Electroporation of Biological Membranes from Multicellular to Nano Scales

IEEE Transactions on Dielectrics and Electrical Insulation

Volumn 10, Issue 5, 2003, Pages 754-768

  Weaver, James C ^a  

^a HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

Bilayer membranes; Biological membranes; Cells; Electroporation; Ionic transport; Lipid membranes; Mitochondria; Molecular transport; Multicellular scale; Nano scale membrane; Nonlinear conduction; Transmembrane voltage

Indexed keywords

ELECTRIC BREAKDOWN; ELECTRIC FIELDS; ELECTRIC POTENTIAL; ELECTROMAGNETIC FIELDS; IONIC CONDUCTION; LIPIDS; MOLECULAR STRUCTURE; PROTEINS; SIGNAL TO NOISE RATIO;

ELECTROPORATION; MOLECULAR TRANSPORT;

BIOLOGICAL MEMBRANES;

EID: 0344465279     PISSN: 10709878     EISSN: None     Source Type: Journal    
DOI: 10.1109/TDEI.2003.1237325     Document Type: Conference Paper

References (187)

1. E. Neumann, A. E. Sowers, and C. A. Jordan, editors, Electro-poration and Electrofusion in Cell Biology, Plenum Press, New York, 1989.
2. D. C. Chang, B. M. Chassy, J. A. Saunders, and A. E. Sowers, editors, Guide to Electroporation and Electrofusion, Academic Press, New York, 1992.
3. J. C. Weaver, "Electroporation: A General Phenomenon for Manipulating Cells and Tissue", J. Cellular Biochem., Vol. 51, pp. 426-435, 1993.
4. J. C. Weaver and Y. A. Chizmadzhev, "Electroporation". In C. Polk and E. Postow, editors, Handbook of Biological Effects of Electromagnetic Fields, CRC Press, Boca Raton, 2nd edition, 1996, pp. 247-274.
5. U. Zimmermann, editor, The Effects of High Intensity Electric Field Pulses on Eukaryotic Cell Membranes: Fundamentals and Applications, CRC Press, Boca Raton, 1996.
6. M. J. Jaroszeski, R. Gilbert, and R. Heller, editors, Electrically Mediated Delivery of Molecules to Cells: Electrochemotherapy, Electrogenetherapy and Transdermal Delivery by Electroporation, Humana Press, Totowa, 2000.
7. J. C. Weaver, "Electroporation of Cells and Tissues", IEEE Trans. Plasma Sci., Vol. 28, pp. 24-33, 2000.
8. K. H. Schoenbach, S. Katsuki, R. H. Stark, E. S. Buescher, and S. J. Beebe, "Bioelectrics - New Applications for Pulsed Power Technology," IEEE Trans. Plasma Sci., Vol. 30, pp. 293-300, 2002.
9. R. C. Lee and M. S. Kolodney, "Electrical Injury Mechanisms: Dynamics of the Thermal Response", Plast. Reconstr. Surg., Vol. 80, pp. 663-671, 1987.
10. R. C. Lee, D. Zhang, and J. Hannig, "Biophysical Injury Mechanisms in Electrical Shock Trauma", Ann. Rev. Biomedical Eng., Vol. 2, pp. 477-509, 2000.
11. W. Chen and R. C. Lee, "Altered Ion Channel Conductance and Ionic Selectivity Induced by Large Imposed Membrane Potential Pulses", Biophys., J., Vol. 67, pp. 603-612, 1994.
12. W. Chen, Y. Han, Y. Chen, and D. Astumiam, "Electric Field-induced Functional Reductions in the K+ Channels Mainly Resulted from Supramembrane Potential-medicated Electroconformational Changes", Biophys. J., Vol. 75, pp. 196-206, 1998.
13. M. Blank and E. Findl, editors, Mechanistic Approaches to Interactions of Electromagnetic Fields with Living Systems, Plenum Press, New York, 1987.
14. J. P. Reilly, Electrical Stimulation and Electropathology, Cambridge University Press, Cambridge, 1992.
15. W. Wiltschko and R. Wiltschko, Magnetic Orientation in Animals, Springer Verlag, Berlin, 1995.
16. C. Polk and E. Postow, editors, CRC Handbook of Biological Effects of Electromagnetic Fields, Second Edition, CRC Press, Boca Raton, 1996.
17. F. Bersani, editor, Electricity and Magnetism in Biology and Medicine, Plenum, New York, 1999.
18. J. C. Weaver, "Understanding Conditions for which Biological Effects of Nonionizing Electromagnetic Fields can be Expected", Bioelectrochemistry, Vol. 56, pp. 207-209, 2002.
19. J. C. Weaver and R. D. Astumian, "The Response of Cells to Very Weak Electric Fields: The Thermal Noise Limit", Science, Vol. 247, pp. 459-462, 1990.
20. R. K. Adair, "Constraints on Biological Effects of Weak Extremely-low-frequency Electromagnetic Fields", Phys. Rev. A, Vol. 43, pp. 1039-104, 1991.
21. R. D. Astumian, J. C. Weaver, and R. K. Adair, "Rectification and Signal Averaging of Weak Electric Fields by Biological Cells", Proc. Nat. Acad. Sci., Vol. 92, pp. 3740-3743, 1995.
22. J. C. Weaver, T. E. Vaughan, R. K. Adair, and R. D. Astumian, "Theoretical Limits on the Threshold for the Response of Long Cells to Weak ELF Electric Fields due to Ionic and Molecular Flux Rectification", Biophys. J., Vol. 75, pp. 2251-2254, 1998.
23. J. C. Weaver, T. E. Vaughan, and G. T. Martin, "Biological Effects due to Weak Electric and Magnetic Fields: The Temperature Variation Threshold", Biophys. J., Vol. 76, pp. 3026-3030, 1999.
24. J. C. Weaver, T. E. Vaughan, and R. D. Astumian, "Magnetically Sensitive Chemical Reactions Can Provide Biological Sensing of Small Field Differences", Nature, Vol. 405, pp. 707-709, 2000.
