Electroporation in cells and tissues: A biophysical phenomenon due to electromagnetic fields

The effect of “strong” electromagnetic fields on cells and tissue can be dramatic but not necessarily harmful. The essentially universal biophysical phenomenon of “electroporation” occurs if an applied field causes the cell transmembrane voltage to reach about 0.5–1 V in a time of microseconds to milliseconds. Ordinarily the cell membrane is a formidable barrier to the transport of ions and charged molecules. However, electroporation results in a large increase in transmembrane conductance, which is believed to be caused by ion transport through temporary membrane openings (“pores”). This high-conductance state limits the transmembrane voltage and thereby protects the membrane. A large increase in molecular transport generally occurs for the same conditions and allows polar molecules to be introduced into cells. Similar enhanced molecular transport can be caused in living tissues. Not only cell membranes, but also cell layers or even the stratum corneum of human skin can be temporarily altered by the electrical creation of aqueous pathways. The mechanism of electroporation is partially understood, in that the electrical and mechanical behavior of artificial planar bilayer membranes can be described quantitatively by a theoretical model based on transient aqueous pores. More complex behavior in cell membranes may be due to both the complicated shapes of cell membranes and the additional participation of metastable pores and interactions with cell structures. In the case of tissues the situation is even more complex and has only recently begun to be studied but has the prospect of providing a new approach to transporting polar molecules across tissue barriers.

[1]  J. Kirschvink,et al.  Magnetite biomineralization in the human brain. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[2]  S. Sukharev,et al.  In vivo electroporation and stable transformation of skin cells of newborn mice by plasmid DNA. , 1991, Biochimica et biophysica acta.

[3]  M. S. Clarke,et al.  Syringe loading introduces macromolecules into living mammalian cell cytosol. , 1992, Journal of cell science.

[4]  James C. Weaver,et al.  7 – Progress toward a Theoretical Model for Electroporation Mechanism: Membrane Electrical Behavior and Molecular Transport , 1991 .

[5]  L. Sagan Epidemiological and laboratory studies of power frequency electric and magnetic fields. , 1992, JAMA.

[6]  L. Chernomordik,et al.  467—The reversible electrical breakdown of bilayer lipid membranes modified by uranyl ions , 1982 .

[7]  A. Sowers The Study of Membrane Electrofusion and Electroporation Mechanisms , 1989 .

[8]  L. Mir,et al.  Cell electropermeabilization: a new tool for biochemical and pharmacological studies. , 1993, Biochimica et biophysica acta.

[9]  R. Astumian,et al.  Estimates for ELF effects: noise-based thresholds and the number of experimental conditions required for empirical searches. , 1992, Bioelectromagnetics.

[10]  Electrical Trauma: Electrical injury to heart muscle cells , 1992 .

[11]  J. Weaver,et al.  Electroporation: A general phenomenon for manipulating cells and tissues , 1993, Journal of cellular biochemistry.

[12]  M. Okino,et al.  Optimal Electric Conditions in Electrical Impulse Chemotherapy , 1992, Japanese journal of cancer research : Gann.

[13]  D. Volsky,et al.  Full-length CD4 electroinserted in the erythrocyte membrane as a long-lived inhibitor of infection by human immunodeficiency virus. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[14]  W. Hamilton,et al.  Effects of high electric fields on microorganisms: I. Killing of bacteria and yeasts , 1967 .

[15]  Adair,et al.  Constraints on biological effects of weak extremely-low-frequency electromagnetic fields. , 1991, Physical review. A, Atomic, molecular, and optical physics.

[16]  L. Chernomordik,et al.  The electrical breakdown of cell and lipid membranes: the similarity of phenomenologies. , 1987, Biochimica et biophysica acta.

[17]  S. Schuster,et al.  Transfer of monoclonal antibodies into mammalian cells by electroporation. , 1989, The Journal of biological chemistry.

[18]  J. Weaver,et al.  Transient aqueous pores in bilayer membranes: A statistical theory , 1986 .

[19]  E. Neumann,et al.  Stochastic model for electric field-induced membrane pores. Electroporation. , 1984, Biophysical chemistry.

[20]  James C. Weaver,et al.  Decreased bilayer stability due to transmembrane potentials , 1981 .

[21]  T. Tsong,et al.  Resonance electroconformational coupling: A proposed mechanism for energy and signal transductions by membrane proteins , 1989, Bioscience reports.

[22]  L. Chernomordik,et al.  Electroporation and electrophoretic DNA transfer into cells. The effect of DNA interaction with electropores. , 1992, Biophysical journal.

[23]  L. Chernomordik 5 – Electropores in Lipid Bilayers and Cell Membranes , 1991 .

[24]  M. R. Tarasevich,et al.  [Electrical breakdown of lipid bilayer membranes]. , 1978, Doklady Akademii nauk SSSR.

[25]  Sugár Ip The effects of external fields on the structure of lipid bilayers. , 1981 .

[26]  C. Nicolau,et al.  Electro-insertion of xeno-glycophorin into the red blood cell membrane. , 1989, Biochemical and biophysical research communications.

[27]  L. Mir,et al.  Electrochemotherapy potentiation of antitumour effect of bleomycin by local electric pulses. , 1991, European journal of cancer.

[28]  J. Crowley,et al.  Electrical breakdown of bimolecular lipid membranes as an electromechanical instability. , 1973, Biophysical journal.

[29]  A Brun,et al.  A new brain tumour therapy combining bleomycin with in vivo electropermeabilization. , 1993, Biochemical and biophysical research communications.

[30]  J. A. Gimm,et al.  Quantitative study of molecular transport due to electroporation: uptake of bovine serum albumin by erythrocyte ghosts. , 1994, Biophysical journal.

