Visualization of membrane loss during the shrinkage of giant vesicles under electropulsation

Biophysical Journal

Volumn 96, Issue 10, 2009, Pages 4109-4121

  Portet, Thomas ^a,b   Camps I Febrer, Franc ^a   Escoffre, Jean Michel ^a   Favard, Cyril ^c   Rols, Marie Pierre ^a   Dean, David S ^b  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1,2 DIOLEOYL SN GLYCERO 3 PHOSPHOCHOLINE; LIPID; PHOSPHATIDYLCHOLINE; PHOSPHORYLCHOLINE; UNCLASSIFIED DRUG; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; 2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; LIPOSOME;

ARTICLE; CELL PERMEABILIZATION; CELL VACUOLE; CHANNEL GATING; ELECTRIC ACTIVITY; ELECTRIC FIELD; ELECTROPULSATION; EXPERIMENT; MEMBRANE; QUALITATIVE ANALYSIS; CHEMISTRY; ELECTRICITY; ELECTRODE; METABOLISM; MOVEMENT (PHYSIOLOGY); PERMEABILITY; PH; POROSITY;

ELECTRICITY; ELECTRODES; HYDROGEN-ION CONCENTRATION; MOVEMENT; PERMEABILITY; PHOSPHATIDYLCHOLINES; POROSITY; UNILAMELLAR LIPOSOMES;

EID: 68049133059     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.02.063     Document Type: Article

References (59)