25. K. R. Foster, "Thermal and Nonthermal Mechanisms of Interaction of Radio-frequency Energy with Biological Systems", IEEE Trans. Plasma Sci., Vol. 28, pp. 15-23, 2000.
26. P. L. McNeil and S. Ito, "Molecular Traffic through Plasma Membrane Disruptions of Cells, in vivo,"J. Cell Sci., Vol. 96, pp. 549-556, 1990.
27. P. L. McNeil, "Cell Wounding and Healing", Am. Sci., Vol. 79, pp. 222-235, 1991.
28. P. L. McNeil and M. Terasaki, "Coping with the Inevitable: How Cells Repair a Torn Surface Membrane", Nat. Cell Biol., Vol. 3, pp. 124-129, 2001.
29. E. Neumann and S. Kakorin, "Electrooptics of Membrane Electroporation and Vesicle Shape Deformation", Current Opinion Colloid & Interface Science, Vol. 1, pp. 790-799, 1996.
30. E. Neumann, S. Kakorin, and K. Toensing, "Membrane Electroporation and Electromechanical Deformation of Vesicles and Cells", Faraday Discuss., Vol. 111, pp. 111-125, 1998.
31. V. L. Sukhorukov, H. Mussauer, and U. Zimmermann, "The Effect of Electrical Deformation Forces on the Electropermeabilization of Erythrocyte Membranes in Low- and High-conductivity Media", J. Membr. Biol., Vol. 163, pp. 235-245, 1998.
32. R. P. Joshi, Q. Hu, K. H. Schoenbach, and H. P. Hjalmarson, "Theoretical Prediction of Electromechanical Deformation of Cells Subjected to High Voltages for Membrane Electroporation, Phys. Rev. E, Vol, 65, pp. 021913-1021913-10, 2002.
33. T. Y. Tsong, "Electroporation of Cell Membranes", Biophysical J., Vol. 60, pp. 297-306, 1991.
34. R. Stämpfli, "Reversible Electrical Breakdown of the Excitable Membrane of a Ranvier Node", An. Acad. Brasil. Ciens., Vol. 30, pp. 57-63, 1958.
35. A. J. H. Sale and A. Hamilton, "Effects of High Electric Fields on Microorganisms: I. Killing of Bacteria and Yeasts", Biochem. Biophys. Acta, Vol. 148, pp. 781-788, 1967.
36. W. A. Hamilton and A. J. H. Sale, "Effects of High Electric Fields on Microorganisms: II. Killing of Bacteria and Yeasts", Biochim. Biophys. Acta, Vol. 148, pp. 7789-800, 1967.
37. A. J. H. Sale and W. A. Hamilton, "Effects of High Electric Fields on Microorganisms: III. Lysis of Erythrocytes and Protoplasts", Biochim. Biophys. Acta, Vol. 163, pp. 37-43, 1968.
38. E. Neumann and K. Rosenheck, "Permeability Changes Induced by Electric Impulses in Vesicular Membranes", J. Membrane Biol., Vol. 10, pp. 279-290, 1972.
39. I. G. Abidor, V. B. Arakelyan, L. V. Chernomordik, Yu. A. Chizmadzhev, V. F. Pastushenko, and M. R. Tarasevich, "Electric Breakdown of Bilayer Membranes: I. The Main Experimental Facts and Their Qualitative Discussion", Bioelectrochem. Bioenerget., Vol. 6, pp. 37-52, 1979.
40. V. F. Pastushenko, Yu. A. Chizmadzhev, and V. B. Arakelyan, "Electric Breakdown of Bilayer Membranes: II. Calculation of the Membrane Lifetime in the Steady-state Diffusion Approximation", Bioelectrochem. Bioenerget., Vol. 6, pp. 53-62, 1979.
41. Y. A. Chizmadzhev, V. B. Arakelyan, and V. F. Pastushenko, "Electric Breakdown of Bilayer Membranes: III. Analysis of Possible Mechanisms of Defect Origin", Bioelectrochem. Bioenerget., Vol. 6, pp. 63-70, 1979.
42. V. F. Pastushenko, Y. A. Chizmadzhev, and V. B. Arakelyan, "Electric Breakdown of Bilayer Membranes: IV. Consideration of the Kinetic Stage in the Case of the Single-defect Membrane", Bioelectrochem. Bioenerget., Vol. 6, pp. 71-79, 1979.
43. V. B. Arakelyan, Y. A. Chizmadzhev, and V. F. Pastushenko, "Electric Breakdown of Bilayer Membranes: V. Consideration of the Kinetic Stage in the Case of the Membrane Containing an Arbitrary Number of Defects", Bioelectrochem. Bioenerget., Vol. 6, pp. 81-87, 1979.
44. V. F. Pastushenko, V. B. Arakelyan, and Y. A. Chizmadzhev, "Electric Breakdown of Bilayer Membranes: VI. A Stochastic Theory Taking into Account the Processes of Defect Formation and Death: Membrane Lifetime Distribution Function", Bioelectrochem. Bioenerget., Vol. 6, pp. 89-95, 1979.
45. V. F. Pastushenko, V. B. Arakelyan, and Yu. A. Chizmadzhev, "Electric Breakdown of Bilayer Membranes: VII. A Stochastic Theory Taking into Account the Processes of Defect Formation and Death: Statistical Properties", Bioelectrochem. Bioenerget., Vol. 6, pp. 97-104, 1979.
46. 2+", Bioelectrochem. Bioenerget, Vol. 9, pp. 149-155, 1982.
47. V. F. Pastushenko and Y. A. Chizmadzhev, "Stabilization of Conducting Pores in BLM by Electric Current", Gen. Physiol. Biophys., Vol. 1, pp. 43-52, 1982.
48. K. C. Melikov, V. A. Frolov, A. Shcherbakov, A. V. Samsonov, and Y. A. Chizmadzhev, "Voltage-induced Nonconductive Prepores and Metastable Pores in Unmodified Planar Bilayer", Biophys. J., Vol. 80, pp. 1829-1836, 2001.
