Computational study of DMPC liposomes loaded with the N-(2-Hydroxyphenyl)-2-propylpentanamide (HO-AAVPA) and determination of its antiproliferative activity in vitro in NIH-3T3 cells

References

• Allen, T. M., & Cullis, P. R. (2013). Liposomal drug delivery systems: From concept to clinical applications. Advanced Drug Delivery Reviews, 65(1), 36–48. https://doi.org/10.1016/j.addr.2012.09.037
   PubMed Web of Science ®Google Scholar
• Almeida, P. F., Vaz, W. L., & Thompson, T. E. (1992). Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: A free volume analysis. Biochemistry, 31(29), 6739–6747. https://doi.org/10.1021/bi00144a013
   PubMed Web of Science ®Google Scholar
• Batrakova, E. V., & Kabanov, A. V. (2008). Pluronic block copolymers: Evolution of drug delivery concept from inert nanocarriers to biological response modifiers. Journal of Controlled Release, 130(2), 98–106. https://doi.org/10.1016/j.jconrel.2008.04.013
   PubMed Web of Science ®Google Scholar
• BIOVIA. (2015). Discovery Studio. 16th ed. Dassault Systèmes.
   Google Scholar
• Briuglia, M. L., Rotella, C., McFarlane, A., & Lamprou, D. A. (2015). Influence of cholesterol on liposome stability and on in vitro drug release. Drug Delivery and Translational Research, 5(3), 231–242. https://doi.org/10.1007/s13346-015-0220-8
   PubMed Web of Science ®Google Scholar
• ChemAxon. (2012). Marvin Sketch 5.10.4. 5.10.4 ed. ChemAxon.
   Google Scholar
• Cheng, Y., & Ji, Y. (2019). RGD-modified polymer and liposome nanovehicles: Recent research progress for drug delivery in cancer therapeutics. European Journal of Pharmaceutical Sciences, 128, 8–17. https://doi.org/10.1016/j.ejps.2018.11.023
   PubMed Web of Science ®Google Scholar
• Chiu, M. H., & Prenner, E. J. (2011). Differential scanning calorimetry: An invaluable tool for a detailed thermodynamic characterization of macromolecules and their interactions. Journal of Pharmacy & Bioallied Sciences, 3(1), 39–59. https://doi.org/10.4103/0975-7406.76463
   PubMedGoogle Scholar
• Chiu, S. W., Jakobsson, E., Mashl, R. J., & Scott, H. L. (2002). Cholesterol-induced modifications in lipid bilayers: A simulation study. Biophysical Journal, 83(4), 1842–1853. https://doi.org/10.1016/s0006-3495(02)73949-0
   PubMed Web of Science ®Google Scholar
• Contis-Montes de Oca, A., Rodarte-Valle, E., Rosales-Hernandez, M. C., Abarca-Rojano, E., Rojas-Hernandez, S., Fragoso-Vazquez, M. J., Mendieta-Wejebe, J. E., Correa-Basurto, A. M., Vazquez-Moctezuma, I., & Correa-Basurto, J. (2018). N-(2'-Hydroxyphenyl)-2-propylpentanamide (OH-VPA), a histone deacetylase inhibitor, induces the release of nuclear HMGB1 and modifies ROS levels in HeLa cells. Oncotarget, 9(70), 33368–33381. https://doi.org/10.18632/oncotarget.26077
   PubMedGoogle Scholar
• Daeihamed, M., Haeri, A., Ostad, S. N., Akhlaghi, M. F., & Dadashzadeh, S. (2017). Doxorubicin-loaded liposomes: Enhancing the oral bioavailability by modulation of physicochemical characteristics. Nanomedicine (London, England), 12(10), 1187–1202. https://doi.org/10.2217/nnm-2017-0007
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• Efimova, S. S., & Ostroumova, O. S. (2020). The disordering effect of plant metabolites on model lipid membranes of various thickness. Cell and Tissue Biology, 14(5), 388–397. https://doi.org/10.1134/S1990519X2005003X
   Google Scholar
• Falck, E., Patra, M., Karttunen, M., Hyvonen, M. T., & Vattulainen, I. (2004). Impact of cholesterol on voids in phospholipid membranes. The Journal of Chemical Physics, 121(24), 12676–12689. https://doi.org/10.1063/1.1824033
   PubMed Web of Science ®Google Scholar
• Haberkorn, R. A., Griffin, R. G., Meadows, M. D., & Oldfield, E. (1977). Deuterium nuclear magnetic resonance investigation of the dipalmitoyl lecithin-cholesterol-water system. Journal of the American Chemical Society, 99(22), 7353–7355. https://doi.org/10.1021/ja00464a043
