Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Molecular dynamics simulations of lipid bilayers in aqueous systems reveal how an applied electric field stabilizes the reorganization of the water–membrane interface into water-filled, membrane-spanning, conductive pores with a symmetric, toroidal geometry. The pore formation process and the resulting symmetric structures are consistent with other mathematical approaches such as continuum models formulated to describe the electroporation process. Some experimental data suggest, however, that the shape of lipid electropores in living cell membranes may be asymmetric. We describe here the axially asymmetric pores that form when mechanical constraints are applied to selected phospholipid atoms. Electropore formation proceeds even with severe constraints in place, but pore shape and pore formation time are affected. Since lateral and transverse movement of phospholipids may be restricted in cell membranes by covalent attachments to or non-covalent associations with other components of the membrane or to membrane-proximate intracellular or extracellular biomolecular assemblies, these lipid-constrained molecular models point the way to more realistic representations of cell membranes in electric fields. © 2017, Springer Science+Business Media, LLC, part of Springer Nature.

Registro:

Documento: Artículo
Título:Electropore Formation in Mechanically Constrained Phospholipid Bilayers
Autor:Fernández, M.L.; Risk, M.R.; Vernier, P.T.
Filiación:Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Física, Buenos Aires, Argentina
CONICET - Universidad de Buenos Aires, Instituto de Física del Plasma (INFIP), Buenos Aires, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
Instituto Tecnológico de Buenos Aires (ITBA), Buenos Aires, Argentina
Frank Reidy Research Center for Bioelectrics, Old Dominion University, Norfolk, VA, United States
Palabras clave:Electroporation; Molecular dynamics; Phospholipid bilayer; Position constraints; 2 oleoyl 1 palmitoylphosphatidylcholine; Article; cell membrane; channel gating; covalent bond; electric field; electroporation; extracellular matrix; mechanical constraint; molecular dynamics; molecular model; particle size; phospholipid bilayer; protein assembly; simulation
Año:2018
Volumen:251
Número:2
Página de inicio:237
Página de fin:245
DOI: http://dx.doi.org/10.1007/s00232-017-0002-y
Título revista:Journal of Membrane Biology
Título revista abreviado:J. Membr. Biol.
ISSN:00222631
CODEN:JMBBB
CAS:2 oleoyl 1 palmitoylphosphatidylcholine, 6753-55-5
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00222631_v251_n2_p237_Fernandez

Referencias:

  • Berendsen, H.J.C., Postma, J.P.M., van Gunsteren, W.F., Hermans, J., Interaction models for water in relation to protein hydration (1981) Intermolecular forces, pp. 341-342. , Pullman B, (ed), Reidel, Dordrecht
  • Berendsen, H.J.C., Postma, J.P.M., van Gunsteren, W.F., DiNola, A., Haak, J.R., Molecular dynamics with coupling to an external bath (1984) J Chem Phys, 81, pp. 3684-3690. , COI: 1:CAS:528:DyaL2cXmtlGksbY%3D
  • Berger, O., Edholm, O., Jahnig, F., Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature (1997) Biophys J, 72, pp. 2002-2013. , COI: 1:CAS:528:DyaK2sXivVOjsL4%3D, PID: 9129804