49. U. Zimmermann, F. Riemann, and G. Pilwat, "Enzyme Loading of Electrically Homogeneous Human Red Blood Cell Ghosts Prepared by Dielectric Breakdown", Biochim. Biophys. Acta, Vol. 436, pp. 460-474, 1976.
50. K. Kinosita, Jr. and T. Y. Tseng, "Formation and Resealing of Pores of Controlled Sizes in Human Erythrocyte Membrane", Nature, Vol. 268, pp. 438-441, 1977.
51. K. Kinosita Jr. and T. Y. Tsong, "Survival of Sucrose-loaded Erythrocytes in Circulation", Nature, Vol. 272, pp. 258-260, 1978.
52. J. Teissie and T. Y. Tsong, "Electric Field Induced Transient Pores in Phospholipid Bilayer Vesicles", Biochemistry, Vol. 20, pp. 1548-1554, 1981.
53. U. Zimmermann, P. Scheurich, G. Pilwat, and R. Benz, "Cells with Manipulated Functions: New Perspectives for Cell Biology, Medicine and Technology", Angew. Chem. Int. Ed. Eng., Vol. 20, pp. 325-344, 1981.
54. E. H. Serpersu, K. Kinosita, Jr., and T. Y. Tsong, "Reversible and Irreversible Modification of Erythrocyte Membrane Permeability by Electric Field", Biochem. Biophys. Acta, Vol. 812, pp. 779-785, 1985.
55. D. Auer, G. Brandner, and W. Bodemer, "Dielectric Breakdown of the Red Blood Cell Membrane and Uptake of SV 40 DNA and Mammalian Cell RNA", Naturwiss., Vol. 63, p. 391, 1976.
56. E. Neumann, M. Schaefer-Ridder, Y. Wang, and P. H. Hofschneider, "Gene Transfer Into Mouse Lyoma Cells by Electroporation in High Electric Fields", EMBO J., Vol. 1, pp. 841-845, 1982.
57. U. Zimmermann and G. Küppers, "Cell Fusion by Electromagnetic Waves and its Possible Relevance for Evolution", Naturwissenschaften, Vol. 70, pp. 568-569, 1983.
58. S. Demanéche, F. Bertolla, F. Buret, R. Nalin, A. Sailland, P. Auriol, T. M. Vogel, and P. Simonet, "Laboratory-scale Evidence for Lightning-mediated Gene Transfer in Soil", Appl. Environ. Microbiol., Vol. 67, pp. 3440-3444, 2001.
59. H. T. Tien, Bilayer lipid membranes (BLM): Theory and practice, Marcel Dekker, New York, 1974.
60. H. T. Tien, R. H Barish, L.-G. Gu, and A. L. Ottova, "Supported Bilayer Lipid Membranes as Ion and Molecular Probes", Analyt. Sci., Vol. 14, pp. 3-18, 1998.
61. R. Benz, F. Beckers, and U. Zimmermann, "Reversible Electrical Breakdown of Lipid Bilayer Membranes: A Charge-pulse Relaxation Study", J. Membrane Bio., Vol. 48, pp. 181-204, 1979.
62. R. Benz and U. Zimmermann, "Relaxation Studies on Cell Membranes and Lipid Bilayers in the High Electric Field Range", Bioelectrochem. and Bioenerg., Vol. 7, pp. 723-739, 1980.
63. A. Barnett and J. C. Weaver, "Electroporation: A Unified, Quantitative Theory of Reversible Electrical Breakdown and Rupture", Bioelectrochem. and Bioenerg., Vol. 25, pp. 163-182, 1991.
64. S. A. Freeman, M. A. Wang, and J. C. Weaver, "Theory of Electroporation for a Planar Bilayer Membrane: Predictions of the Fractional Aqueous Area, Change in Capacitance and Pore-pore Separation", Biophys. J., Vol. 67, pp. 42-56, 1994.
65. D. H. Michael, M. E. O'Neill, and J. C. Zuecher, "The Breakdown of Electrical Insulation in a Planar Layer of Insulating Fluid by Electrocapillary Instability, J. Fluid Mech., Vol. 47, Vol. 609-623, 1972.
66. J. M. Crowley, "Electrical Breakdown of Bimolecular Lipid Membranes as an Electromechanical Instability", Biophysical J., Vol. 13, pp, 711-724, 1973.
67. D. S. Dimitrov, "Electric Field-induced Breakdown of Lipid Bilayers and Cell Membranes: a Thin Viscoelastic Film Model", J. Membrane Biol., Vol. 78, pp. 53-60, 1984.
68. D. S. Dimitrov and R. K. Jain, "Membrane Stability", Biochim. Biophys. Acta, Vol. 779, pp. 437-468, 1984.
69. J. C. Weaver and Y. A. Chizmadzhev, "Theory of Electroporation: A Review", Bioelectrochem. Bioenerget., Vol. 41, pp. 135-160, 1996.
70. J. D. Litster, "Stability of Lipid Bilayers and Red Blood Cell Membranes", Phys. Lett., Vol. 53A, pp. 193-194, 1975.
71. C. Taupin, M. Dvolaitzky, and C. Sauterey, "Osmotic Pressure Induced Pores in Phospholipid Vesicles", Biochemistry, Vol. 14, pp. 4771-4775, 1975.
72. J. C. Weaver and R. A. Mintzer, "Decreased Bilayer Stability due to Transmembrane Potentials", Phys. Lett., Vol. 86A, pp. 57-59, 1981.
73. I. P. Sugar, "The Effects of External Fields on the Structure of Lipid Bilayers", J. Physiol. Paris, Vol. 77, pp. 1035-1042, 1981.
74. K. T. Powell and J. C. Weaver, "Transient Aqueous Pores in Bilayer Membranes: A Statistical Theory", Bioelectrochem. Bioelectroenerg., Vol. 15, pp. 211-227, 1986.