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(sici)1096-987x(199709)18:12 < 1463::aid-jcc4 > 3.0.co;2-h
   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. Journal of Chemical Theory and Computation, 4(3), 435–447. https://doi.org/10.1021/ct700301q
   PubMed Web of Science ®Google Scholar
• Hoover, W. G. (1985). Canonical dynamics: Equilibrium phase-space distributions. Physical Review A, General Physics, 31(3), 1695–1697. https://doi.org/10.1103/PhysRevA.31.1695
   PubMedGoogle Scholar
• Huang, J., & MacKerell, A. D., Jr. (2013). CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data. Journal of Computational Chemistry, 34(25), 2135–2145. https://doi.org/10.1002/jcc.23354
   PubMed Web of Science ®Google Scholar
• Inamura, K., Komizu, Y., Yamakuchi, M., Ishida, S., Matsumoto, Y., & Matsushita, T. (2019). Inhibitory effect of hybrid liposomes on the growth of liver cancer stem cells. Biochemical and Biophysical Research Communications, 509(1), 268–274. https://doi.org/10.1016/j.bbrc.2018.12.118
   PubMed Web of Science ®Google Scholar
• Jo, S., Kim, T., Iyer, V. G., & Im, W. (2008). CHARMM-GUI: a web-based graphical user interface for CHARMM. Journal of Computational Chemistry, 29(11), 1859–1865. https://doi.org/10.1002/jcc.20945
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Kaddah, S., Khreich, N., Kaddah, F., Charcosset, C., & Greige-Gerges, H. (2018). Cholesterol modulates the liposome membrane fluidity and permeability for a hydrophilic molecule. Food and Chemical Toxicology, 113, 40–48. https://doi.org/10.1016/j.fct.2018.01.017
   PubMed Web of Science ®Google Scholar
• Khajeh, A., & Modarress, H. (2014). The influence of cholesterol on interactions and dynamics of ibuprofen in a lipid bilayer. Biochimica et Biophysica Acta, 1838(10), 2431–2438. https://doi.org/10.1016/j.bbamem.2014.05.029
   PubMed Web of Science ®Google Scholar
• Kheirolomoom, A., & Ferrara, K. W. (2007). Cholesterol transport from liposomal delivery vehicles. Biomaterials, 28(29), 4311–4320. https://doi.org/10.1016/j.biomaterials.2007.06.008
   PubMed Web of Science ®Google Scholar
• Khelashvili, G., Pabst, G., & Harries, D. (2010). Cholesterol orientation and tilt modulus in DMPC bilayers. The Journal of Physical Chemistry B, 114(22), 7524–7534. https://doi.org/10.1021/jp101889k
   PubMed Web of Science ®Google Scholar
• Kucerka, N., Kiselev, M. A., & Balgavy, P. (2004). Determination of bilayer thickness and lipid surface area in unilamellar dimyristoylphosphatidylcholine vesicles from small-angle neutron scattering curves: A comparison of evaluation methods. European Biophysics Journal, 33(4), 328–334. https://doi.org/10.1007/s00249-003-0349-0
   PubMed Web of Science ®Google Scholar
• Kucerka, N., Perlmutter, J. D., Pan, J., Tristram-Nagle, S., Katsaras, J., & Sachs, J. N. (2008). The effect of cholesterol on short- and long-chain monounsaturated lipid bilayers as determined by molecular dynamics simulations and X-ray scattering. Biophysical Journal, 95(6), 2792–2805. https://doi.org/10.1529/biophysj.107.122465
   PubMed Web of Science ®Google Scholar
• Kulthe, S. S., Inamdar, N. N., Choudhari, Y. M., Shirolikar, S. M., Borde, L. C., & Mourya, V. K. (2011). Mixed micelle formation with hydrophobic and hydrophilic Pluronic block copolymers: Implications for controlled and targeted drug delivery. Colloids and Surfaces B, Biointerfaces, 88(2), 691–696. https://doi.org/10.1016/j.colsurfb.2011.08.002
   PubMed Web of Science ®Google Scholar
• Lee, A. G. (2004). How lipids affect the activities of integral membrane proteins. Biochimica et Biophysica Acta, 1666(1–2), 62–87. https://doi.org/10.1016/j.bbamem.2004.05.012
   PubMed Web of Science ®Google Scholar
