158
Views
1
CrossRef citations to date
0
Altmetric
Articles

Accuracy and precision of simulated free energies: water permeation of hydrated DPPC bilayers as a paradigm

&
Pages 466-473 | Received 28 Oct 2018, Accepted 13 Jan 2019, Published online: 07 Feb 2019

References

  • Diamond JM, Katz Y. Interpretation of nonelectrolyte partition coefficients between dimyristoyl lecithin and water. J Membr Biol. 1974;17:121–154. doi: 10.1007/BF01870176
  • Marrink SJ, Berendsen HJC. Simulation of water transport through a lipid membrane. J Phys Chem. 1994;98:4155–4168. doi: 10.1021/j100066a040
  • Marrink SJ, Berendsen HJC. Permeation process of small molecules across lipid membranes studied by molecular dynamics simulations. J Phys Chem. 1996;100:16729–16738. doi: 10.1021/jp952956f
  • Bemporad D, Essex J, Luttmann C. Permeation of small molecules through a lipid bilayer: a computer simulation study. J Phys Chem B. 2004;108:4875–4884. doi: 10.1021/jp035260s
  • Ulander J, Haymet ADJ. Permeation across hydrated DPPC lipid bilayers: simulation of the titrable amphiphilic drug valproic acid. Biophys J. 2003;85:3475–3484. doi: 10.1016/S0006-3495(03)74768-7
  • Orsi M, Sanderson WE, Essex JW. Permeability of small molecules through a lipid bilayer: a multiscale simulation study. J Phys Chem B. 2009;113:12019–12029. doi: 10.1021/jp903248s
  • Santosdos D, Eriksson LA. Permeability of psoralen derivatives in lipid membranes. Biophys J. 2006;91:2464–2474. doi: 10.1529/biophysj.105.077156
  • Fiedler SL, Violi A. Simulation of nanoparticle permeation through a lipid membrane. Biophys J. 2010;99:144–152. doi: 10.1016/j.bpj.2010.03.039
  • Hub JS, Winkler FK, Merrick M, et al. Potentials of mean force and permeabilities for carbon dioxide, ammonia, and water flux across a rhesus protein channel and lipid membranes. J Am Chem Soc. 2009;132:13251–13263. doi: 10.1021/ja102133x
  • Wei C, Pohorille A. Permeation of nucleosides through lipid bilayers. J Phys Chem B. 2011;115:3681–3688. doi: 10.1021/jp112104r
  • Saito H, Shinoda W. Cholesterol effect on water permeability through DPPC and PSM lipid bilayers: a molecular dynamics study. J Phys Chem B. 2011;115:15241–15250. doi: 10.1021/jp201611p
  • Eriksson ESE, Eriksson LA. The influence of cholesterol on the properties and permeability of hypericin derivatives in lipid membranes. J Chem Theory Comput. 2011;7:560–574. doi: 10.1021/ct100528u
  • Issack BB, Peslherbe GH. Effects of cholesterol on the thermodynamics and kinetics of passive transport of water through lipid membranes. J Phys Chem B. 2015;119:9391–9400. doi: 10.1021/jp510497r
  • Lee BL, Kuczera K, Middaugh CR, et al. Permeation of the three aromatic dipeptides through lipid bilayers: experimental and computational study. J Chem Phys. 2015;144:245103.
  • Zwanzig RW. High temperature equation of state by a perturbation method. I. Nonpolar gases. J Chem Phys. 1954;22:1420–1426. doi: 10.1063/1.1740409
  • Kirkwood JG. Statistical mechanics of fluid mixtures. J Chem Phys. 1935;3:300–313. doi: 10.1063/1.1749657
  • Torrie GM, Valleau JP. Nonphysical sampling distributions in monte carlo free-energy estimation: umbrella sampling. J Comput Phys. 1977;23:187–199. doi: 10.1016/0021-9991(77)90121-8
  • Widom B. Some topics in theory of fluids. J Phys Chem. 1963;39:2808–2812. doi: 10.1063/1.1734110
  • Jedlovszky P, Mezei M. Calculation of the free energy profile of H2O, O2, CO, CO2, NO, and CHCl3 in a lipid bilayer with a cavity insertion variant of the widom method. J Am Chem Soc. 2000;122:5125–5131. doi: 10.1021/ja000156z
  • Shinoda W, Mikami M, Baba T, et al. Molecular dynamics study on the effects of chain branching on the physical properties of lipid bilayers: 2. Permeability. J Phys Chem B. 2004;108:9346–9356. doi: 10.1021/jp035998+
  • Darve E, Pohorille A. Calculating free energies using average force. J Chem Phys. 2001;115:9169–9183. doi: 10.1063/1.1410978