75. R. W. Glaser, S. L. Leikin, L. V. Chernomordik, V. F. Pastushenko, and A. I. Sokirko, "Reversible Electrical Breakdown of Lipid Bilayers: Formation and Evolution of Pores", Biochim. Biophys. Acta, Vol. 940, pp. 275-287, 1988.
76. K. A. DeBruin and W. Krassowska, "Electroporation and Shock-induced Transmembrane Potential in a Cardiac Fiber During Defibrillation Strength Shocks", Ann. Biomed. Eng., Vol. 26, pp. 584-596, 1998.
77. J. C. Neu and W. Krassowska, "Asymptotic Model of Electroporation", Phys. Rev. E, Vol. 59, pp. 3471-3482, 1999.
78. R. P. Joshi and K. H. Schoenbach, "Electroporation Dynamics in Biological Cells Subjected to Ultrafast Electrical Pulses: a Numerical Simulation Study", Phys. Rev. E, Vol. 62, pp. 1025-1033, 2000.
79. R. P. Joshi, Q. Hu, R. Aly, K. H. Schoenbach, and H. P. Hjalmarson, "Self-consistent Simulations of Electroporation Dynamics in Biological Cells Subjected to Ultrashort Pulses", Phys. Rev. E, Vol. 64, pp. 011913-1-011913-10, 2001.
80. R. P. Joshi, Q. Hu, K. H. Schoenbach, and H. P. Hjalmarson, "Improved Energy Model for Membrane Electroporation in Biological Cells Subjected to Electrical Pulses", Phys. Rev. E, Vol. 62, pp. 041920-1-041920-8, 2002.
81. R. P. Joshi and K. H. Schoenbach, "Mechanism for Membrane Electroporation Irreversibility under Highintensity, Ultrashort Pulse Conditions", Phys. Rev. E, Vol. 66, pp. 052901-1-052901-4, 2002.
82. A. Ridi, E. Scalas, and A. Gliozzi, "Noise Measurement in Bilayer Lipid Membranes During Electroporation", Eur. Phys. J. E, Vol. 2, pp. 161-168, 2000.
83. E. A. Gift and J. C. Weaver, "Observation of Extremely Heterogeneous Electroporative Molecular Uptake by Saccharomyces Cerevisiae which Changes with Electric Field Pulse Amplitude", Biochim. Biophys. Acta, Vol. 1234, pp. 52-62, 1995.
84. D. C. Bartoletti, G. I. Harrison, and J. C. Weaver, "The Number of Molecules Taken up by Electroporated Cells: Quantitative Determination", FEBS Letters, Vol. 256, pp. 4-10, 1989.
85. M. R. Prausnitz, B. S. Lau, C. D. Milano, S. Conner, R. Langer, and J. C. Weaver, "A Quantitative Study of Electroporation Showing a Plateau in Net Molecular Transport", Biophys. J., Vol. 65, pp. 414-422, 1993.
86. M. R. Prausnitz, C. D. Milano, J. A. Gimm, R. Langer, and J. C. Weaver, "Quantitative Study of Molecular Transport due to Electroporation: Uptake of Bovine Serum Albumin by Human Red Blood Cell Ghosts", Biophys. J., Vol. 66, pp. 1522-1530, 1994.
87. E. A. Gift and J. C. Weaver, "Simultaneous Quantitative Determination of Electroporative Molecular Uptake and Subsquent Cell Survival Using Gel Microdrops and Flow Cytometry", Cytometry, Vol. 39, pp. 243-249, 2000.
88. Y. Huang and B. Rubinsky, "Micro-electroporation: Improving the Efficiency and Understanding of Electrical Permeabilization of Cells", Biomedical Microdevices, Vol. 2, pp. 145-150, 1999.
89. R. Davalos, Y. Huang, and B. Rubinsky, "Electroporation: Bioelectrochemical Mass Transfer at the Nano Scale", Microscale Thermophys. Engr., Vol. 4, pp. 147-159, 2000.
90. Y. Huang and B. Rubinsky, "Microfabricated Electroporation Chip for Single Cell Membrane Permeabilization", Sensors and Actuators A, Vol. 89, Vol. 242-249, 2001.
91. J. A. Lundqvist, F. Sahlin, M. A. Aberg, A. Stromberg, P. S. Eriksson, and O. Orwar, "Altering the Biochemical State of Individual Cultured Cells and Organelles with Ultramicroelectrodes", Proc. Natl. Acad. Sci., Vol. 95, pp. 10356-10360, 1998.
92. F. Ryttsén, C. Farre, C. Brennan, S. G. Weber, K. Nolkrantz, K. Jardemark, D. T. Chiu, and O. Orwar, "Characterization of Single-cell Electroporation by Using Patch-clamp and Fluorescence Microscopy", Biophysical J., Vol. 79, pp. 1993-2001, 2000.
93. D. S. Dimitrov and A. E. Sowers, "Membrane Electroporation-fast Molecular Exchange by Electroosmosis", Biochim. Biophys. Acta, Vol. 1022, pp. 381-392, 1990.
94. L. V. Chernomordik, A. V. Sokolov, and V. G. Budker, "Electrostimulated Uptake of DNA by Liposomes", Biochim. Biophys. Acta, Vol. 1024, pp. 179-183, 1990.
95. M. P. Rols, P. Femenia, and J. Teissie, "Long-lived Macropinocytosis Takes Place in Electropermeabilized Mammalian Cells", Biochem. Biophys. Res. Commun., Vol. 208, pp. 26-35, 1995.
96. S. Šatkauskas, M. F. Bureau, A. Mahfoudi, and L. M. Mir, "Slow Accumulation of Plasmid in Muscle Cells: Supporting Evidence for a Mechanism of DNA Uptake by Receptor-mediated Endocytosis", Mol. Ther., Vol. 4, pp. 317-323, 2001.
97. W. Mehrle, U. Zimmermann, and R. Hampp, "Evidence for Asymmetrical Uptake of Fluorescent Dyes Through Electro-permeabilized Membranes of Avena Meosphyll Protoplasts", FEBS Lett., Vol. 185, pp. 89-94, 1985.
