The partition and transport behavior of cytotoxic ionic liquids (ILs) through the DPPC bilayer: Insights from molecular dynamics simulation

References

• Allen WJ, Lemkul JA, Bevan DR. 2009. GridMAT-MD: a grid-based membrane analysis tool for use with molecular dynamics. J Comput Chem 30:1952–1958.
   PubMed Web of Science ®Google Scholar
• Azizi K, Koli MG. 2016. Molecular dynamics simulations of Oxprenolol and Propranolol in a DPPC lipid bilayer. J Mol Graph Model 64:153–164.
   PubMed Web of Science ®Google Scholar
• Benedetto A. 2017. Room-temperature ionic liquids meet bio-membranes: the state-of-the-art. Biophys Rev 1–12.
   PubMedGoogle Scholar
• Benedetto A, Ballone P. 2015. Room temperature ionic liquids meet biomolecules: a microscopic view of structure and dynamics. ACS Sustain Chem Eng 4:392–412.
   Web of Science ®Google Scholar
• Benedetto A, Ballone P. 2016. Room temperature ionic liquids interacting with bio-molecules: an overview of experimental and computational studies. Philos Mag 96:870–894.
   Web of Science ®Google Scholar
• Benedetto A, Bingham RJ, Ballone P. 2015. Structure and dynamics of POPC bilayers in water solutions of room temperature ionic liquids. J Chem Phys 142:124706.
   PubMed Web of Science ®Google Scholar
• Benedetto A, Heinrich F, Gonzalez MA, Fragneto G, Watkins E, Ballone P. 2014. Structure and stability of phospholipid bilayers hydrated by a room-temperature ionic liquid/water solution: a neutron reflectometry study. J Phys Chem B 118:12192–12206.
   PubMed Web of Science ®Google Scholar
• Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J. 1981. Interaction models for water in relation to protein hydration. In Intermolecular forces. Berlin: Springer, 331–342.
   Google Scholar
• Berger O, Edholm O, Jähnig F. 1997. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys J 72:2002.
   PubMed Web of Science ®Google Scholar
• Biswal HS. 2015. Hydrogen bonds involving sulfur: new insights from ab initio calculations and gas phase laser spectroscopy. In Noncovalent forces. Berlin: Springer, 15–45.
   Google Scholar
• Boggara MB, Krishnamoorti R. 2010. Partitioning of nonsteroidal antiinflammatory drugs in lipid membranes: a molecular dynamics simulation study. Biophys J 98:586–595.
   PubMed Web of Science ®Google Scholar
• Canzar S, El-Kebir M, Pool R, Elbassioni K, Malde AK, Mark AE, et al. 2013. Charge group partitioning in biomolecular simulation. J Comput Biol 20:188–198.
   PubMed Web of Science ®Google Scholar
• Carter EB, Culver SL, Fox PA, Goode RD, Ntai I, Tickell MD, et al. 2004. Sweet success: ionic liquids derived from non-nutritive sweeteners. Chem Commun 6:630–631.
   PubMed Web of Science ®Google Scholar
• Cevc G. 1990. Membrane electrostatics. Biochim Biophys Acta 1031:311–382.
   PubMed Web of Science ®Google Scholar
• Clarke RJ. 2001. The dipole potential of phospholipid membranes and methods for its detection. Adv Colloid Interface Sci 89:263–281.
   PubMed Web of Science ®Google Scholar
• Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. 1995. A smooth particle mesh ewald method. J Chem Phys 103:8577–8593.
   Web of Science ®Google Scholar
• Fujita K, Forsyth M, MacFarlane DR, Reid RW, Elliott GD. 2006. Unexpected improvement in stability and utility of cytochrome c by solution in biocompatible ionic liquids. Biotechnol Bioeng 94:1209–1213.
   PubMed Web of Science ®Google Scholar
• Fujita K, MacFarlane DR, Forsyth M. 2005. Protein solubilising and stabilising ionic liquids. Chem Commun 38:4804–4806.
   PubMed Web of Science ®Google Scholar
• Gulati M, Grover M, Singh S, Singh M. 1998. Lipophilic drug derivatives in liposomes. Int J Pharm 165:129–168.
   Web of Science ®Google Scholar
• Gullapalli RR, Demirel MC, Butler PJ. 2008. Molecular dynamics simulations of DiI-C18(3) in a DPPC lipid bilayer. Phys Chem Chem Phys 10:3548–3560.
   PubMed Web of Science ®Google Scholar
• Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. 1997. LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18:1463–1472.
   Web of Science ®Google Scholar
• Hess B, Kutzner C, Van Der Spoel D, Lindahl E. 2008. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4:435–447.
   PubMed Web of Science ®Google Scholar
• Hockney RW, Goel SP, Eastwood JW. 1974. Quiet high-resolution computer models of a plasma. J Comput Phys 14:148–158.
