A scaling law for membrane permeabilization with nanopulses

Experimental studies of plasma membrane permeabilization, caused by single, intense, submicrosecond square wave pulses, indicate that the product of electric field amplitude and pulse duration (the electrical impulse) can be considered a similarity or scaling factor. A model based on the hypothesis that the intensity of membrane permeabilization effects is linearly dependent on the electric charge transferred through the permeabilized membrane, provides results, which are consistent with the empirical observations. For multiple pulses, bioelectric effects caused by ultrashort pulses were found to scale with the square root of the pulse number. This square root dependence on the pulse number points to a statistical motion of cells between pulses with respect to the applied electric field, and can be explained using an extension of the random walk statistical results to random rotations. Besides membrane permeabilization, the scaling law has also been shown to hold for secondary bioelectric effects, which are caused by permeability changes in the plasma membrane or subcellular membranes.

[1]  A. T. Esser,et al.  Membrane electroporation: The absolute rate equation and nanosecond time scale pore creation. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[2]  Juergen F Kolb,et al.  Membrane permeabilization and cell damage by ultrashort electric field shocks. , 2007, Archives of biochemistry and biophysics.

[3]  C. Baum,et al.  A Scaling Law for Bioelectric Effects of Nanosecond Pulses , 2008 .

[4]  K. H. Schoenbach,et al.  Effects of submicrosecond, high intensity pulsed electric fields on living cells - intracellular electromanipulation , 2003 .

[5]  K. Schoenbach,et al.  Simulations of nanopore formation and phosphatidylserine externalization in lipid membranes subjected to a high-intensity, ultrashort electric pulse. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[6]  J. Weaver,et al.  The Spatially Distributed Dynamic Transmembrane Voltage of Cells and Organelles due to 10 ns Pulses: Meshed Transport Networks , 2006, IEEE Transactions on Plasma Science.

[7]  John H Ashmore,et al.  Characterization of the cytotoxic effect of high-intensity, 10-ns duration electrical pulses , 2004, IEEE Transactions on Plasma Science.

[8]  E. Neumann,et al.  Permeability changes induced by electric impulses in vesicular membranes , 1972, The Journal of Membrane Biology.

[9]  E. Hall,et al.  Radiobiology for the radiologist , 1973 .

[10]  K. Schoenbach,et al.  Diverse effects of nanosecond pulsed electric fields on cells and tissues. , 2003, DNA and cell biology.

[11]  Qin Hu,et al.  Molecular Dynamics Analysis of High Electric Pulse Effects on Bilayer Membranes Containing DPPC and DPPS , 2006, IEEE Transactions on Plasma Science.

[12]  James C. Weaver,et al.  Electroporation of cells and tissues , 2000 .

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

[14]  James C Weaver,et al.  Active mechanisms are needed to describe cell responses to submicrosecond, megavolt-per-meter pulses: cell models for ultrashort pulses. , 2008, Biophysical journal.

[15]  E. Neumann,et al.  The Relaxation Hysteresis of Membrane Electroporation , 1989 .

[16]  Karl H. Schoenbach,et al.  Stimulation of Capacitative Calcium Entry in HL-60 Cells by Nanosecond Pulsed Electric Fields* , 2004, Journal of Biological Chemistry.

[17]  A. H. W. Nias,et al.  An introduction to radiobiology , 1990 .

[18]  R. O. Price,et al.  Plasma membrane voltage changes during nanosecond pulsed electric field exposure. , 2006, Biophysical journal.

[19]  K. Schoenbach,et al.  Nanosecond pulsed electric fields modulate cell function through intracellular signal transduction mechanisms. , 2004, Physiological measurement.

[20]  J. Reilly,et al.  Applied Bioelectricity , 1998, Springer New York.

[21]  K. Schoenbach,et al.  Intracellular effect of ultrashort electrical pulses , 2001, Bioelectromagnetics.

[22]  Laura Marcu,et al.  Ultrashort pulsed electric fields induce membrane phospholipid translocation and caspase activation: differential sensitivities of Jurkat T lymphoblasts and rat glioma C6 cells , 2003 .

[23]  K. Schoenbach,et al.  Submicrosecond intense pulsed electric field effects on intracellular free calcium: mechanisms and effects , 2004, IEEE Transactions on Plasma Science.

[24]  J. Weaver,et al.  Transport lattice approach to describing cell electroporation: use of a local asymptotic model , 2004, IEEE Transactions on Plasma Science.

[25]  Kenneth S. Cole Electric impedance of marine egg membranes , 1937 .

[26]  Shu Xiao,et al.  Bioelectric Effects of Intense Nanosecond Pulses , 2007, IEEE Transactions on Dielectrics and Electrical Insulation.

[27]  Juergen F. Kolb,et al.  Nanosecond pulsed electric fields cause melanomas to self-destruct , 2006 .

[28]  K. Schoenbach,et al.  Simulations of transient membrane behavior in cells subjected to a high-intensity ultrashort electric pulse. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[29]  R P Joshi,et al.  Improved energy model for membrane electroporation in biological cells subjected to electrical pulses. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[30]  Ravindra P. Joshi,et al.  Ultrashort electrical pulses open a new gateway into biological cells , 2004 .

[31]  L. Chernomordik,et al.  Voltage-induced nonconductive pre-pores and metastable single pores in unmodified planar lipid bilayer. , 2001, Biophysical journal.

[32]  Shu Xiao,et al.  Nanosecond pulse electric field (nanopulse): a novel non-ligand agonist for platelet activation. , 2008, Archives of biochemistry and biophysics.

[33]  Laura Marcu,et al.  Nanosecond pulsed electric fields perturb membrane phospholipids in T lymphoblasts , 2004, FEBS letters.

[34]  Martin A Gundersen,et al.  Nanopore-facilitated, voltage-driven phosphatidylserine translocation in lipid bilayers—in cells and in silico , 2006, Physical biology.

[35]  Laura Marcu,et al.  Calcium bursts induced by nanosecond electric pulses. , 2003, Biochemical and biophysical research communications.

[36]  Damijan Miklavcic,et al.  Theoretical evaluation of voltage inducement on internal membranes of biological cells exposed to electric fields. , 2006, Biophysical journal.

[37]  Michael R Murphy,et al.  Plasma membrane permeabilization by 60‐ and 600‐ns electric pulses is determined by the absorbed dose , 2009, Bioelectromagnetics.

[38]  Alan E Mark,et al.  Simulation of pore formation in lipid bilayers by mechanical stress and electric fields. , 2003, Journal of the American Chemical Society.

[39]  T. Heeren,et al.  The Effect of Intense Subnanosecond Electrical Pulses on Biological Cells , 2008, IEEE Transactions on Plasma Science.

[40]  S. Xiao,et al.  Compact, Nanosecond, High Repetition Rate, Pulse Generator for Bioelectric Studies , 2007, IEEE Transactions on Dielectrics and Electrical Insulation.

[41]  K. Schoenbach,et al.  Nanosecond, high‐intensity pulsed electric fields induce apoptosis in human cells , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[42]  K. Schoenbach,et al.  Self-consistent simulations of electroporation dynamics in biological cells subjected to ultrashort electrical pulses. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.