98. C. S. Djuzenova, U. Zimmermann, H. Frank, V. L. Sukhrukoov, E. Richter, and G. Fuhr, "Effect of Medium Conductivity and Composition on the Uptake of Propidium Iodide into Electropermeabilized Myeloma Cells", Biochim. Biophys. Acta, Vol. 1284, pp. 143-152, 1996.
99. B. Gabriel and J. Teissie, "Time Courses of Mammalian Cell Electropermeabilization Observed by Millisecond Imaging of Membrane Property Changes During the Pulse", Biophys. J., Vol. 76, pp. 2158-2165, 1999.
100. E. Tekle, R. D. Astumian, W. A. Fraiuf, and P. B. Chokk, "Asymmetric Pore Distribution and Loss of Membrane Lipid in Electroporated DOPC Vesicles", Biophys. J., Vol. 81, pp. 960-968, 2001.
101. M. Golzio, J. Teissie, and M. P. Rols, "Direct Visualization at the Single-cell Level of Electrically Mediated Gene Delivery", Proc. Nat. Acad. Sci., Vol. 99, pp. 1292-1297, 2002.
102. J. C. Weaver and A. Barnett, Guide to Electroporation and Electrofusion, Ch. "Progress Towards a Theoretical Model of Electroporation Mechanism: Membrane Electrical Behavior and Molecular Transport", Academic Press, New York, pp. 91-117, 1992.
103. S. I. Sukharev, V. A. Klenchin, S. M. Serov, L. V. Chernomordik, and Y. A. Chizmadzhev, "Electroporation and Electrophoretic DNA Transfer into Cells. The Effect of DNA Interaction with Electropores", Biophys. J., Vol. 63, pp. 1320-1327, 1992.
104. J. C. Weaver, R. Vanbever, T. E. Vaughan, and M. R. Prausnitz, "Heparin Alters Transdermal Transport Associated with Electroporation", Biochem. Biophy. Res. Comm., Vol. 234, pp. 637-640, 1997.
105. P.-G. de Gennes, "Passive Entry of a DNA Molecule into a Small Pore", Proc. Nat. Acad. Sci., Vol. 96, pp. 7262-7264, 1999.
106. Y. Mouneimne, P.-F. Tosi, Y. Gazitt, and C. Nicolau, "Electro-insertion of Xeno-glycophorin into the Red Blood Cell Membrane", Biochem. Biophys. Res. Comm., Vol. 159, pp. 34-40, 1989.
107. M. Zeira, P.-F. Tosi, Y. Mouneimne, J. Lazarte, L. Sneed, D. J. Volsky, and C. Nicolau, "Full-length CD4 Electro-inserted in the Erythrocyte Membrane as a Long-lived Inhibitor of Infection by Human Immunodeficiency Virus", Proc. Nat. Acad. Sci., Vol. 88, pp. 4409-4413, 1991.
108. C. Nicolau, Y. Mouneimne, and P.-F. Tosi, "Electroinsertion of Proteins in the Plasma Membrane of Red Blood Cells", Analytic. Biochem., Vol. 1993, pp. 1-10, 1993.
109. K. E. Ouagari, J. Teissie, and H. Benoist, "Glycophorin a Protects K562 Cells from Natural Killer Cell Attack", J. Biol. Chem., Vol. 270, pp. 26970-26975, 1995.
110. D. Mycue, J. Zahn, M. Zahn, and J. C. Weaver, "Interaction Mechanism of Electric Fields with Cells: Alteration of Binding Site Access of Membrane Proteins", in M. Blank, editor, Electricity and Magnetism in Biology and Medicine, San Francisco Press, San Francisco, pp. 773-776, 1993.
111. M. Balázs, J. Matkó, J. Szöllósi, L. Mátyus, M. J. Fulwyler, and S. Damjanovich, "Accessibility of Cell Surface Thiols in Human Lymphocytes is Altered by Ionophores or OKT-3 Antibody", Biochem. Biophys. Res. Comm., Vol. 140, pp. 999-1006, 1986.
112. K. H. Schoenbach, F. E. Peterkin, R. W. Alden III, and S. J. Beebe, "The Effect of Pulsed Electric Fields on Biological Cells: Experiments and Applications", IEEE Trans. Plasma Sci., Vol. 23, 1997.
113. P. Lubicki. and S. Jayaram, "High Voltage Pulse Application for the Destruction of the Gram-negative Bacterium Yersinia enterocolitic", Bioelectrochem. Bioenerget., Vol, 43, pp. 135-141, 1997.
114. H. M. Eppich, R. Foxall, K. Gaynor, D. Dombkowski, N. Mirua, T. Cheng, S. Silva-Arrieta, R. H. Evans, J. A. Mangano, F. I. Preffer, and D. T. Scadden, "Pulsed Electric Fields for Selection of Hematopoietic Cells and Depletion of Tumor Cell Contaminants", Nat. Biotechnol., Vol. 18, pp. 882-887, 2000.
115. A. Abou-Ghazala and K. H. Schoenbach, "Biofouling Prevention with Pulsed Electric Fields", IEEE Trans. Plasma Sci., Vol. 28, pp. 115-121, 2000.
116. H. M. Ulmer, V. Heinz, M. G., Gänzle, D. Knorr, and R. F. Vogel, "Effects of Pulsed Electric Fields on Inactivation and Metabolic Activity of Lactobacillus plantarum in Model Beer", J. Appl. Microbiol., Vol. 93, pp. 326-335, 2002.
117. H. H. Lado and A. E. Yousef, "Alternative Food-preservation Technologies: Efficacy and Mechanisms", Microbes. Infect., Vol. 4, pp. 443-440, 2002.
118. L. M. Mir, H. Banoun, and C. Paoletti, "Introduction of Definite Amounts of Nonpermeant Molecules into Living Cells After Electropermeabilization: Direct Access to the Cytosol",Exp. Cell Res., Vol. 175, pp, 15-25, 1988.