• Lipowsky, R. (2013). Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Faraday Discussions, 161, 305–331, discussion 419-359. https://doi.org/10.1039/C2FD20105D
   PubMed Web of Science ®Google Scholar
• Lipowsky, R., Rouhiparkouhi, T., Discher, D. E., & Weikl, T. R. (2013). Domain formation in cholesterol–phospholipid membranes exposed to adhesive surfaces or environments. Soft Matter, 9(35), 8438–8453. https://doi.org/10.1039/c3sm50712b
   Web of Science ®Google Scholar
• Liu, J., & Yang, L. (2006). Effect of cholesterol on DMPC phospholipid membranes and QSAR model construction in membrane-interaction QSAR study through molecular dynamics simulation. Bioorganic & Medicinal Chemistry, 14(7), 2225–2234. https://doi.org/10.1016/j.bmc.2005.11.009
   PubMed Web of Science ®Google Scholar
• Mabrey, S., Mateo, P. L., & Sturtevant, J. M. (1978). High-sensitivity scanning calorimetric study of mixtures of cholesterol with dimyristoyl- and dipalmitoylphosphatidylcholines. Biochemistry, 17(12), 2464–2468. https://doi.org/10.1021/bi00605a034
   PubMed Web of Science ®Google Scholar
• Marcos, X., Padilla-Beltran, C., Bernad-Bernad, M. J., Rosales-Hernandez, M. C., Perez-Casas, S., & Correa-Basurto, J. (2018). Controlled release of N-(2-hydroxyphenyl)-2-propylpentanamide nanoencapsulated in polymeric micelles of P123 and F127 tested as anti-proliferative agents in MDA-MB-231 cells. Journal of Drug Delivery Science and Technology, 48, 403–413. https://doi.org/10.1016/j.jddst.2018.10.005
   Web of Science ®Google Scholar
• McIntosh, T. J., & Simon, S. A. (1986). Hydration force and bilayer deformation: A reevaluation. Biochemistry, 25(14), 4058–4066. https://doi.org/10.1021/bi00362a011
   PubMed Web of Science ®Google Scholar
• Mitra, K., Ubarretxena-Belandia, I., Taguchi, T., Warren, G., & Engelman, D. M. (2004). Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proceedings of the National Academy of Sciences of the United States of America, 101(12), 4083–4088. https://doi.org/10.1073/pnas.0307332101
   PubMed Web of Science ®Google Scholar
• Mojumdar, E. H., & Lyubartsev, A. P. (2010). Molecular dynamics simulations of local anesthetic articaine in a lipid bilayer. Biophysical Chemistry, 153(1), 27–35. https://doi.org/10.1016/j.bpc.2010.10.001
   PubMed Web of Science ®Google Scholar
• Nosé, S. (1984). A molecular dynamics method for simulations in the canonical ensemble. Molecular Physics, 52(2), 255–268. https://doi.org/10.1080/00268978400101201
   Web of Science ®Google Scholar
• Oldfield, E., Meadows, M., Rice, D., & Jacobs, R. (1978). Spectroscopic studies of specifically deuterium labeled membrane systems. Nuclear magnetic resonance investigation of the effects of cholesterol in model systems. Biochemistry, 17(14), 2727–2740. https://doi.org/10.1021/bi00607a006
   PubMed Web of Science ®Google Scholar
• Paiva, J. G., Paradiso, P., Serro, A. P., Fernandes, A., & Saramago, B. (2012). Interaction of local and general anaesthetics with liposomal membrane models: A QCM-D and DSC study. Colloids and Surfaces B, Biointerfaces, 95, 65–74. https://doi.org/10.1016/j.colsurfb.2012.02.027
   PubMed Web of Science ®Google Scholar
• Páll, S., & Hess, B. (2013). A flexible algorithm for calculating pair interactions on SIMD architectures. Computer Physics Communications, 184(12), 2641–2650. https://doi.org/10.1016/j.cpc.2013.06.003
   Web of Science ®Google Scholar
• Pan, J., Mills, T. T., Tristram-Nagle, S., & Nagle, J. F. (2008). Cholesterol perturbs lipid bilayers nonuniversally. Physical Review Letters, 100(19), 198103. https://doi.org/10.1103/PhysRevLett.100.198103
   PubMed Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
   Web of Science ®Google Scholar
• Pasenkiewicz-Gierula, M., Murzyn, K., Rog, T., & Czaplewski, C. (2000a). Molecular dynamics simulation studies of lipid bilayer systems. Acta Biochimica Polonica, 47(3), 601–611. doi:10.18388/abp.2000_3982.