  • Laio A, Parrinello M. Escaping free energy minima. Proc Natl Acad Sci USA. 2002;99:12562–12566. doi: 10.1073/pnas.202427399
  • Ghaemi Z, Minozzi M, Carloni P, et al. A novel approach to the investigation of passive molecular permeation through lipid bilayers from atomistic simulations. J Phys Chem B. 2012;116:8714–8721. doi: 10.1021/jp301083h
  • Jämbeck JPM, Lyubartsev AP. Exploring the free energy landscape of solutes embedded in lipid bilayers. J Phys Chem Lett. 2014;4:1781–1787. doi: 10.1021/jz4007993
  • Elber R. A milestoning study of the kinetics of an allosteric transition atomically detailed simulations of deoxy scapharca hemoglobin. Biophys J. 2007;92:L85–L87. doi: 10.1529/biophysj.106.101899
  • Lee BL, Kuczera K. Simulating the free energy of passive membrane permeation for small molecules. Mol Simul. 2018;44:1147–1157. doi: 10.1080/08927022.2017.1407029
  • Awoonor-Williams E, Rowley CN. Molecular simulation of nonfacilitated membrane permeation. Biochim Biophys Acta (BBA) – Biomembr. 2015;1858:1672–1687. doi: 10.1016/j.bbamem.2015.12.014
  • Shinoda W. Permeability across lipid membranes. Biochim et Biophys Acta (BBA)– Biomembr. 2016;1858:2254–2265. doi: 10.1016/j.bbamem.2016.03.032
  • MacCallum JM, Tieleman DP. Computer simulation of the distribution of hexane in a lipid bilayer: spatially resolved free energy, entropy, and enthalpy profiles. J Am Chem Soc. 2006;128:125–130. doi: 10.1021/ja0535099
  • Norman KE, Nymeyer H. Indole localization in lipid membranes revealed by molecular simulation. Biophys J. 2006;91:2046–2054. doi: 10.1529/biophysj.105.080275
  • MacCallum JM, Bennett WFD, Tieleman DP. Distribution of amino acids in a lipid bilayer from computer simulations. BioPhys J. 2008;94:3393–3404. doi: 10.1529/biophysj.107.112805
  • MacCallum JM, Bennett WFD, Tieleman DP. Partitioning of amino acid side chains into lipid bilayers: results from computer simulation and comparison to experiment. J Gen Physiol. 2007;129:371–377. doi: 10.1085/jgp.200709745
  • Wilson MA, Pohorille A. Mechanism of unassisted ion transport across membrane bilayers. J Am Chem Soc. 1996;118:6580–6587. doi: 10.1021/ja9540381
  • Lee CT, Comer J, Herndon C, et al. Simulation-based approaches for determining membrane permeability of small compounds. J Chem Inf Model. 2016;56:721–733. doi: 10.1021/acs.jcim.6b00022
  • Pokhrel N, Maibaum L. Free energy calculations of membrane permeation: challenges due to strong headgroup-solute interactions. J Chem Theory Comput. 2018;14:1762–1771. doi: 10.1021/acs.jctc.7b01159
  • Berendsen HJC, van der Spoel D, van Drunen R. GROMACS: a message-passing parallel molecular dynamics implementation. Comp Phys Comm. 1995;91:43–56. doi: 10.1016/0010-4655(95)00042-E
  • Lindahl E, Hess B, van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J Mol Model. 2001;7:306–317. doi: 10.1007/s008940100045
  • van der Spoel D, Lindahl E, Hess B, et al. GROMACS: fast, flexible, and free. J Comput Chem. 2005;26:1701–1718. doi: 10.1002/jcc.20291
  • Johansson AC, Lindahl E. Position-resolved free energy of solvation for amino acids in lipid membranes from molecular dynamics simulations. Proteins. 2015;70:1332–1344. doi: 10.1002/prot.21629
  • Berger O, Edholm O, Jahnig F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys J. 1997;72:2002–2013. doi: 10.1016/S0006-3495(97)78845-3
  • Berendsen HJC, Postma JPM, van Gunsteren WF, et al. Interaction models for water in relation to protein hydration. In: Pullman B, editor. Intramolecular forces. The Netherlands: Reidel Dordrecht; 1981.
  • Darden T, York D, Pedersen L. Particle mesh Ewald: An N⋅log⁡(N) method for Ewald sums in large systems. J Chem Phys. 1993;98:10089–10092. doi: 10.1063/1.464397
  • Essmann U, Perera L, Berkowitz ML, et al. A smooth particle mesh Ewald method. J Chem Phys. 1995;103:8577–8593. doi: 10.1063/1.470117