119. B. Poddevin, S. Orlowski, J. Belehradek Jr., and L. M. Mir, "Very High Cytotoxicity of Bleomycin Introduced into the Cytosol of Cells in Culture", Biochem. Pharmacol., Vol. 42, Suppl., pp. 567-575, 1991.
120. L. M. Mir, "Therapeutic Perspectives of in vivo Cell Electropermeabilization", Bioelectrochemistry, Vol. 53, pp. 1-10, 2001.
121. M. Bier, W. Chen, T. R. Gowrishankar, R. D. Astumian, and R. C. Lee, "Resealing Dynamics of a Cell Membrane after Electroporation", Phys. Rev. E, Vol. 66, pp. 062905-1-062905-4, 2002.
122. D. C. Chang and T. S. Reese, "Changes in Membrane Structure Induced by Electroporation as Revealed by Rapid-freezing Electron Microscopy", Biophysical J., Vol. 58, pp. 1-12, 1990.
123. O. Sandre, L. Moreaux, and F. Brochard-Wyart, "Dynamics of Transient Pores in Stretched Vesicles", Proc. Nat. Acad. Sci., Vol. 96, pp. 10591-10596, 1999.
124. F. Brochard-Wyart, P. G. de Gennes, and O. Sandre, "Transient Pores in Stretched Vesicles: Role of Leak-out", Physica A, 'Vol. 278, pp. 32-51, 2000.
125. U. Bröggemann, E. C. Roux, J. Hannig, and C. Nicolau, "Low-oxygen-affinity Red Cells Produced in a Large Volume, Continuous-flow Electroporation System", Transfusion, Vol. 35, pp. 478-486, 1995.
126. S. Sixou and J. Teissie, "Specific Electropermeabilization of Leucocytes in a Blood Sample and Application to Large Volume Samples", Biochim. Biophys. Acta, Vol. 1028, pp. 154-160, 1990.
127. i Signals Generated by Electroporation Functionally Mimic Those Evoked by Hormonal Stimulation", FASEB J., Vol. 13, pp. 365-376, 1999.
128. T. C. Bakker Schut, B. G. de Grooth, and J. Greve, "A New Principle of Cell Sorting by Using Selective Electroporation in a Modified Flow Cytometer", Cytometry, Vol. 11, pp. 659-666, 1990.
129. I. Uno, K. Fukami, H. Kato, T. Takenawa, and T. Ishikawa, "Essential Role for Phosphatidylinositol 4,5 Bisphosphate in Yeast Cell Proliferation", Nature, Vol. 333, pp. 188-190, 1988.
130. D. L. Berglund and J. R. Starkey, Isolation of Viable Tumor Cells Following Introduction of Labelled Antibody to an Intracellular Oncogene Product Using Electroporation", J. Immunol. Methods, Vol. 125, pp. 79-87, 1989.
131. M. Rui, Y. Chen, Y. Zhang, and D. Ma, "Transfer of Anti-TFAR19 Monoclonal Antibody into HeLa Cells by in Situ Electroporation Can Inhibit Apoptosis", Life Sci., Vol. 71, pp. 1771-1778, 2002.
132. J. C. Weaver, "Molecular Basis for Cell Membrane Electroporation", Ann. N. Y. Acad. Sci., Vol. 720, pp. 141-152, 1994.
133. M. Okino and H. Mohri, "Effects of a High-voltage Electrical Impulse and an Anticancer Drug on in vivo Growing Tumors", Jpn. J. Cancer Res., Vol. 78, pp. 1319-1321, 1987.
134. K. T. Powell, A. W. Morgenthaler, and J. C. Weaver, "Tissue Electroporation: Observation of Reversible Electrical Breakdown in Viable Frog Skin", Biophys. J., Vol. 56, pp. 1163-1171, 1989.
135. O. Tovar and L. Tung, "Electroporation of Cardiac Cell Membranes with Monophasic or Biphasic Rectangular Pulses", Pacing Clin. Electrophysiol., Vol. 14, pp. 1887-1892, 1991.
136. J. Gehl, T. Skovsgaard, and L. M. Mir, "Vascular Reactions to in vivo Electroporation: Characterization and Consequences for Drug and Gene Delivery", Biochim. Biophys. Acta, Vol. 1428, pp. 233-240, 1999.
137. L. M. Mir, S. Orlowski, Jr. J. Belehradek, and C. Paoletti, "In Vivo Potentiation of the Bleomycin Cytotoxicity by Local Electric Pulses", Eur. J. Cancer, Vol. 27, pp. 68-72, 1991.
138. R. Heller, M. Jarozeski, J. Leo-Messina, R. Perrot, N. Van Voorhis, D. Reintgen, and R. Gilbert, "Treatment of B16 Mouse Melanoma with the Combination of Electropermeabilization and Chemotherapy", Bioelectrochem. Bioenerget., Vol. 36, pp. 83-87, 1995.
139. R. Heller, M. Jaroszeski, A. Atkin, D. Moradpour, R. Gilbert, J. Wands, and C. Nicolau, "In Vivo Gene Electroinjection and Expression in Rat Liver", FEBS Lett., Vol. 389, pp. 225-228, 1996.
140. L. M. Mir, M. F. Bureau, J. Gehl, R. Rangara, D. Rouy, J-M. Caillaud, P. Delaere, D. Brannellec, B. Schwarts, and D. Scherman, "High-efficiency Gene Transfer into Skeletal Muscle Mediated by Electric Pulses", Proc. Natl. Acad. Sci., Vol. 96, pp. 4262-4267, 1999.
141. H. Schaefer and T. E. Redelmeier, Skin Barrier: Principles of Percutaneous Absorption, Karger, Basel, 1996.
142. A. S. Michaels, S. K. Chandrasekaran, and J. E. Shaw, "Drug Permeation Through Human Skin: Theory and in vitro Experimental Measurements", AIChE J., Vol. 21, pp. 985-996, 1975.
143. M. R. Prausnitz, V. G. Bose, R. Langer, and J. C. Weaver, "Electroporation of Mammalian Skin: A Mechanism to Enhance Transdermal Drug Delivery", Proc. Nat. Acad. Sci., Vol. 90, pp. 10504-10508, 1993.
