A molecular dynamic study of cholesterol rich lipid membranes: Comparison of electroporation protocols

Bioelectrochemistry

Volumn 100, Issue , 2014, Pages 11-17

  Casciola, M ^a,b,c   Bonhenry, D ^c   Liberti, M ^a   Apollonio, F ^a,b   Tarek, M ^c,d  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c UNIVERSITÉ DE LORRAINE   (France)

^d CNRS   (France)

Author keywords

Electric fields; Lipid bilayers; Molecular modeling; Nanopore morphologies; Permeabilization

Indexed keywords

LIPID BILAYERS; MOLECULAR MODELING;

ELECTROPORATION; LIPID MEMBRANES; PERMEABILIZATION;

ELECTRIC FIELDS;

AMPHOLYTE; CHOLESTEROL; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; LIPID BILAYER; PHOSPHATIDYLCHOLINE;

ARTICLE; BILAYER MEMBRANE; CELL MEMBRANE; ELECTROPORATION; LIPID BILAYER; LIPID MEMBRANE; MOLECULAR DYNAMICS; MORPHOLOGY; SIMULATION; CHEMISTRY; COMPARATIVE STUDY; CONFORMATION; METABOLISM; PROCEDURES; TIME;

CELL MEMBRANE; CHOLESTEROL; ELECTROPORATION; LIPID BILAYERS; MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION; PHOSPHATIDYLCHOLINES; TIME FACTORS;

EID: 84908070863     PISSN: 15675394     EISSN: 1878562X     Source Type: Journal    
DOI: 10.1016/j.bioelechem.2014.03.009     Document Type: Article

References (75)