[31]  J. Weaver,et al.  Tissue electroporation. Observation of reversible electrical breakdown in viable frog skin. , 1989, Biophysical journal.

[32]  R. Benz,et al.  Pulse-length dependence of the electrical breakdown in lipid bilayer membranes. , 1980, Biochimica et biophysica acta.

[33]  T. Tsong,et al.  Study of mechanisms of electric field-induced DNA transfection. II. Transfection by low-amplitude, low-frequency alternating electric fields. , 1990, Biophysical journal.

[34]  U. Zimmermann,et al.  Large scale transfection of mouse L-cells by electropermeabilization. , 1987, Biochimica et biophysica acta.

[35]  L. Chernomordik,et al.  Reversible electrical breakdown of lipid bilayers: formation and evolution of pores. , 1988, Biochimica et biophysica acta.

[36]  R. Lee,et al.  Surfactant-induced sealing of electropermeabilized skeletal muscle membranes in vivo. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[37]  J. L. Phillips Effects of electromagnetic field exposure on gene transcription , 1993, Journal of cellular biochemistry.

[38]  J. Kirschvink,et al.  Comment on "Constraints on biological effects of weak extremely-low-frequency electromagnetic fields" , 1992, Physical review. A, Atomic, molecular, and optical physics.

[39]  M. Okino,et al.  Effects of a high-voltage electrical impulse and an anticancer drug on in vivo growing tumors. , 1987, Japanese journal of cancer research : Gann.

[40]  J. Weaver Molecular Basis for Cell Membrane Electroporation a , 1994, Annals of the New York Academy of Sciences.

[41]  T. Tsong,et al.  Electroporation of cell membranes. , 1991, Biophysical journal.

[42]  J. Weaver,et al.  Electroporation: High frequency of occurrence of a transient high‐permeability state in erythrocytes and intact yeast , 1988, FEBS letters.

[43]  L. Mir,et al.  Electrochemotherapy tumor treatment is improved by interleukin-2 stimulation of the host's defenses. , 1992, European cytokine network.

[44]  J. Weaver,et al.  A quantitative theory of reversible electrical breakdown in bilayer membranes , 1986 .

[45]  D. Chang 2 – Structure and Dynamics of Electric Field-Induced Membrane Pores as Revealed by Rapid-Freezing Electron Microscopy , 1991 .

[46]  Roland Benz,et al.  Cells with Manipulated Functions: New Perspectives for Cell Biology, Medicine, and Technology , 1981 .

[47]  Yasuyuki Yamada,et al.  A novel method for transformation of intact yeast cells by electroinjection of plasmid DNA , 1985, Applied Microbiology and Biotechnology.

[48]  L. Chernomordik,et al.  Breakdown of lipid bilayer membranes in an electric field , 1983 .

[49]  L. Chernomordik,et al.  Electrically induced DNA uptake by cells is a fast process involving DNA electrophoresis. , 1991, Biophysical journal.

[50]  N Crawford,et al.  Reversible electropermeabilisation of human and rat blood platelets: evaluation of morphological and functional integrity 'in vitro' and 'in vivo'. , 1989, Biochimica et biophysica acta.

[51]  A. Parsegian,et al.  Energy of an Ion crossing a Low Dielectric Membrane: Solutions to Four Relevant Electrostatic Problems , 1969, Nature.

[52]  T. Tsong,et al.  Formation and resealing of pores of controlled sizes in human erythrocyte membrane , 1977, Nature.

[53]  J Teissié,et al.  An experimental evaluation of the critical potential difference inducing cell membrane electropermeabilization. , 1993, Biophysical journal.

[54]  L. Mir,et al.  Introduction of definite amounts of nonpermeant molecules into living cells after electropermeabilization: direct access to the cytosol. , 1988, Experimental cell research.

[55]  Raphael C. Lee,et al.  Electrical Injury Mechanisms: Electrical Breakdown of Cell Membranes , 1987, Plastic and reconstructive surgery.

[56]  J. Weaver,et al.  The number of molecules taken up by electroporated cells: quantitative determination , 1989, FEBS letters.

[57]  C. Polk,et al.  Biological effects of low-level low-frequency electric and magnetic fields , 1991 .

[58]  M. R. Tarasevich,et al.  246 - Electric breakdown of bilayer lipid membranes I. The main experimental facts and their qualitative discussion , 1979 .

[59]  D. Trichopoulos,et al.  Extremely low-frequency electric and magnetic fields and cancer , 1991, Cancer Causes & Control.

[60]  J. Gauthier,et al.  Electroporation-mediated uptake of proteins into mammalian cells. , 1990, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[61]  J. Weaver,et al.  A quantitative study of electroporation showing a plateau in net molecular transport. , 1993, Biophysical journal.

[62]  P. Mcneil,et al.  Incorporation of macromolecules into living cells. , 1989, Methods in cell biology.

[63]  James C. Weaver,et al.  Electroporation: a unified, quantitative theory of reversible electrical breakdown and mechanical rupture in artificial planar bilayer membranes☆ , 1991 .

[64]  J. Weaver,et al.  Electroporation of mammalian skin: a mechanism to enhance transdermal drug delivery. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[65]  J. Weaver,et al.  Theory of electroporation of planar bilayer membranes: predictions of the aqueous area, change in capacitance, and pore-pore separation. , 1994, Biophysical journal.

[66]  Reinhard Lipowsky,et al.  The conformation of membranes , 1991, Nature.

[67]  M. Toner,et al.  Kinetics and likelihood of membrane rupture during electroporation , 1990 .

[68]  T. Yamane,et al.  Transformation of a Methylotrophic Bacterium, Methylobacterium extorquens, with a Broad-Host-Range Plasmid by Electroporation , 1991, Annals of the New York Academy of Sciences.