144. J. C. Weaver, T. E. Vaughan, and Y. Chizmadzhev, "Theory of Electrical Creation of Aqueous Pathways Across Skin Transport Barriers", Advanced Drug Delivery Reviews, Vol. 35, pp. 21-39, 1999.
145. Y. Chizmadzhev, A. V. Indenbom, P. I. Kuzmin, S. V. Galinchenko, J. C. Weaver, and R. Potts, "Electrical Properties of Skin at Moderate Voltages: Contribution of Appendageal Macropores", Biophys. J., Vol. 74, pp. 843-856, 1998.
146. J. C. Weaver and R. Langer, "Electrochemical Creation of Large Aqueous Pathways: An Approach to Transdermal Drug Delivery", Progress in Dermatology, Vol. 33, pp. 1-10, 1999.
147. G. Martin, U. Pliquett, and J. C. Weaver, "Theoretical Analysis of Localized Heating in Human Skin Subjected to High Voltage Pulses", Bioelectrochemistry, Vol. 57, pp. 55-64, 2002.
148. U. Pliquett, G. T. Martin, and J. C. Weaver, "Experimental Detection of the Temperature Rise within Human Stratum Corneum during High Voltage Pulsing", Bioelectrochemistry, Vol. 57, pp. 65-72.
149. T. E. Zewert, U. F. Pliquett, R. Langer, and J. C. Weaver, "Transdermal Transport of DNA Antisense Oligonucleotides by Electroporation", Biochem. Biophy. Res. Comm., Vol. 212, pp. 286-292, 1995.
150. T. E. Zewert, U. Pliquett, R. Vanbever, R. Langer, and J. C. Weaver, "Creation of Transdermal Pathways for Macromolecule Transport by Skin Electroporation and a Low Toxicity, Pathway-enlarging Molecule", Bioelectrochem. Bioenerget., Vol. 49, pp. 11-20, 1999.
151. U. F. Pliquett, T. E. Zewert, T. Chen, R. Langer, and J. C. Weaver, "Imaging of Fluorescent Molecule and Small Ion Transport Through Human Stratum Corneum During High-voltage Pulsing: Localized Transport Regions are Involved", J. Biophys. Chem., Vol. 58, pp. 185-204, 1996.
152. M. R. Prausnitz, J. A. Gimm, R. H. Guy, R. Langer, J. C. Weaver, and C. Cullander, "Imaging Regions of Transport Across Human Stratum Corneum During High Voltage and Low Voltage Exposures", J. Pharm. Sci., Vol. 85, pp. 1363-1370, 1996.
153. T. R. Gowrishankar, T. O. Herndon, T. E. Vaughan, and J. C. Weaver, "Spatially Constrained Localized Transport Regions due to Skin Electroporation", J. Controlled Release, Vol. 60, pp. 101-110, 1999.
154. L. Ilic, T. R. Gowrishankar, T. E. Vaughan, T. O. Herndon, and J. C. Weaver, "Spatially Constrained Skin Electroporation with Sodium Thiosulfate and Urea Creates Transdermal Micro-conduits", J. Control. Release, Vol. 61, pp. 185-202, 1999.
155. L. Ilic, T. R. Gowrishankar, T. E. Vaughan, T. O. Herndon, and J. C. Weaver, "Microfabrication of Individual 200 pm Diameter Microconduits using High Voltage Pulsing in Salicylic Acid and Benzoic Acid", J. Invest. Dermatol., Vol. 116, pp. 40-49, 2001.
156. R. C. Lee and M. S. Kolodney, "Electrical Injury Mechanisms: Electrical Breakdown of Cell Membranes", Plast. Reconstr. Surg., Vol. 80, pp. 672-679, 1987.
157. D. C. Gaylor, K. Prakah-Asante, and R. C. Lee, "Significance of Cell Size and Tissue Structure in Electrical Trauma", J. Theor. Biol., Vol. 133, pp. 223-237, 1988.
158. R. C. Lee, "Injury by Electrical Forces: Pathology, Manifestations, and Therapy", Curr. Probl. Surg., Vol. 34, pp. 677-764, 1997.
159. R. C. Lee, L. P. River, F.-S. Pan, L. Ji, and R. L. Wollmann, "Surfactant Induced Sealing of Electropermeabilized Skeletal Muscle Membranes in vivo", Proc. Nat. Acad. Sci., Vol. 89, pp. 4524-4528, 1992.
160. D. Miklavčič, K. Beravs, D. Semrov, M. Cemazar, F. Demsar, and G. Sersa, "The Importance of Electric Field Distribution for Effective in vivo Electroporation of Tissues", Biophys. J., Vol. 74, pp. 2151-2158, 1998.
161. J. C. Lin and O. P. Gandhi, "Computational Methods for Predicting Field Intensity", in C. Polk and E. Postow, editors, Handbook of Biological Effects of Electromagnetic Fields, CRC Press, Boca Raton, 2nd edition, pp. 337-402, 1996.
162. R. V. Davalos, B. Rubinsky, and D. M. Otten, "A Feasibility Study for Electrical Impedance Tomography as a Means to Monitor Tissue Electroporation for Molecular Medicine", IEEE Trans. Biomed. Eng., Vol. 49, pp. 400-403, 2002.
163. T. R. Gowrishankar and J. C. Weaver, "An Approach to Electrical Modeling of Single and Multiple Cells", Proc. Nat. Acad. Sci., Vol. 100, pp. 3203-3208, 2003.
164. K. H. Schoenbach, S. J. Beebe, and E. S. Buescher, "Intracellular Effect of Ultrashort Pulses", Bioelectromagnetics, Vol. 22, pp. 440-448, 2001.
165. S. J. Beebe, P. M. Fox, L. J. Rec, K. Somers, R. H. Stark, and K. H. Schoenbach, "Nanosecond Pulsed Electric Field (nsPEF) Effects on Cells and Tissues: Apoptosis Induction and Tumor Growth Inhibition", IEEE Trans. Plasma Sci., Vol. 30, pp. 286-292, 2002.