1. Neumann E. The relaxation hysteresis of membrane electroporation. Plenum Publ. Corp. 1989, 61-82. E. Neumann, A.E. Sowers, C.A. Jordan (Eds.).
2. Nickoloff J.A. Animal Cell Electroporation and Electrofusion Protocols 1995, Humana Press, Totowa, NJ.
3. Li S. Electroporation Protocols: Preclinical and Clinical Gene Medecine 2008, Humana press, Totowa, NJ.
4. Neumann E., Rosenheck K. Permeability changes induced by electric impulses in vesicular membranes. J. Membr. Biol. 1972, 10:279-290.
5. Zimmerman U., Pilwat G., Beckers F., et al. Effects of external electrical fields on cell membranes. Bioelectrochem. Bioenerg. 1976, 3:58-83.
6. Glaser R.W., Leiken S.L., Chernomordik L.V., et al. Reversible electrical breakdown of lipid bilayers: formation and evolution of pores. Biochim. Biophys. Acta 1988, 940:275-287.
7. Needham D., Hochmuth R.M. Electro-mechanical permeabilization of lipid vesicles. Biophys. J. 1989, 55:1001-1009.
8. Zimmerman U. The Effect of High Intensity Electric Field Pulses on Eukaryotic Cell Membranes: Fundamentals and Applications 1996, CRC Press, Boca Raton, Florida.
9. Teissié J., Eynard N., Gabriel B., et al. Electropermeabilization of cell membranes. Adv. Drug Deliv. Rev. 1999, 35:3-19.
10. Tsong T.Y. Electric modification of membrane permeability for drug loading into living cells. Methods Enzymol. 1987, 149:248-259.
11. Weaver J.C. Electroporation Theory, Methods in Molecular Biology 1995, 3-29. Humana Press, Clifton, New Jersey.
12. Tsong T.Y. Electroporation of cell membranes. Biophys. J. 1991, 60:297-306.
13. Neumann E., Schaefer-Ridder M., Wang Y., et al. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J. 1982, 1:841-845.
14. Lee R.C., River L.P., Pan F.S., et al. Surfactant-induced sealing of electropermeabilized skeletal muscle membrane in vivo. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:4524-4528.
15. Nishi T., Yoshizato K., Yamashiro S., et al. High-efficiency in vivo gene transfer using intraarterial plasmid DNA injection following in vivo electroporation. Cancer Res. 1996, 56:1050-1055.
16. Lundqvist J.A., Sahlin F., Aberg M.A., et al. Altering the biochemical state of individual cultured cells and organelles with ultramicroelectrodes. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:10356-10360.
17. Harrison R.L., Byrne B.J., Tung L. Electroporation-mediated gene transfer in cardiac tissue. FEBS Lett. 1998, 435:1-5.
18. Golzio M., Teissie J., Rols M.-P. Direct visualization at the single-cell level of electrically mediated gene delivery. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1292-1297.
19. Tsong T.Y. Voltage modulation of membrane permeability and energy utilization in cells. Biosci. Rep. 1983, 3:487-505.
20. Prausnitz M.R., Bose V.G., Langer R., et al. Electroporation of mammalian skin: a mechanism to enhance transdermal drug delivery. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:10504-10508.
21. Breton M., Delemotte L., Silve A., et al. Transport of siRNA through lipid membranes driven by nanosecond electric pulses: an experimental and computational study. J. Am. Chem. Soc. 2012, 134:13938-13941.
22. Testori A., Soteldo J., Di Pietro A., et al. The treatment of cutaneous and subcutaneous lesions with electrochemotherapy with bleomycin. Eur. Dermatol. 2008, 3:1-3.
23. Cemazar M., Tamzali Y., Sersa G., et al. Electrochemotherapy in veterinary oncology. J. Vet. Int. Med. 2008, 22:826-831.
24. Villemejane J., Mir L.M. Physical methods of nucleic acid transfer: general concepts and applications. Brit. J. Pharma. 2009, 157:207-219.
25. Bodles-Brakhop A.M., Heller R., Draghia-Akli R. Electroporation for the delivery of DNA-based vaccines and immunotherapeutics: current clinical developments. Mol. Ther. 2009, 17:585-592.
26. Campana L.G., Mocellin S., Basso M., et al. Bleomycin-based electrochemotherapy: clinical outcome from a single institution's experience with 52 patients. Ann. Surg. Oncol. 2009, 16:191-199.
27. Pakhomov A., Miklavcic D., Markov M. Advanced Electroporation Techniques in Biology and Medicine 2010, Taylor and Francis/CRC Press.