  • Berghöfer, T., Eing, C., Flickinger, B., Hohenberger, P., Wegner, L.H., Frey, W., Nick, P., Nanosecond electric pulses trigger actin responses in plant cells (2009) Biochem Biophys Res Commun, 387, pp. 590-595. , PID: 19619510
  • Breton, M., Mir, L.M., Microsecond and nanosecond electric pulses in cancer treatments (2012) Bioelectromagnetics, 33, pp. 106-123. , PID: 21812011
  • Chopinet, L., Etienne, D., Rols, M.P., AFM sensing cortical actin cytoskeleton destabilization during plasma membrane electropermeabilization (2014) Cytoskeleton, 71, pp. 587-594
  • DeBruin, K.A., Krassowka, W., Modeling electroporation in a single cell. I. Effects of field strength and rest potential (1999) Biophys J, 77, pp. 1213-1224. , COI: 1:CAS:528:DyaK1MXmtVanuro%3D, PID: 10465736
  • Dehez, F., Delemotte, L., Kramar, P., Miklavčič, D., Tarek, M., Evidence of conducting hydrophobic nanopores across membranes in response to an electric field (2014) J Phys Chem C, 118, pp. 6752-6757. , COI: 1:CAS:528:DC%2BC2cXivFyqtr0%3D
  • Essman, U., Perera, L., Berkowitz, M.L., Darden, H.T.L., Pedersen, L.G., A smooth particle mesh Ewald method (1995) J Chem Phys, 103, pp. 8577-8593
  • Fernández, M.L., Marshall, G., Sagués, F., Reigada, R., Structural and kinetic molecular dynamics study of electroporation in cholesterol-containing bilayers (2010) J Phys Chem B, 114, pp. 6855-6865. , PID: 20429602
  • Fernández, M.L., Reigada, R., Effects of dimethyl sulfoxide on lipid membrane electroporation (2014) J Phys Chem B, 118, pp. 9306-9312. , PID: 25035931
  • Fernández, M.L., Risk, M.R., Reigada, R., Vernier, P.T., Size-controlled nanopores in lipid membranes with stabilizing electric fields (2012) Biochem Biophys Res Commun, 423, pp. 325-330. , PID: 22659739
  • Gurtovenko, A.A., Lyulina, A.S., Electroporation of asymmetric phospholipid bilayers (2014) J Phys Chem B, 118, pp. 9909-9918. , COI: 1:CAS:528:DC%2BC2cXhtVymtr%2FP, PID: 24986456
  • Hess, B., Bekker, H., Berendsen, H.J.C., Fraaije, J.G.E.M., LINCS: a linear constraint solver for molecular simulations (1997) J Comput Chem, 18, pp. 1463-1472. , COI: 1:CAS:528:DyaK2sXlvV2nu7g%3D
  • Hess, B., Kutzner, C., van der Spoel, D., Lindahl, E., GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation (2008) J Chem Theory Comput, 4, pp. 435-447. , COI: 1:CAS:528:DC%2BD1cXhsVSqurc%3D, PID: 26620784
  • Ho, M.C., Levine, Z.A., Vernier, P.T., Nanoscale, electric field-driven water bridges in vacuum gaps and lipid bilayers (2013) J Membr Biol, 246, pp. 793-801. , COI: 1:CAS:528:DC%2BC3sXhs1SrtL7L, PID: 23644990
  • Humphrey, W., Dalke, A., Schulten, K., VMD—visual molecular dynamics (1996) J Mol Graph, 14, pp. 33-38. , http://www.ks.uiuc.edu/Research/vmd/
  • Ingólfsson, H.I., Melo, M.N., van Eerden, F.J., Arnarez, C., Lopez, C.A., Wassenaar, T.A., Periole, X., Marrink, S.J., Lipid organization of the plasma membrane (2014) J Am Chem Soc, 136, pp. 14554-14559. , PID: 25229711
  • Joshi, R.P., Hu, Q., Analysis of the cell membrane permeabilization mechanics and pore shape due to ultrashort electrical pulsing (2010) Med Biol Eng Comput, 48, pp. 837-844. , PID: 20635223
  • Kanthou, C., Kranjc, S., Sersa, G., Tozer, G., Zupanic, A., Cemazar, M., The endothelial cytoskeleton as a target of electroporation-based therapies (2006) Mol Cancer Ther, 5, pp. 3145-3152. , COI: 1:CAS:528:DC%2BD28XhtlagsbvO, PID: 17172418
