Impact of external medium conductivity on cell membrane electropermeabilization by microsecond and nanosecond electric pulses

The impact of external medium conductivity on the efficiency of the reversible permeabilisation caused by pulsed electric fields was investigated. Pulses of 12 ns, 102 ns or 100 μs were investigated. Whenever permeabilisation could be detected after the delivery of one single pulse, media of lower conductivity induced more efficient reversible permeabilisation and thus independently of the medium composition. Effect of medium conductivity can however be hidden by some saturation effects, for example when pulses are cumulated (use of trains of 8 pulses) or when the detection method is not sensitive enough. This explains the contradicting results that can be found in the literature. The new data are complementary to those of one of our previous study in which an opposite effect of the conductivity was highlighted. It stresses that the conductivity of the medium influences the reversible permeabilization by several ways. Moreover, these results clearly indicate that electropermeabilisation does not linearly depend on the energy delivered to the cells.

[1]  T. Tsong,et al.  Mechanism of cell protrusion formation in electrical field: the role of actin. , 1991, Biochimica et biophysica acta.

[2]  G. Bryant,et al.  Electromechanical stresses produced in the plasma membranes of suspended cells by applied electric fields , 2005, The Journal of Membrane Biology.

[3]  Martin A Gundersen,et al.  Nanosecond electric pulse-induced calcium entry into chromaffin cells. , 2008, Bioelectrochemistry.

[4]  Clair Poignard,et al.  “Classical” Electropermeabilization Modeling at the Cell Scale , 2014, Journal of mathematical biology.

[5]  Shu Xiao,et al.  Electroporation-Induced Electrosensitization , 2011, PloS one.

[6]  Julie Gehl,et al.  Clinical aspects of electroporation , 2011 .

[7]  Hao Lin,et al.  The current-voltage relation for electropores with conductivity gradients. , 2010, Biomicrofluidics.

[8]  Shu Xiao,et al.  Manipulation of cell volume and membrane pore comparison following single cell permeabilization with 60- and 600-ns electric pulses. , 2011, Biochimica et biophysica acta.

[9]  M. Risk,et al.  Size-controlled nanopores in lipid membranes with stabilizing electric fields. , 2012, Biochemical and biophysical research communications.

[10]  Lluis M. Mir,et al.  Nanosecond-Duration Electric Pulse Delivery In Vitro and In Vivo: Experimental Considerations , 2012, IEEE Transactions on Instrumentation and Measurement.

[11]  J Teissié,et al.  Electropermeabilization of mammalian cells. Quantitative analysis of the phenomenon. , 1990, Biophysical journal.

[12]  Hao Lin,et al.  Numerical simulation of molecular uptake via electroporation. , 2011, Bioelectrochemistry.

[13]  Martin A Gundersen,et al.  Nanoelectropulse-driven membrane perturbation and small molecule permeabilization , 2006, BMC Cell Biology.

[14]  L. Mir,et al.  Nucleic Acids Electrotransfer-Based Gene Therapy (Electrogenetherapy): Past, Current, and Future , 2009, Molecular biotechnology.

[15]  Bennett L Ibey,et al.  Lipid nanopores can form a stable, ion channel-like conduction pathway in cell membrane. , 2009, Biochemical and biophysical research communications.

[16]  J Teissié,et al.  Electropermeabilization of mammalian cells to macromolecules: control by pulse duration. , 1998, Biophysical journal.

[17]  U. Zimmermann,et al.  The Effect of Electrical Deformation Forces on the Electropermeabilization of Erythrocyte Membranes in Low- and High-Conductivity Media , 1998, The Journal of Membrane Biology.

[18]  W. Krassowska,et al.  Modeling electroporation in a single cell. I. Effects Of field strength and rest potential. , 1999, Biophysical journal.

[19]  U. Zimmermann,et al.  Reversible Electropermeabilization of Mammalian Cells by High-Intensity, Ultra-Short Pulses of Submicrosecond Duration , 2001, The Journal of Membrane Biology.

[20]  J Teissié,et al.  Control by electrical parameters of short- and long-term cell death resulting from electropermeabilization of Chinese hamster ovary cells. , 1995, Biochimica et biophysica acta.

[21]  L. Mir,et al.  Optimization of a gene electrotransfer method for mesenchymal stem cell transfection , 2008, Gene Therapy.

[22]  Isabelle Leray,et al.  Demonstration of cell membrane permeabilization to medium-sized molecules caused by a single 10 ns electric pulse. , 2012, Bioelectrochemistry.

[23]  D Miklavcic,et al.  The influence of medium conductivity on electropermeabilization and survival of cells in vitro. , 2001, Bioelectrochemistry.

