the hydrocarbon chain length on permeability. The Journal of Chemical Physics, 123 (18), 184714. https://doi.org/https://doi.org/10.1063/1.2102900
- Tobias, D. J., & Brooks, C. L. (1992). Conformational equilibrium in the alanine dipeptide in the gas-phase and aqueous-solution - a comparison of theoretical results. The Journal of Physical Chemistry, 96(9), 3864–3870. https://doi.org/https://doi.org/10.1021/j100188a054
- Torrie, G., & Valleau, J. (1977). Non-physical sampling distributions in Monte-Carlo free-energy estimation - Umbrella sampling. Journal of Computational Physics, 23(2), 187–199. https://doi.org/https://doi.org/10.1016/0021-9991(77)90121-8
- Tu, K., Tobias, D. J., Blasie, J. K., & Klein, M. L. (1996). Molecular dynamics investigation of the structure of a fully hydrated gel phase dipalmitoylphosphatidylcholine bilayer. Biophysical Journal, 70(2), 595–608. https://doi.org/https://doi.org/10.1016/S0006-3495(96)79623-6
- Ulander, J., & Haymet, A. D. J. (2003). Permeation across hydrated DPPC lipid bilayers: Simulation of the titrable amphiphilic drug valproic acid. Biophysical Journal, 85(6), 3475–3484. https://doi.org/https://doi.org/10.1016/S0006-3495(03)74768-7
- Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., & Mackerell, A. D. (2010). CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. Journal of Computational Chemistry, 31(4), 671–690. https://doi.org/https://doi.org/10.1002/jcc.21367
- Vaz, W. L. C., & Almeida, P. F. (1991). Microscopic versus macroscopic diffusion in one-component fluid phase lipid bilayer membranes. Biophysical Journal, 60(6), 1553–1554. https://doi.org/https://doi.org/10.1016/S0006-3495(91)82190-7
- Venable, R. M., Brooks, B. R., & Pastor, R. W. (2000). Molecular dynamics simulations of gel (LβI) phase lipid bilayers in constant and constant surface area ensembles. Journal of Chemical Physics, 112(10), 4822–4832. https://doi.org/https://doi.org/10.1063/1.481085
- Wei, C., & Pohorille, A. (2014). Flip-flop of oleic acid in a phospholipid membrane: Rate and mechanism. The Journal of Physical Chemistry B, 118 (45), 12919–12926. https://doi.org/https://doi.org/10.1021/jp508163e
- Wohnsland, F., & Faller, B. (2001). High-throughput permeability pH profile and high-throughput alkane/water log P with artificial membranes. Journal of Medicinal Chemistry, 44(6), 923–930. https://doi.org/https://doi.org/10.1021/jm001020e
- Wu, E. L., Cheng, X., Jo, S., Rui, H., Song, K. C., Dávila-Contreras, E. M., Qi, Y., Lee, J., Monje-Galvan, V., Venable, R. M., Klauda, J. B., & Im, W. (2014). CHARMM-GUI Membrane Builder toward realistic biological membrane simulations. Journal of Computational Chemistry, 35(27), 1997–2004. https://doi.org/https://doi.org/10.1002/jcc.23702
- Xiang, T. X., & Anderson, B. D. (1998). Influence of chain ordering on the selectivity of dipalmitoyl phosphatidylcholine bilayer membranes for permeant size and shape. Biophysical Journal, 75(6), 2658–2671. https://doi.org/https://doi.org/10.1016/S0006-3495(98)77711-2
- Xiang, T.-X., & Anderson, B. D. (2006). Liposomal drug transport: A molecular perspective from molecular dynamics simulations in lipid bilayers. Advanced Drug Delivery Reviews, 58(12–13), 1357–1378. https://doi.org/https://doi.org/10.1016/j.addr.2006.09.002
- Zhu, C., Jiang, L., Chen, T. M., & Hwang, K. K. (2002). A comparative study of artificial membrane permeability assay for high throughput profiling of drug absorption potential. European Journal of Medicinal Chemistry, 37(5), 399–407. https://doi.org/https://doi.org/10.1016/S0223-5234(02)01360-0
- Zusman, L. D. (1980). Outer-sphere electron-transfer in polar-solvents. Chemical Physics, 49(2), 295–304. https://doi.org/https://doi.org/10.1016/0301-0104(80)85267-0