  • Kiessling, V., Crane, J.M., Tamm, L.K., Transbilayer effect of raft-like domains in asymmetric planar bilayers measured by single molecule tracking (2006) Biophys J, 91, pp. 3313-3326. , COI: 1:CAS:528:DC%2BD28XhtFensLbN, PID: 16905614
  • Kotnik, T., Frey, W., Sack, M., Meglič, S.H., Peterka, M., Miklavčič, D., Electroporation-based applications in biotechnology (2015) Trends Biotechnol, 33, pp. 480-488. , COI: 1:CAS:528:DC%2BC2MXhtVeis73N, PID: 26116227
  • Kotulska, M., Dyrka, W., Sadowsi, P., Fluorescent methods in evaluation of nanopore conductivity and their computational validation (2010) Advanced electroporation techniques in biology and medicine, pp. 123-139. , Pakhomov AG, Miklavčič D, Markov MS, (eds), CRC Press, Taylor & Francis Group, Boca Raton
  • Levine, Z.A., Vernier, P.T., Life cycle of an electropore: field-dependent and field-independent steps in pore creation and annihilation (2010) J Membr Biol, 236, pp. 27-36. , COI: 1:CAS:528:DC%2BC3cXps1CrsL8%3D, PID: 20623350
  • Levine, Z.A., Vernier, P.T., Calcium and phosphatidylserine inhibit lipid electropore formation and reduce pore lifetime (2012) J Membr Biol, 245, pp. 599-610. , COI: 1:CAS:528:DC%2BC38XhsV2qsL7L, PID: 22815071
  • Lyubartsev, A.P., Rabinovich, A.L., Force field development for lipid membrane simulations (2016) Biochim Biophys Acta, 1828, pp. 2483-2497
  • MacCallum, J.L., Bennett, W.F.D., Tieleman, D.P., Distribution of amino acids in a lipid bilayer from computer simulations (2008) Biophys J, 94, pp. 3393-3404. , COI: 1:CAS:528:DC%2BD1cXltVOht7g%3D, PID: 18212019
  • Marrink, S.J., de Vries, A.H., Tieleman, D.P., Lipids on the move: Simulations of membrane pores, domains, stalks and curves (2009) Biochim Biophys Acta, 1788, pp. 149-168. , COI: 1:CAS:528:DC%2BD1MXksVWmtQ%3D%3D, PID: 19013128
  • Mihajlovic, M., Lazaridies, T., Antimicrobial peptides in toroidal and cylindrical pores (2010) Biochim Biophys Acta, 1798, pp. 1485-1493. , COI: 1:CAS:528:DC%2BC3cXntlalurs%3D, PID: 20403332
  • Miyamoto, S., Kollman, P.A., SETTLE: an analytical version of the SHAKE and RATTLE algorithms for rigid water models (1992) J Comput Chem, 13, pp. 952-962. , COI: 1:CAS:528:DyaK38Xlslykt7o%3D
  • Ollila, O.H., Pabst, G., Atomistic resolution structure and dynamics of lipid bilayers in simulations and experiments (2016) Biochim Biophys Acta, 1858, pp. 2512-2528. , COI: 1:CAS:528:DC%2BC28XhsFygsLc%3D, PID: 26809025
  • Pakhomov, A.G., Bowman, A.M., Ibey, B.L., Andre, F.M., Pakhomova, O.N., Schoenbach, K.H., Lipid nanopores can form stable, ion channel-like conduction pathway in cell membrane (2009) Biochem Biophys Res Commun, 385, pp. 181-186. , COI: 1:CAS:528:DC%2BD1MXntVGmtrY%3D, PID: 19450553
  • Pakhomov, A.G., Pakhomova, O.N., Nanopores: a distinct transmembrane passageway in electroporated cells (2010) Advanced electroporation techniques in biology and medicine, pp. 177-194. , Pakhomov AG, Miklavčič D, Markov MS, (eds), CRC Press, Taylor & Francis Group, Boca Raton
  • Polak, A., Bonhenry, D., Dehez, F., Kramar, P., Miklavčič, D., Tarek, M., On the electroporation thresholds of lipid bilayers: molecular dynamics simulation investigations (2013) J Membr Biol, 246, pp. 843-850. , COI: 1:CAS:528:DC%2BC3sXhs1SrsLnM, PID: 23780415