  • Mobley DL, Dumont E, Chodera JD, et al. Comparison of charge models for fixed-charge force fields: small-molecule hydration free energies in explicit solvent. J Phys Chem B. 2007;111:2242–2254. doi: 10.1021/jp0667442
  • van Gunsteren WF, Berendsen HJC. A leap-frog algorithm for stochastic dynamics. Mol Simul. 1988;1:173–185. doi: 10.1080/08927028808080941
  • Miyamoto S, Kollman PA. Settle: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem. 1992;13:952–962. doi: 10.1002/jcc.540130805
  • Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comp Phys. 1977;23:327–341. doi: 10.1016/0021-9991(77)90098-5
  • Berendsen HJC, Postma JPM, Gunsterenvan WF, et al. Molecular dynamics with coupling to an external bath. J Chem Phys. 1984;81:3684–3690. doi: 10.1063/1.448118
  • Kumar S, Bouzida D, Swendsen RH, et al. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J Comp Chem. 1992;13:1011–1021. doi: 10.1002/jcc.540130812
  • MacCallum JM, Tieleman DP. Calculation of the water-cyclohexane transfer free energies of neutral amino acid side-chain analogs using the OPLS all-atom force field. J Comput Chem. 2003;24:1930–1935. doi: 10.1002/jcc.10328
  • Abraham MJ, van der Spoel D, Lindahl E, et al., and the GROMACS development team. Avoiding singularities and numerical instabilities in free energy calculations based on molecular simulations, 2018. p. 100–101. www.gromacs.org.
  • Beutler TC, Mark AE, van Schaik RC, et al. GROMACS user manual version 2018. Chem Phys Lett. 1994;222:529–539. doi: 10.1016/0009-2614(94)00397-1
  • Jedlovszky P, Mezei M. Effect of cholesterol on the properties of phospholipid membranes. 2. Free energy profile of small molecules. J Phys Chem B. 2003;107:5322–5332. doi: 10.1021/jp021951x
  • Zhu F, Hummer G. Convergence and error estimation in free energy calculations using the weighted histogram analysis method. J Comput Chem. 2012;33:453–465. doi: 10.1002/jcc.21989
  • Hub JS, de Groot BL, van der Spoel D. g_wham – A free weighted histogram analysis implementation including robust error and autocorrelation estimates. J Chem Theory Comput. 2010;6:3713–3720. doi: 10.1021/ct100494z
  • Mathai JC, Tristram-Nagle S, Nagle JF, et al. Structural determinants of water permeability through the lipid membrane. J Gen Physiol. 2008;131:69–76. doi: 10.1085/jgp.200709848
  • Wenberg CL, van der Spoel D, Hub JS. Large influence of cholesterol on solute partitioning into lipid membranes. J Am Chem Soc. 2012;134:5351–5361. doi: 10.1021/ja211929h
  • Kučerka N, Nagle JF, Sachs JN, et al. Lipid bilayer structure determined by the simultaneous analysis of neutron and X-ray scattering data. Biophys J. 2008;95:2356–2367. doi: 10.1529/biophysj.108.132662
  • Kučerka N, Nieh M-P, Katsaras J. Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biophys Biochim Acta. 2011;1808:2761–2771. doi: 10.1016/j.bbamem.2011.07.022
  • Krylov NA, Pentkovsky VM, Efremov RG. Nontrivial behavior of water in the vicinity and inside lipid bilayers as probed by molecular dynamics simulations. ACS Nano. 2013;7:9428–9442. doi: 10.1021/nn4042392
  • Neale C, Bennett WFD, Tieleman DP, et al. Statistical convergence of equilibrium properties in simulations of molecular solutes embedded in lipid bilayers. Journal of Chemical Theory and Computation. 2011;11:4175–4188. doi: 10.1021/ct200316w
  • Filipe HAL, Moreno MJ, Roǵ T, et al. How to tackle the issues in free energy simulations of long amphiphiles interacting with lipid membranes: convergence and local membrane deformations. J Phys Chem B. 2014;118:3572–3581. doi: 10.1021/jp501622d
  • Parisio G, Stocchero M, Ferrarini A. Passive membrane permeability: beyond the standard solubility-diffusion model. J Chem Theory Comput. 2013;9:5236–5246. doi: 10.1021/ct400690t

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.