[24]  W. Helfrich Deformation of Lipid Bilayer Spheres by Electric Fields , 1974, Zeitschrift fur Naturforschung. Section C, Biosciences.

[25]  C. Baum,et al.  A scaling law for membrane permeabilization with nanopulses , 2009, IEEE Transactions on Dielectrics and Electrical Insulation.

[26]  Andrei G. Pakhomov,et al.  Two Modes of Cell Death Caused by Exposure to Nanosecond Pulsed Electric Field , 2013, PloS one.

[27]  L. Mir,et al.  Very high cytotoxicity of bleomycin introduced into the cytosol of cells in culture. , 1991, Biochemical pharmacology.

[28]  E. Neumann,et al.  Membrane electroporation and direct gene transfer , 1992 .

[29]  Rumiana Dimova,et al.  Electric pulses induce cylindrical deformations on giant vesicles in salt solutions. , 2006, Biophysical journal.

[30]  L. Mir,et al.  Therapeutic perspectives of in vivo cell electropermeabilization. , 2001, Bioelectrochemistry.

[31]  H. Akiyama,et al.  Different involvement of extracellular calcium in two modes of cell death induced by nanosecond pulsed electric fields. , 2014, Archives of biochemistry and biophysics.

[32]  U. Zimmermann,et al.  Effect of medium conductivity and composition on the uptake of propidium iodide into electropermeabilized myeloma cells. , 1996, Biochimica et biophysica acta.

[33]  O. Pakhomova,et al.  Multiple nanosecond electric pulses increase the number but not the size of long-lived nanopores in the cell membrane. , 2015, Biochimica et biophysica acta.

[34]  D Needham,et al.  Electro-mechanical permeabilization of lipid vesicles. Role of membrane tension and compressibility. , 1989, Biophysical journal.

[35]  Hervé Isambert,et al.  Understanding the Electroporation of Cells and Artificial Bilayer Membranes , 1998 .

[36]  L. Mir,et al.  Conducting and permeable states of cell membrane submitted to high voltage pulses: mathematical and numerical studies validated by the experiments. , 2014, Journal of theoretical biology.

[37]  M. Rols,et al.  Mechanisms of cell membrane electropermeabilization: a minireview of our present (lack of ?) knowledge. , 2005, Biochimica et biophysica acta.

[38]  L. Mir,et al.  Comparison of the effects of the repetition rate between microsecond and nanosecond pulses: electropermeabilization-induced electro-desensitization? , 2014, Biochimica et biophysica acta.

[39]  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.

[40]  Rumiana Dimova,et al.  Recent developments in the field of bending rigidity measurements on membranes. , 2014, Advances in colloid and interface science.

[41]  Antoni Ivorra,et al.  Electrical modeling of the influence of medium conductivity on electroporation. , 2010, Physical chemistry chemical physics : PCCP.

[42]  A. Haase,et al.  Resistivity of Red Blood Cells Against High-Intensity, Short-Duration Electric Field Pulses Induced by Chelating Agents , 1999, The Journal of Membrane Biology.

[43]  Winterhalter,et al.  Effect of voltage on pores in membranes. , 1987, Physical review. A, General physics.

[44]  W. Frey,et al.  Pulsed Electric Field Treatment of Microalgae—Benefits for Microalgae Biomass Processing , 2013, IEEE Transactions on Plasma Science.

[45]  Lluis M. Mir,et al.  Implementation of a broad band, high level electric field sensor in biological exposure device , 2010, 2010 IEEE International Power Modulator and High Voltage Conference.

[46]  Wolfgang Frey,et al.  Research on Industrial-Scale Electroporation Devices Fostering the Extraction of Substances from Biological Tissue , 2010 .

[47]  Isabelle Leray,et al.  Cell membrane permeabilization by 12-ns electric pulses: Not a purely dielectric, but a charge-dependent phenomenon. , 2015, Bioelectrochemistry.

[48]  W. Frey,et al.  Pulsed electric field assisted extraction of intracellular valuables from microalgae , 2013 .

[49]  Alexander Barbul,et al.  Electroendocytosis: exposure of cells to pulsed low electric fields enhances adsorption and uptake of macromolecules. , 2005, Biophysical journal.

[50]  K. Schoenbach,et al.  Membrane Permeability and Cell Survival After Nanosecond Pulsed-Electric-Field Exposure—Significance of Exposure-Media Composition , 2010, IEEE Transactions on Plasma Science.

[51]  S. Šatkauskas,et al.  The dependence of efficiency of transmembrane molecular transfer using electroporation on medium viscosity , 2015, The journal of gene medicine.