1. Neumann, E., A. E. Sowers, and C. A. Jordan. 1989. Electroporation and Electrofusion in Cell Biology. Plenum Press, New York.
2. Weaver, J. C. 1995. Electroporation theory. Concepts and mechanisms. Methods Mol. Biol. 55:3-28.
3. Weaver, J. C., and Y. A. Chizmadzhev. 1996. Theory of electroporation: a review. Bioelectrochem. Bioenerg. 41:135-160.
4. Teissié, J., M. Golzio, and M.-P. Rols. 2005. Mechanisms of cell membrane electropermeabilization: a minireview of our present (lack of?) knowledge. Biochim. Biophys. Acta. 1724:270-280.
5. Escoffre, J.-M., D. S. Dean, M. Hubert, M.-P. Rols, and C. Favard. 2007. Membrane perturbation by an external electric field: a mechanism to permit molecular uptake. Eur. Biophys. J. 36:973-983.
6. Favard, C., D. S. Dean, and M.-P. Rols. 2007. Electrotransfer as a nonviral method of gene delivery. Curr. Gene Ther. 7:67-77.
7. Dimova, R., K. A. Riske, S. Aranda, N. Bezlyepkina, R. L. Knorr, et al. 2007. Giant vesicles in electric fields. Soft Matter. 3:817-827.
8. Neumann, E., and K. Rosenheck. 1972. Permeability changes induced by electric impulses in vesicular membranes. J. Membr. Biol. 10:279-290.
9. Rols, M.-P. 2006. Electropermeabilization, a physical method for the delivery of therapeutic molecules into cells. Biochim. Biophys. Acta. 1758:423-428.
10. Robello, M., and A. Gliozzi. 1989. Conductance transition induced by an electric field in lipid bilayers. Biochim. Biophys. Acta. 982:173-176.
11. Rols, M.-P., and J. Teissié. 1998. Electropermeabilization of mammalian cells to macromolecules: control by pulse duration. Biophys. J. 75:1415-1423.
12. Golzio, M., J. Teissié, and M.-P. Rols. 2002. Direct visualization at the single-cell level of electrically mediated gene delivery. Proc. Natl. Acad. Sci. USA. 99:1292-1297.
13. Antov, Y., A. Barbul, H. Mantsur, and R. Korenstein. 2005. Exposure of cells to pulsed low electric fields enhances adsorption and uptake of macromolecules. Biophys. J. 88:2206-2223.
14. Belehradek, M., C. Domenge, B. Luboinski, S. Orlowski, J. Belehradek, Jr, et al. 1993. Electrochemotherapy, a new antitumor treatment. First clinical phase I-II trial. Cancer. 72:3694-3700.
15. Gehl, J., T. Sorensen, K. Nielsen, P. Raskmark, S. Nielsen, et al. 1999. In vivo electroporation of skeletal muscle: threshold, efficacy and relation to electric field distribution. Biochim. Biophys. Acta. 1428:233-240.
16. Sersa, G., D. Miklavcic, M. Cemazar, Z. Rudolf, G. Pucihar, et al. 2008. Electrochemotherapy in treatment of tumors. Eur. J. Surg. Oncol. 34:232-240.
17. Gilbert, R., M. Jaroszeski, and R. Heller. 1997. Novel electrode designs for electrochemotherapy. Biochim. Biophys. Acta. 1334:9-14.
18. Gothelf, A., L. Mir, and J. Gehl. 2003. Electrochemotherapy: results of cancer treatment using enhanced delivery of bleomycin by electroporation. Cancer Treat. Rev. 29:371-387.
19. Winterhalter, M., and W. Helfrich. 1988. Deformation of spherical vesicles by electric fields. J. Colloid Interface Sci. 122:583-586.
20. Kummrow, M., and W. Helfrich. 1991. Deformation of giant lipid vesicles by electric fields. Phys. Rev. A. 44:8356-8360.
21. Riske, K. A., and R. Dimova. 2005. Electro-deformation and poration of giant vesicles viewed with high temporal resolution. Biophys. J. 88:1143-1155.
22. Riske, K. A., and R. Dimova. 2006. Electric pulses induce cylindrical deformations on giant vesicles in salt solutions. Biophys. J. 91:1778-1786.
23. Crowley, J. 1973. Electrical breakdown of bimolecular lipid membranes as an electromechanical instability. Biophys. J. 13:711-724.
24. Abidor, I., V. Arakelyan, L. Chernomordik, Y. A. Chizmadzhev, V. Pastushenko, et al. 1979. Electric breakdown of bilayer membranes I: The main experimental facts and their qualitative description. Bioelectrochem. Bioenerg. 6:37-52.
25. Pastushenko, V., Y. Chizmadzhev, and V. Arekelyan. 1979. Electric breakdown of bilayer membranes II. Calculation of the membrane lifetime in the steady-state diffusion approximation. Bioelectrochem. Bioenerg. 6:53-62.
26. Needham, D., and R. M. Hochmuth. 1989. Electro-mechanical permeabilization of lipid vesicles - role of membrane tension and compressibility. Biophys. J. 55:1001-1009.
27. Isambert, H. 1998. Understanding the electroporation of cells and artificial bilayer membranes. Phys. Rev. Lett. 80:3404-3407.
28. Sens, P., and H. Isambert. 2002. Undulation instability of lipid membranes under an electric field. Phys. Rev. Lett. 88:128102-128105.
29. Powell, K., and J. Weaver. 1986. Transient aqueous pores in bilayer membranes: a statistical theory. Bioelectrochem. Bioenerg. 15:211-227.
30. Glaser, R., S. Leikin, L. Chernomordik, V. Pastushenko, and A. Sokirko. 1988. Reversible electrical breakdown of lipid bilayers and formation and evolution of pores. Biochim. Biophys. Acta. 940:272-287.