166. S. J. Beebe, P. M. Fox, L. J. Rec, L. K. Willis, and K. H. Schoenbach, "Nanosecond, High Intensity Pulsed Electric Fields Induce Apoptosis in Human Cells", FASEB J., Vol. 30, pp. 286-292, 2003.
167. J. M. Collombet, V. C. Wheeler, F. Vogel, and C. Coutelle, "Introduction of Plasmid DNA into Isolated Mitochondria by Electroporation, a Novel Approach Toward Gene Correction for Mitochondrial Disorders", J. Biol. Chem., Vol. 21, pp. 5342-5347, 1997.
168. A. M. Estevez, O. H. Thiemann, J. D. Alfonzo, and L. Simpson, "T7 RNA Polymerase-driven Transcription in Mitochondria of Leishmania Tarentolae and Trypanosoma Brucei", Mol. Bioehem. Parasitol., Vol. 103, pp. 251-259, 1999.
169. J. C. Farre and A. Araya, "Gene Expression in Isolated Plant Mitochondria: High Fidelity of Transcription, Splicing and Editing of a Transgene Product in Electroporated Organelles", Nucleic Acids Res., Vol. 29, pp. 2484-2491, 2001.
170. A. McGregor, R. Temperley, Z. M. Chrzanowska-Lightowlers, and R. N. Lightowlers, "Absence of Expression from RNA Internalized into Electroporated Mammalian Mitochondria", Mol. Genet. Genomics, Vol. 5, pp. 721-729, 2001.
171. C. M. Palmeira and K. B. Wallace, "Benzoquinone Inhibits the Voltage-dependent Induction of the Mitochondrial Permeability Transition Caused by Redox-cycling Naphthoquinones", Toxicol. Appl. Pharmacol., Vol. 143, pp. 338-347, 1997.
172. N. Leducq, M.-C. Delmas-Beavieux, I. Bourdel-Marchasson, S. Dufour, J.-L. Gallis, P. Canioni, and P. Diolez, "Mitochondrial Permeability Transition during Hypothermic to Normothermic Reperfusion in Rat Liver Demonstrated by the Protective Effect of Cyclosporin", A. Bioehem. J., Vol. 336, pp. 501-506, 1998.
173. I. Lee, E. Bender, S. Arnold, and B. Kadenbach, "New Control of Mitochondrial Membrane Potential and ROS Formation - a Hypothesis", Biol. Chem., Vol. 382, pp. 1629-1636, 2001.
174. J. Darnell, H. Locish, and D. Baltimore, Molecular Cell Biology, Scientific American Books, New York, 1986.
175. G. B. Benedek and F. M. H. Villars, Physics with Illustrative Examples from Medicine and Biology, 2nd Ed.: Volume 3, Electricity and Magnetism, AIP Press, New York, 2000.
176. A. P. Halestrap, G. P. McStay, and S. J. Clarke, "The Permeability Transition Pore Complex: Another View", Biochimie, Vol. 84, pp. 153-166, 2002.
177. Y. Tsujimot and S. Shimizu, "The Voltage-dependent Anion Channel: an Essential Player in Apoptosis", Biochmie, Vol. 84, pp. 187-193, 2002.
178. V. Petronilli, A. Nicolli, P. Costantini, R. Colonna, and P. Bernardi, "Regulation of the Permeability Transition Pore, a Voltage-dependent Mitochondrial Channel Inhibited by Cyclosporin A", Biochim. Biophys. Acta, Vol. 1187, pp. 255-259, 1994.
179. 2+-dependent Channel Formed by Recombinant ADP/ATP Carrier from Neurospora crassa Resembles the Mitochondrial Permeability Transition Pore", Biochemistry, Vol. 41, pp. 11804-11811, 2002.
180. C. Loupatatzis, G. Seitz, P. Schonfeld, F. Lang, and D. Siemen, "Single-channel Currents of the Permeability Transition Pore from the Inner Mitochondrial Membrane of Rat Liver and of a Human Hepatoma Cell Line", Cell Physiol. Biochem., Vol. 12, pp. 269-278, 2002.
181. G. Bainbridge, I. Gokce, and J. H. Lakey, "Voltage Gating is a Fundamental Feature of Porin and Toxin β-barrel Membrane Channels", FEES Lett., Vol. 431, pp. 305-308, 1998.
182. F. Hofmann, L. H. Scheller, W. Strupp, U. Zimmermann, and C. Jassoy, "Electric Field Pulses Can Induce Apoptosis", J. Membr. Biol., Vol. 169, pp. 103-109, 1999.
183. S. Kakorin, S. P. Stoylov, and E. Neumann, "Electro-optics of Membrane Electroporation in Diphenylhexatriene-doped Lipid Bilayer Vesicles", Biophys. Chem., Vol. 58, pp. 109-116, 1996.
184. W. Knoll, C. W. Frank, C. Heibel, R. Naumann, A. Offenhäuser, J. Rühe, E. K. Schmidt, W. W. Shen, and A. Sinner, "Functional Tethered Lipid Bilayers", Rev. Molec. Biotech., Vol. 74, pp. 137-158, 2000.
185. P. Bassereau and F. Pincet, "Quantitative Analysis of Holes in Supported Bilayers Providing the Absorption Energy of Surfactants on Solid Substrate", Langmuir, Vol. 13, pp. 7003-7007, 1997.
186. T. Gassier, A. Sinner, A. Offenhäuser, and H. Möhwald, "Homogeneity, Electrical Resistivity and Lateral Diffusion of Lipid Bilayers Coupled to Polyelectrolyte Multilayers", Colloids and Surfaces B: Biointerfaces, Vol. 15, pp. 215-225, 1999.
187. T. Hianik and A. Labajova, "Electrostriction of Supported Lipid Films at Presence of Cationic Surfactants, Sufactant-DNA and DNA-Mg(2 +) Complexes", Bioelectrochemistry, Vol. 58, pp. 97-105, 2002.