28. Zorec B., Préat V., Miklavčič D., Pavšelj N. Active enhancement methods for intra- and transdermal drug delivery: a review. Zdrav Vestn. 2013, 82:339-356.
29. Chabot S., Rosazza C., Golzio M., Zumbusch A., Teissie J., Rols M.P. Nucleic acids electro-transfer: from bench to bedside. Curr. Drug Metab. 2013, 14:300-308.
30. Chen C., Smye S.W., Robinson M.P., et al. Membrane electroporation theories: a review. Med. Biol. Eng. Comput. 2006, 44:5-14.
31. Beebe S.J., Schoenbach K.H. Nanosecond pulsed electric fields: a new stimulus to activate intracellular signaling. J. Biomed. Biotechnol. 2005, 4:297-300.
32. Benz R., Beckers F., Zimmerman U. Reversible electrical breakdown of lipid bilayer membranes - charge-pulse relaxation study. J. Membr. Biol. 1979, 48:181-204.
33. Chernomordik L.V., Sukharev S.I., Popov S.V., et al. The electrical breakdown of cell and lipid membranes: the similarity of phenomenologies. Biochim. Biophys. Acta 1987, 902:360-373.
34. Tieleman D.P. The molecular basis of electroporation. BMC Biochem. 2004, 5:10.
35. Hu Q., Viswanadham S., Joshi R.P., et al. Simulations of transient membrane behavior in cells subjected to a high-intensity ultrashort electric pulse. Phys. Rev. E. 2005, 71:031914.
36. Gurtovenko A.A., Vattulainen I. Pore formation coupled to ion transport through lipid membranes as induced by transmembrane ionic charge imbalance: atomistic molecular dynamics study. J. Am. Chem. Soc. 2005, 127:17570-17571.
37. Tarek M. Membrane electroporation: a molecular dynamics simulation. Biophys. J. 2005, 88:4045-4053.
38. Vernier P.T., Ziegler M.J., Sun Y., et al. Nanopore formation and phosphatidylserine externalization in a phospholipid bilayer at high transmembrane potential. J. Am. Chem. Soc. 2006, 128:6288-6289.
39. Bockmann R.A., de Groot B.L., Kakorin S., et al. Kinetics, statistics, and energetics of lipid membrane electroporation studied by molecular dynamics simulations. Biophys. J. 2008, 95:1837-1850.
40. Ziegler M.J., Vernier P.T. Interface water dynamics and porating electric fields for phospholipid bilayers. J. Phys. Chem. B 2008, 112:13588-13596.
41. Gurtovenko A.A., Jamshed Anwar J., Vattulainen I. Defect-mediated trafficking across cell membranes: insights from in silico modeling. Chem. Rev. 2010, 110:6077-6103.
42. Levine Z.A., Vernier P.T. Life cycle of an electropore: field dependent and field-independent steps in pore creation and annihilation. J. Membr. Biol. 2010, 236:27-36.
43. Delemotte L., Tarek M. Molecular dynamics simulations of lipid membrane electroporation. J. Membr. Biol. 2012, 245:531-543.
44. Ho M.-C., Casciola M., Levine Z.A., Vernier P.T. Molecular dynamics simulations of ion conductance in field-stabilized nanoscale lipid electropores. J. Phys. Chem. B 2013, 117:11633-11640.
45. Vernier P.T., Ziegler M.J., Sun Y., Gundersen M.A., Tieleman D.P. Nanopore-facilitated, voltage-driven phosphatidylserine translocation in lipid bilayers - in cells and in silico. Phys. Biol. 2006, 3:233-247.
46. Kramar P., Delemotte L., Lebar A.M., et al. Molecular-level characterization of lipid membrane electroporation using linearly rising current. J. Membr. Biol. 2012, 245:651-659.
47. Polak A., Tarek M., Tomšič M., Valant J., Ulrih N.P., Jamnik A., Kramar P., Miklavčič D. Electroporation of archaeal lipid membranes using MD simulations. Bioelectrochemistry 2014, 100:18-26.
48. Benvegnu T., Brard M., Plusquellec D. Archaeabacteria bipolar lipid analogues: structure, synthesis and lyotropic properties. Curr. Opin. Colloid Interface Sci. 2004, 8:469-479.
49. Ulrih N.P., Gmajner D., Raspor P. Structural and physicochemical properties of polar lipids from thermophilic archaea. Appl. Microbiol. Biotechnol. 2009, 84:249-260.
50. Ulrih N.P., Adamlje U., Nemec M., Sentjurc M. Temperature- and pH-induced structural changes in the membrane of the hyperthermophilic archaeon Aeropyrum pernix K1. J. Membr. Biol. 2007, 219:1-8.