31. Barnett, A., and J. C. Weaver. 1991. Electroporation: a unified, quantitative theory of reversible electrical breakdown and mechanical rupture in artificial planar bilayer membranes. Bioelectrochem. Bioenerg. 25:163-182.
32. Neu, J., and W. Krassowska. 2003. Modeling postshock evolution of large electropores. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 67:021915-021926.
33. Neu, J., K. Smith, and W. Krassowska. 2003. Electrical energy required to form large conducting pores. Bioelectrochem. Bioenerg. 60:107-114.
34. Derjaguin, B., and Y. Gutop. 1961. Theory of the breakdown (rupture) of free films. Kolloidn Zh. 24:370-374.
35. Tieleman, D. P. 2004. The molecular basis of electroporation. BMC Biochem. 5:10.
36. Leontiadou,H.,A.Mark, and S.Marrink. 2004.Molecular dynamics simulations of hydrophilic pores in lipid bilayers. Biophys. J. 86:2156-2164.
37. Tarek, M. 2005. Membrane electroporation: a molecular dynamics simulation. Biophys. J. 88:4015-4053.
38. Hu, Q., R. P. Joshi, and K. H. Schoenbach. 2005. Simulations of nanopore formation and phosphatidylserine externalization in lipid membrane subjected to high intensity, ultra-short electric pulse. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72:031902.
39. Hu, Q., S. Viswanadham, R. P. Joshi, K. H. Schoenbach, S. J. Beebe, et al. 2005. Simulations of transient membrane behavior in cells subjected to a high intensity, ultra-short electric pulse. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71:031914.
40. Tieleman, D. P. 2006. Computer simulations of transport through membranes: passive diffusion, pores, channels and transporters. Clin. Exp. Pharm. Phys. 33:893-903.
41. Wohlert, J., W. den Otter, O. Edholm, and W. J. Briels. 2006. Free energy of a trans-membrane pore calculated from atomist molecular dynamics simulations. J. Chem. Phys. 124:154905-154914.
42. Tekle, E., R. D. Astumian, W. A. Friauf, and P. B. Chock. 2001. Asymmetric pore distribution and loss of membrane lipid in electroporated DOPC vesicles. Biophys. J. 81:960-968.
43. Angelova, M. I., and D. S. Dimitrov. 1986. Liposome electroformation. Faraday Discuss. Chem. Soc. 81:303-311.
44. Rodriguez, N., F. Pincet, and S. Cribier. 2005. Giant vesicles formed by gentle hydration and electroformation: a comparison by fluorescence microscopy. Colloids Surf. B. 42:125-130.
45. Teissié, J., and M.-P. Rols. 1993. An experimental evaluation of the critical potential difference inducing cell membrane electropermeabilization. Biophys. J. 65:409-413.
46. Gabriel, B., and J. Teissié. 1997. Direct observation in the millisecond time range of fluorescent molecule asymmetrical interaction with the electropermeabilized cell membrane. Biophys. J. 73:2630-2637.
47. Tsong, T. Y. 1991. Electroporation of cell membranes. Biophys. J. 60:297-306.
48. Pavlin, M., N. Pavselj, and D. Miklavcic. 2002. Dependence of induced transmembrane potential on cell density, arrangement, and cell position inside a cell system. IEEE Trans. Biomed. Eng. 49:605-612.
49. Carvalho, K., L. Ramos, C. Roy, and C. Picart. 2008. Giant unilamellar vesicles containing phosphatidylinositol(4,5)biphosphate: characterization and functionality. Biophys. J. In press.
50. Khalifat, N., N. Puff, S. Bonneau, J.-B. Fournier, and M. Angelova. 2008. Membrane deformation under local pH gradient: mimicking mitochondrial crystal dynamics. Biophys. J. In press.
51. Marszalek, P., and T. Tsong. 1995. Cell fission and formation of mini cell bodies by high frequency alternating electric field. Biophys. J. 68:1218-1221.
52. Rodriguez, N., S. Cribier, and F. Pincet. 2006. Transition from long- to short-lived transient pores in giant vesicles in an aqueous medium. Phys. Rev. E. 74, 061902.1-10.
53. Kinosita, K., and T. Tsong. 1977. Formation and resealing of pores of controlled sizes in human erythrocyte membrane. Nature. 268:438-441.
54. Abidor, I., A. Barbul, D. Zhelev, P. Doinov, I. Bandrina, et al. 1993. Electrical properties of cell pellets and cell electrofusion in a centrifuge. Biochim. Biophys. Acta. 1152:207-218.
55. Abidor, I., L. Li, and S. Hui. 1994. Studies of cell pellets: II. Osmotic properties, electroporation, and related phenomena: membrane interactions. Biophys. J. 67:427-435.
56. Golzio, M., M. Mora, C. Raynaud, C. Delteil, J. Teissié, et al. 1998. Control by osmotic pressure of voltage-induced permeabilization and gene transfer in mammalian cells. Biophys. J. 74:3015-3022.
57. Pasenkiewicz-Gierula, M., Y. Takaoka, H. Miyagawa, K. Kitamura, and A. Kusumi. 1999. Charge pairing of headgroups in phosphatidylcholine membranes: a molecular dynamics simulation study. Biophys. J. 76:1228-1240.
58. Israelachvili, J. 2000. Intermolecular and Surface Forces, 2nd Ed. Academic Press, San Diego, CA.
59. Sugár, I. P. 1979. A theory of the electric field-induced phase transition of phospholipid bilayers. Biochim. Biophys. Acta. 556:72-85.