   PubMed Web of Science ®Google Scholar
• Pasenkiewicz-Gierula, M., Rog, T., Kitamura, K., & Kusumi, A. (2000b). Cholesterol effects on the phosphatidylcholine bilayer polar region: A molecular simulation study. Biophysical Journal, 78(3), 1376–1389. https://doi.org/10.1016/S0006-3495(00)76691-4
   PubMed Web of Science ®Google Scholar
• Pencer, J., Nieh, M. P., Harroun, T. A., Krueger, S., Adams, C., & Katsaras, J. (2005). Bilayer thickness and thermal response of dimyristoylphosphatidylcholine unilamellar vesicles containing cholesterol, ergosterol and lanosterol: A small-angle neutron scattering study. Biochimica et Biophysica Acta, 1720(1–2), 84–91. https://doi.org/10.1016/j.bbamem.2005.10.017
   PubMed Web of Science ®Google Scholar
• Porasso, R. D., Bennett, W. F., Oliveira-Costa, S. D., & Lopez Cascales, J. J. (2009). Study of the benzocaine transfer from aqueous solution to the interior of a biological membrane. The Journal of Physical Chemistry B, 113(29), 9988–9994. https://doi.org/10.1021/jp902931s
   PubMed Web of Science ®Google Scholar
• Prestegui-Martel, B., Bermudez-Lugo, J. A., Chavez-Blanco, A., Duenas-Gonzalez, A., Garcia-Sanchez, J. R., Perez-Gonzalez, O. A., Padilla, M., II, Fragoso-Vazquez, M. J., Mendieta-Wejebe, J. E., Correa-Basurto, A. M., Mendez-Luna, D., Trujillo-Ferrara, J., & Correa-Basurto, J. (2016). N-(2-hydroxyphenyl)-2-propylpentanamide, a valproic acid aryl derivative designed in silico with improved anti-proliferative activity in HeLa, rhabdomyosarcoma and breast cancer cells. Journal of Enzyme Inhibition and Medicinal Chemistry, 31(Sup 3), 140–149. https://doi.org/10.1080/14756366.2016.1210138
   PubMedGoogle Scholar
• Rode, A., Sharma, S., & Mishra, D. K. (2018). Carbon nanotubes: Classification, method of preparation and pharmaceutical application. Current Drug Delivery, 15(5), 620–629. https://doi.org/10.2174/1567201815666171221124711
   PubMed Web of Science ®Google Scholar
• Rogers, J. A., & Anderson, K. E. (1998). The potential of liposomes in oral drug delivery. Critical Reviews in Therapeutic Drug Carrier Systems, 15(5), 421–480. doi:10.1615/CritRevTherDrugCarrierSyst.v15.i5.10.
   PubMed Web of Science ®Google Scholar
• Romero-Arrieta, M. R., Uria-Canseco, E., & Perez-Casas, S. (2020). Simultaneous encapsulation of hydrophilic and lipophilic molecules in liposomes od DSPC. Thermochimica Acta, 687(178402), 178462. https://doi.org/10.1016/j.tca.2019.178462
   Google Scholar
• Sander, T., Freyss, J., von Korff, M., & Rufener, C. (2015). DataWarrior: An open-source program for chemistry aware data visualization and analysis. Journal of Chemical Information and Modeling, 55(2), 460–473. https://doi.org/10.1021/ci500588j
   PubMed Web of Science ®Google Scholar
• Saxton, M. J. (1982). Lateral diffusion in an archipelago. Effects of impermeable patches on diffusion in a cell membrane. Biophysical Journal, 39(2), 165–173. https://doi.org/10.1016/S0006-3495(82)84504-9
   PubMed Web of Science ®Google Scholar
• Schmid, P., Adams, S., Rugo, H. S., Schneeweiss, A., Barrios, C. H., Iwata, H., Dieras, V., Hegg, R., Im, S. A., Shaw Wright, G., Henschel, V., Molinero, L., Chui, S. Y., Funke, R., Husain, A., Winer, E. P., Loi, S., Emens, L. A., & Investigators, I. M. T. (2018). Atezolizumab and nab-paclitaxel in advanced triple-negative breast cancer. New England Journal of Medicine, 379(22), 2108–2121. https://doi.org/10.1056/NEJMoa1809615
   PubMed Web of Science ®Google Scholar
• Schonsee, C. D., & Bucheli, T. D. (2020). Experimental determination of octanol–water partition coefficients of selected natural toxins. Journal of Chemical & Engineering Data, 65(4), 1946–1953. https://doi.org/10.1021/acs.jced.9b01129
   Web of Science ®Google Scholar
• Schrödinger. (2021). The PyMOL Molecular Graphics System. 2nd ed.