   Web of Science ®Google Scholar
• Högberg CJ, Lyubartsev AP. 2008. Effect of local anesthetic lidocaine on electrostatic properties of a lipid bilayer. Biophys J 94:525–531.
   PubMed Web of Science ®Google Scholar
• Hough WL, Rogers RD. 2007. Ionic liquids then and now: from solvents to materials to active pharmaceutical ingredients. Bull Chem Soc Jpn 80:2262–2269.
   Web of Science ®Google Scholar
• Hub JS, De Groot BL, Van Der Spoel D. 2010. G_wham—A free weighted histogram analysis implementation including robust error and autocorrelation estimates. J Chem Theory Comput 6:3713–3720.
   Web of Science ®Google Scholar
• Hughes ZE, Mark AE, Mancera RL. 2012. Molecular dynamics simulations of the interactions of DMSO with DPPC and DOPC phospholipid membranes. J Phys Chem B 116:11911–11923.
   PubMed Web of Science ®Google Scholar
• Humphrey W, Dalke A, Schulten K. 1996. “VMD–visual molecular dynamics”. J Mol Graph 14:33–38.
   PubMed Web of Science ®Google Scholar
• Jastorff B, Mölter K, Behrend P, Bottin-Weber U, Filser J, Heimers A, et al. 2005. Progress in evaluation of risk potential of ionic liquids-basis for an eco-design of sustainable products. Green Chem 7:362–372.
   Web of Science ®Google Scholar
• Jastorff B, Störmann R, Ranke J, Mölter K, Stock F, Oberheitmann B, et al. 2003. How hazardous are ionic liquids? Structure–activity relationships and biological testing as important elements for sustainability evaluation. Green Chem 5:136–142.
   Web of Science ®Google Scholar
• Kandt C, Ash WL, Tieleman DP. 2007. Setting up and running molecular dynamics simulations of membrane proteins. Methods 41:475–488.
   PubMed Web of Science ®Google Scholar
• Koziara KB, Stroet M, Malde AK, Mark AE. 2014. Testing and validation of the Automated Topology Builder (ATB) version 2.0: prediction of hydration free enthalpies. J Comput Aided Mol Des 28:221–233.
   PubMed Web of Science ®Google Scholar
• Kučerka N, Nieh M-P, Katsaras J. 2011. Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biochim Biophys Acta Biomembr 1808:2761–2771.
   PubMed Web of Science ®Google Scholar
• Kumar S, Rosenberg JM, Bouzida D, Swendsen RH, Kollman PA. 1992. The weighted histogram analysis method for free-energy calculations on biomolecules. J Comput Chem 13:1011–1021.
   Web of Science ®Google Scholar
• Marrink SJ, Lindahl E, Edholm O, Mark AE. 2001. Simulation of the spontaneous aggregation of phospholipids into bilayers. J Am Chem Soc 123:8638–8639.
   PubMed Web of Science ®Google Scholar
• Mojumdar EH, Lyubartsev AP. 2010. Molecular dynamics simulations of local anesthetic articaine in a lipid bilayer. Biophys Chem 153:27–35.
   PubMed Web of Science ®Google Scholar
• Moniruzzaman M, Kamiya N, Goto M. 2010. Ionic liquid based microemulsion with pharmaceutically accepted components: formulation and potential applications. J Colloid Interface Sci 352:136–142.
   PubMed Web of Science ®Google Scholar
• Mosaddeghi H, Alavi S, Kowsari MH, Najafi B. 2012. Simulations of structural and dynamic anisotropy in nano-confined water between parallel graphite plates. J Chem Phys 137:184703.
   PubMed Web of Science ®Google Scholar
• Nagle JF, Zhang R, Tristram-Nagle S, Sun W, Petrache HI, Suter RM. 1996. X-ray structure determination of fully hydrated Lα, phase dipalmitoylphosphatidylcholine bilayers. Biophys J 70:1419.
   PubMed Web of Science ®Google Scholar
• Ohno H. 2011. Electrochemical aspects of ionic liquids. Hoboken (NJ): John Wiley & Sons.
   Google Scholar
• Parrinello M, Rahman A. 1980. Crystal structure and pair potentials: a molecular-dynamics study. Phys Rev Lett 45:1196.
   Web of Science ®Google Scholar
• Patra M, Salonen E, Terama E, Vattulainen I, Faller R, Lee BW, et al. 2006. Under the Influence of Alcohol: the effect of ethanol and methanol on lipid bilayers. Biophys J 90:1121–1135.
   PubMed Web of Science ®Google Scholar
• Pernak J, Stefaniak F, Węglewski J. 2005. Phosphonium acesulfamate based ionic liquids. European J Org Chem 2005:650–652.
   Web of Science ®Google Scholar
• Petkovic M, Ferguson JL, Gunaratne HQN, Ferreira R, Leitao MC, Seddon KR, et al. 2010. Novel biocompatible cholinium-based ionic liquids—toxicity and biodegradability. Green Chem 12:643–649.