  • Polak, A., Tarek, M., Tomšič, M., Valant, J., Poklar Ulrihe, N., Jamnik, A., Kramar, P., Miklavčič, D., Electroporation of archaeal lipid membranes using MD simulations (2014) Bioelectrochemistry, 100, pp. 18-26. , COI: 1:CAS:528:DC%2BC2cXhtV2rsbo%3D, PID: 24461702
  • Python, , http://www.python.org
  • (2016) R: a language and environment for statistical computing, , R Foundation for Statistical Computing, Vienna
  • Raghupathy, R., Anilkumar, A.A., Polley, A., Singh, P.P., Yadav, M., Johnson, C., Suryawanshi, S., Mayor, S., Transbilayer lipid interactions mediate nanoclustering of lipid-anchored proteins (2015) Cell, 161, pp. 581-594. , COI: 1:CAS:528:DC%2BC2MXnt1emtrk%3D, PID: 25910209
  • Reigada, R., Electroporation of heterogeneous lipid membranes (2014) Biochim Biophys Acta, 1838, pp. 814-821. , COI: 1:CAS:528:DC%2BC2cXhsFClsrs%3D, PID: 24144543
  • Risselada, H.J., Mark, A.E., Marrink, S.J., Application of mean field boundary potentials in simulations of lipid vesicles (2008) J Phys Chem B, 112, pp. 7438-7447. , PID: 18512884
  • Rols, M.P., Teissié, J., Experimental evidence for the involvement of the cytoskeleton in mammalian cell electropermeabilization (1992) Biochim Biophys Acta, 1111, pp. 45-50. , COI: 1:CAS:528:DyaK3sXjsFehtA%3D%3D, PID: 1390863
  • Rosazza, C., Escoffre, J.M., Zumbusch, A., Rols, M.P., The actin cytoskeleton has an active role in the electrotransfer of plasmid DNA in mammalian cells (2011) Mol Ther, 19, pp. 913-921. , COI: 1:CAS:528:DC%2BC3MXitleqsLo%3D, PID: 21343915
  • Sapay, N., Bennett, W.F.D., Tieleman, D.P., Thermodynamics of flip-flop and desorption for a systematic series of phosphatidylcholine lipids (2009) Soft Matter, 5, pp. 3295-3302. , COI: 1:CAS:528:DC%2BD1MXhtVSlsLjF
  • Sengupta, D., Leontiadou, H., Mark, A.E., Marrink, S.J., Toroidal pores formed by antimicrobial peptides show significant disorder (2008) Biochim Biophys Acta Biomembr, 1778, pp. 2308-2317. , COI: 1:CAS:528:DC%2BD1cXhtFCktbrO
  • Silve, A., Brunet, A.G., Al-Sakere, B., Ivorra, A., Mir, L.M., Comparison of the effects of the repetition rate between microsecond and nanosecond pulses: electropermeabilization-induced electro-desensitization? (2014) Bichem Biophys Acta, 1840, pp. 2139-2151. , COI: 1:CAS:528:DC%2BC2cXhtVSlsLnL
  • Siwi, Z., Gu, Y., Spohr, H.A., Baur, D., Wolf-Reber, A., Spohr, R., Apel, P., Korchev, Y.E., Rectification and voltage gating of ion currents in a nanofabricated pore (2002) Europhys Lett, 60, pp. 349-355
  • Smith, K.C., Weaver, J.C., Transmembrane molecular transport during versus after extremely large, nanosecond electric pulses (2011) Biochem Biophys Res Commun, 412, pp. 8-12. , COI: 1:CAS:528:DC%2BC3MXhtVKlu7%2FM, PID: 21756883
  • Son, R.S., Smith, K.C., Gowrishankar, T.R., Vernier, P.T., Weaver, J.C., Basic features of a cell electroporation model: Illustrative behavior for two very different pulses (2014) J Membr Biol, 247, pp. 1209-1228. , COI: 1:CAS:528:DC%2BC2cXhtF2qu7fP, PID: 25048527
  • Stacey, M., Fox, P., Buescher, S., Kolb, J., Nanosecond pulsed electric field induced cytoskeleton, nuclear membrane and telomere damage adversely impact cell survival (2011) Bioelectrochemistry, 82, pp. 131-134. , COI: 1:CAS:528:DC%2BC3MXht1ejtbbL, PID: 21719360