   Google Scholar
• Schwengber, A., Prado, H. J., Zilli, D. A., Bonelli, P. R., & Cukierman, A. L. (2015). Carbon nanotubes buckypapers for potential transdermal drug delivery. Materials Science & Engineering C, 57, 7–13. https://doi.org/10.1016/j.msec.2015.07.030
   Google Scholar
• Serro, A. P., Galante, R., Kozica, A., Paradiso, P., da Silva, A., Luzyanin, K. V., Fernandes, A. C., & Saramago, B. (2014). Effect of tetracaine on DMPC and DMPC plus cholesterol biomembrane models: Liposomes and monolayers. Colloids and Surfaces B: Biointerfaces, 116, 63–71. https://doi.org/10.1016/j.colsurfb.2013.12.042
   PubMed Web of Science ®Google Scholar
• Sharma, S., Mehra, N. K., Jain, K., & Jain, N. K. (2016). Effect of functionalization on drug delivery potential of carbon nanotubes. Artificial Cells, Nanomedicine, and Biotechnology, 44(8), 1851–1860. https://doi.org/10.3109/21691401.2015.1111227
   PubMed Web of Science ®Google Scholar
• Siddiquee, A. M., Houri, A., Messalea, K. A., Lin, J., Daeneke, T., Abbey, B., Mechler, A., & Kou, S. (2020). Nanoscale probing of cholesterol-rich domains in single bilayer dimyristoyl-phosphocholine membranes using near-field spectroscopic imaging. The Journal of Physical Chemistry Letters, 11(21), 9476–9484. https://doi.org/10.1021/acs.jpclett.0c02192
   PubMed Web of Science ®Google Scholar
• Sk, U. H., & Kojima, C. (2015). Dendrimers for theranostic applications. Biomolecular Concepts, 6(3), 205–217. https://doi.org/10.1515/bmc-2015-0012
   PubMedGoogle Scholar
• Tetko, I. V., Gasteiger, J., Todeschini, R., Mauri, A., Livingstone, D., Ertl, P., Palyulin, V. A., Radchenko, E. V., Zefirov, N. S., Makarenko, A. S., Tanchuk, V. Y., & Prokopenko, V. V. (2005). Virtual computational chemistry laboratory-design and description. Journal of Computer-Aided Molecular Design, 19(6), 453–463. https://doi.org/10.1007/s10822-005-8694-y
   PubMed Web of Science ®Google Scholar
• Uria-Canseco, E., & Perez-Casas, S. (2020). Spherical and tubular dimyristoylphosphatidylcholine liposomes. Journal of Thermal Analysis and Calorimetry, 139(1), 399–409. https://doi.org/10.1007/s10973-019-08416-0
   Web of Science ®Google Scholar
• White, K., Rades, T., Kearns, P., Toth, I., & Hook, S. (2006). Immunogenicity of liposomes containing lipid core peptides and the adjuvant Quil A. Pharmaceutical Research, 23(7), 1473–1481. https://doi.org/10.1007/s11095-006-0272-z
   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. Journal of Chemical Physics, 125(20), 204703. https://doi.org/10.1063/1.2393240
   PubMed Web of Science ®Google Scholar
• Wu, E. L., Cheng, X., Jo, S., Rui, H., Song, K. C., Davila-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/10.1002/jcc.23702
   PubMed Web of Science ®Google Scholar
• Yi, X., Batrakova, E., Banks, W. A., Vinogradov, S., & Kabanov, A. V. (2008). Protein conjugation with amphiphilic block copolymers for enhanced cellular delivery. Bioconjugate Chemistry, 19(5), 1071–1077. https://doi.org/10.1021/bc700443k
   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. International Journal of Quantum Chemistry, 113(15), 1919–1930. https://doi.org/10.1002/qua.24415
   Web of Science ®Google Scholar
• Zhu, Y., & Liao, L. (2015). Applications of nanoparticles for anticancer drug delivery: A review. Journal of Nanoscience and Nanotechnology, 15(7), 4753–4773. https://doi.org/10.1166/jnn.2015.10298
   PubMed Web of Science ®Google Scholar
• Zoete, V., Cuendet, M. A., Grosdidier, A., & Michielin, O. (2011). SwissParam: A fast force field generation tool for small organic molecules. Journal of Computational Chemistry, 32(11), 2359–2368. https://doi.org/10.1002/jcc.21816
   PubMed Web of Science ®Google Scholar
• Zununi Vahed, S., Salehi, R., Davaran, S., & Sharifi, S. (2017). Liposome-based drug co-delivery systems in cancer cells. Materials Science & Engineering C, 71, 1327–1341. https://doi.org/10.1016/j.msec.2016.11.073
   Google Scholar