   Web of Science ®Google Scholar
• Petrache HI, Dodd SW, Brown MF. 2000. Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by 2H NMR spectroscopy. Biophys J 79:3172–3192.
   PubMed Web of Science ®Google Scholar
• Snyman J. 2005. Practical mathematical optimization: an introduction to basic optimization theory and classical and new gradient-based algorithms. Berlin: Springer Science & Business Media.
   Google Scholar
• Stoimenovski J, MacFarlane DR, Bica K, Rogers RD. 2010. Crystalline vs. ionic liquid salt forms of active pharmaceutical ingredients: a position paper. Pharm Res 27:521–526.
   PubMed Web of Science ®Google Scholar
• Stolte S, Arning J, Bottin-Weber U, Matzke M, Stock F, Thiele K, et al. 2006. Anion effects on cytotoxicity of ionic liquids. Green Chem 8:621–629.
   Web of Science ®Google Scholar
• Tieleman DP, MacCallum JL, Ash WL, Kandt C, Xu Z, Monticelli L. 2006. Membrane protein simulations with a united-atom lipid and all-atom protein model: lipid-protein interactions, side chain transfer free energies and model proteins. J Phys Condens Matter 18:S1221.
   PubMed Web of Science ®Google Scholar
• Torrie GM, Valleau JP. 1977. Nonphysical sampling distributions in Monte Carlo free-energy estimation – Umbrella sampling. J Comput Phys 23:187–199.
   Web of Science ®Google Scholar
• Ulmschneider JP, Ulmschneider MB. 2009. United atom lipid parameters for combination with the optimized potentials for liquid simulations all-atom force field. J Chem Theory Comput 5:1803–1813.
   PubMed Web of Science ®Google Scholar
• van der Spoel D, van Maaren PJ, Larsson P, Timneanu N. 2006. Thermodynamics of hydrogen bonding in hydrophilic and hydrophobic media. J Phys Chem B 110:4393–4398.
   PubMed Web of Science ®Google Scholar
• Vrikkis RM, Fraser KJ, Fujita K, MacFarlane DR, Elliott GD. 2009. Biocompatible ionic liquids: a new approach for stabilizing proteins in liquid formulation. J Biomech Eng 131:74514.
   Web of Science ®Google Scholar
• Wang L, Bose PS, Sigworth FJ. 2006. Using cryo-EM to measure the dipole potential of a lipid membrane. Proc Natl Acad Sci USA 103:18528–18533.
   PubMed Web of Science ®Google Scholar
• Weaver KD, Kim HJ, Sun J, MacFarlane DR, Elliott GD. 2010. Cyto-toxicity and biocompatibility of a family of choline phosphate ionic liquids designed for pharmaceutical applications. Green Chem 12:507–513.
   Web of Science ®Google Scholar
• Weaver KD, Van Vorst MP, Vijayaraghavan R, MacFarlane DR, Elliott GD. 2013. Interaction of choline salts with artificial biological membranes: DSC studies elucidating cellular interactions. Biochim Biophys Acta Biomember 1828:1856–1862.
   PubMed Web of Science ®Google Scholar
• Welton T. 1999. Room-temperature ionic liquids. Solvents for synthesis and catalysis. Chem Rev 99:2071–2084.
   PubMed Web of Science ®Google Scholar
• Wennberg CL, Van Der Spoel D, Hub JS. 2012. Large influence of cholesterol on solute partitioning into lipid membranes. J Am Chem Soc 134:5351–5361.
   PubMed Web of Science ®Google Scholar
• Wohlert J, Edholm O. 2004. The range and shielding of dipole-dipole interactions in phospholipid bilayers. Biophys J 87:2433–2445.
   PubMed Web of Science ®Google Scholar
• Wohlert J, Edholm O. 2006. Dynamics in atomistic simulations of phospholipid membranes: nuclear magnetic resonance relaxation rates and lateral diffusion. J Chem Phys 125:204703.
   PubMed Web of Science ®Google Scholar
• Xu W, Angell CA. 2003. Solvent-free electrolytes with aqueous solution-like conductivities. Science 302:422–425.
   PubMed Web of Science ®Google Scholar
• Yoo B, Jing B, Jones SE, Lamberti GA, Zhu Y, Shah JK, Maginn EJ. 2016. Molecular mechanisms of ionic liquid cytotoxicity probed by an integrated experimental and computational approach. Sci Rep 6:19889.
   PubMed Web of Science ®Google Scholar
• Yousefpour A, Amjad Iranagh S, Nademi Y, Modarress H. 2013. Molecular dynamics simulation of nonsteroidal antiinflammatory drugs, naproxen and relafen, in a lipid bilayer membrane. Int J Quantum Chem 113:1919–1930.
   Web of Science ®Google Scholar