51. Bloom M., Evans E., Mouritsen O.G. Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective. Q. Rev. Biophys. 1991, 24:293-397.
52. Brown D.A., London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 2000, 275:17221-17224.
53. Berkowitz M.L. Detailed molecular dynamics simulations of model biological membranes containing cholesterol. Biochim. Biophys. Acta 2009, 1788:86-96.
54. Tu K., Klein M.L., Tobias D.J. Constant-pressure molecular dynamics investigation of cholesterol effects in a dipalmitoyl phosphatidyl choline bilayer. Biophys. J. 1998, 75(5):2147-2156.
55. Martinez-Seara H., Rog T., Karttunen M., Vattulainen I., Reigada R. Cholesterol induces specific spatial and orientational order in cholesterol/phospholipid membranes. PLoS ONE 2010, 5:1-11.
56. Kucerka N., Perlmutter J.D., Pan J., Tristram-Nagle S., Katsaras J., Sachs J.N. The effect of cholesterol on short- and long-chain mono-unsaturated lipid bilayers as determined by molecular dynamics simulations and X-ray scattering. Biophys. J. 2008, 95:2792-2805.
57. Kakorin S., Brinkmann U., Neumann E. Cholesterol reduces membrane electro-poration and electric deformation of small bilayer vesicles. Biophys. Chem. 2005, 117:155-171.
58. Koronkiewicz S., Kalinowski S. Influence of cholesterol on electroporation of bilayer lipid membranes: chronopotentiometric studies. Biochim. Biophys. Acta 2004, 1661:196-203.
59. Naumowicz M., Figaszewski Z.A. Pore formation in lipid bilayer membranes made of phosphatidylcholine and cholesterol followed by means of constant current. Cell Biochem. Biophys. 2013, 66:109-119.
60. van Uitert I., Le Gac S., van den Berg A. The influence of different membrane components on the electrical stability of bilayer lipid membranes. Biochim. Biophys. Acta 2010, 1798:21-31.
61. Fernández M.L., Marshall G., Sagués F., et al. Structural and kinetic molecular dynamics study of electroporation in cholesterol-containing bilayers. J. Phys. Chem. B 2010, 114:6855-6865.
62. Hung W.C., Lee M.T., Chen F.T., et al. The condensing effect of cholesterol in lipid bilayers. Biophys. J. 2007, 92:3960-3967.
63. de Meyer F., Smit B. Effect of cholesterol on the structure of a phospholipid bilayer. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3654-3658.
64. Marrink S.J., de Vries A.H., Harroun T.A., Katsaras J., Wassall S.R. Cholesterol shows preference for the interior of polyunsaturated lipid membranes. J. Am. Chem. Soc. 2008, 130:10-11.
65. Bennett W.F., MacCallum J.L., Tieleman D.P. Thermodynamic analysis of the effect of cholesterol on dipalmitoylphosphatidylcholine lipid membranes. J. Am. Chem. Soc. 2009, 131:1972-1978.
66. Delemotte L., Dehez F., Treptow W., et al. Modeling membranes under a transmembrane potential. J. Phys. Chem. B 2008, 112:5547-5550.
67. Klauda J.B., Venable R.M., Freites J.A., et al. Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types. J. Phys. Chem. B 2010, 114:7830-7843.
68. Jorgensen W.L., Chandrasekhar J., Madura J.D., et al. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 1983, 79:926-935.
69. Hess B., Bekker H., Berendsen H.J.C., et al. LINCS: a linear constraint solver for molecular simulations. J. Comp. Chem. 1997, 18:1463-1472.
70. Essmann U., Perera L., Berkowitz M.L., et al. A smooth particle mesh Ewald method. J. Chem. Phys. 1995, 103:8577-8593.
71. Hess B., Kutzner C., van der Spoel D., et al. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Comp. Theor. Chem. 2008, 4:435-447.
72. Zhong Q., Moore P.B., Newns D.M., et al. Molecular dynamics study of the LS3 voltage-gated ion channel. FEBS Lett. 1998, 427:267-270.
73. Tieleman D.P., Berendsen J.H.C., Sansom M.S.P. Voltage-dependent insertion of alamethicin at phospholipid/water and octane water interfaces. Biophys. J. 2001, 80:331-346.
74. Henderson D., Crozier P., et al. Permeation of ions through a model biological channel: effect of periodic boundary condition and cell size. Mol. Phys. 2002, 100:3011-3019.
75. Hofsäß C., Lindahl E., Edholm O. Molecular dynamics simulations of phospholipid bilayers with cholesterol. Biophys. J. 2003, 84:2192-2206.