  • Stoddart, D., Ayub, M., Höfler, L., Raychaudhuri, P., Klingelhoefer, J.W., Maglia, G., Heron, A., Bayley, H., Functional truncated membrane pores (2014) Proc Natl Acad Sci USA, 111, pp. 2425-2430. , COI: 1:CAS:528:DC%2BC2cXivFamsLk%3D, PID: 24469792
  • Sugar, I.P., Neumann, E., Stochastic model for electric field-induced membrane pores electroporation (1984) Biophys Chem, 19, pp. 211-225. , COI: 1:CAS:528:DyaL2cXksFSntr0%3D, PID: 6722274
  • Sun, S., Yin, G., Lee, Y.K., Wong, J.T., Zhang, T.Y., Effects of deformability and thermal motion of lipid membrane on electroporation: by molecular dynamics simulations (2011) Biochem Biophys Res Commun, 404, pp. 684-688. , COI: 1:CAS:528:DC%2BC3MXntVWltA%3D%3D, PID: 21156156
  • Tarek, M., Membrane electroporation: a molecular dynamics study (2005) Biophys J, 88, pp. 4045-4053. , COI: 1:CAS:528:DC%2BD2MXksl2jtrg%3D, PID: 15764667
  • Teissié, J., Rols, M.P., Manipulation of cell cytoskeleton affects the lifetime of cell membrane electropermeabilization (1994) Ann N Y Acad Sci, 720, pp. 98-110. , PID: 8010657
  • Tieleman, D.P., The molecular basis of electroporation (2004) BMC Biochem, 5, p. 10. , PID: 15260890
  • Thompson, G.L., Roth, C., Tolstykh, G., Kuipers, M., Ibey, B.L., Disruption of the actin cortex contributes to susceptibility of mammalian cells to nanosecond pulsed electric fields (2014) Bioelectromagnetics, 35, pp. 262-272. , COI: 1:CAS:528:DC%2BC2cXltFegtb4%3D, PID: 24619788
  • Tsong, T., Electroporation of cell membranes (1991) Biophys J, 60, pp. 297-306. , COI: 1:CAS:528:DyaK3MXltlSrt7s%3D, PID: 1912274
  • Weaver, J.C., Chizmadzhev, Y.A., Theory of electroporation: a review (1996) Bioelectrochem Bioenerg, 41, pp. 135-160. , COI: 1:CAS:528:DyaK28XntlKrtro%3D
  • Weaver, J.C., Electroporation of cells and tissues (2000) IEEE Trans Plasma Sci, 28, pp. 24-33. , COI: 1:CAS:528:DC%2BD3cXktVOms74%3D
  • Yarmush, M.L., Golberg, A., Serša, G., Kotnik, T., Miklavčič, D., Electroporation-based technologies for medicine: principles, applications, and challenges (2014) Annu Rev Biomed Eng, 16, pp. 295-320. , COI: 1:CAS:528:DC%2BC2cXhsVKgt7%2FI, PID: 24905876
  • Ziegler, M.J., Vernier, P.T., Interface water dynamics and porating electric field for phospholipid bilayers (2008) J Phys Chem B, 112, pp. 13588-13596. , COI: 1:CAS:528:DC%2BD1cXht1SksLnP, PID: 18837540

Citas:

---------- APA ----------
Fernández, M.L., Risk, M.R. & Vernier, P.T. (2018) . Electropore Formation in Mechanically Constrained Phospholipid Bilayers. Journal of Membrane Biology, 251(2), 237-245.
http://dx.doi.org/10.1007/s00232-017-0002-y
---------- CHICAGO ----------
Fernández, M.L., Risk, M.R., Vernier, P.T. "Electropore Formation in Mechanically Constrained Phospholipid Bilayers" . Journal of Membrane Biology 251, no. 2 (2018) : 237-245.
http://dx.doi.org/10.1007/s00232-017-0002-y
---------- MLA ----------
Fernández, M.L., Risk, M.R., Vernier, P.T. "Electropore Formation in Mechanically Constrained Phospholipid Bilayers" . Journal of Membrane Biology, vol. 251, no. 2, 2018, pp. 237-245.
http://dx.doi.org/10.1007/s00232-017-0002-y
---------- VANCOUVER ----------
Fernández, M.L., Risk, M.R., Vernier, P.T. Electropore Formation in Mechanically Constrained Phospholipid Bilayers. J. Membr. Biol. 2018;251(2):237-245.
http://dx.doi.org/10.1007/s00232-017-0002-y