Simulation of nanoparticle based enhancement of cellular electroporation for biomedical applications

Introduction of nanoparticles can modify electrical properties such as the permittivity and conductivity of a medium. This model based study focuses on such modulated changes of an extracellular medium from the standpoint of enhancing electroporation to achieve more efficient delivery into biological cells. A finite element, time-dependent axisymmetric bio-model, coupled with the Smoluchowski equation, has been used to evaluate the transmembrane potentials and evolution of pore densities. Our simulation results show that a relatively small fraction of gold nanoparticles in the extracellular medium effectively enhances the transmembrane potentials, leads to much higher pore densities, and shifts the pore distribution towards larger radii. This collectively bodes well for enhancing drug delivery or gene transfection in cells.

[1]  G. Navarro,et al.  In vivo targeted gene delivery by cationic nanoparticles for treatment of hepatocellular carcinoma , 2009, The journal of gene medicine.

[2]  B. Persson,et al.  Optical properties of small metallic particles in a continuous dielectric medium , 1983 .

[3]  D. Miklavčič,et al.  Chapter Seven Electroporation of Planar Lipid Bilayers and Membranes , 2008 .

[4]  J. Gehl,et al.  Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. , 2003, Acta physiologica Scandinavica.

[5]  Shengnian Wang,et al.  Micronozzle array enhanced sandwich electroporation of embryonic stem cells. , 2010, Analytical chemistry.

[6]  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.

[7]  Luke P. Lee,et al.  A single cell electroporation chip. , 2005, Lab on a chip.

[8]  J. Lekner Electroporation in cancer therapy without insertion of electrodes , 2014, Physics in medicine and biology.

[9]  Daniela O. H. Suzuki,et al.  Theoretical and Experimental Analysis of Electroporated Membrane Conductance in Cell Suspension , 2011, IEEE Transactions on Biomedical Engineering.

[10]  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.

[11]  T. Geng,et al.  Flow-through electroporation based on constant voltage for large-volume transfection of cells. , 2010, Journal of controlled release : official journal of the Controlled Release Society.

[12]  K. Schoenbach,et al.  Simulations of intracellular calcium release dynamics in response to a high-intensity, ultrashort electric pulse. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[13]  Chad A Mirkin,et al.  Spherical nucleic acids. , 2012, Journal of the American Chemical Society.

[14]  Bo Yu,et al.  Nanochannel electroporation delivers precise amounts of biomolecules into living cells. , 2011, Nature nanotechnology.

[15]  W. Mark Saltzman,et al.  Enhancement of transfection by physical concentration of DNA at the cell surface , 2000, Nature Biotechnology.

[16]  Ravindra P. Joshi,et al.  Synergistic effects of local temperature enhancements on cellular responses in the context of high-intensity, ultrashort electric pulses , 2011, Medical & Biological Engineering & Computing.

[17]  Vincent M Rotello,et al.  Gold nanoparticles in delivery applications. , 2008, Advanced drug delivery reviews.

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

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

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

[21]  R. J. Lee,et al.  Targeted drug delivery via the folate receptor. , 2000, Advanced drug delivery reviews.

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

[23]  C. Yao,et al.  Simulation study of delivery of subnanosecond pulses to biological tissues with an impulse radiating antenna , 2014, Bioelectromagnetics.

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

[25]  K. Schoenbach,et al.  Modeling studies of cell response to ultrashort, high-intensity electric fields-implications for intracellular manipulation , 2004, IEEE Transactions on Plasma Science.

[26]  Keunchang Cho,et al.  A multi-channel electroporation microchip for gene transfection in mammalian cells. , 2007, Biosensors & bioelectronics.

[27]  S. W. Kim,et al.  Women and heart disease--physiologic regulation of gene delivery and expression: bioreducible polymers and ischemia-inducible gene therapies for the treatment of ischemic heart disease. , 2009, Advanced Drug Delivery Reviews.

[28]  A. Cuschieri,et al.  BNNT-Mediated Irreversible Electroporation: Its Potential on Cancer Cells , 2012, Technology in cancer research & treatment.

[29]  A. Cuschieri,et al.  Carbon nanotube-enhanced cell electropermeabilisation. , 2010, Bioelectrochemistry.

[30]  A. Irimajiri,et al.  A dielectric theory of "multi-stratified shell" model with its application to a lymphoma cell. , 1979, Journal of theoretical biology.

[31]  K. Schoenbach,et al.  Bioelectric effects of intense ultrashort pulses. , 2010, Critical reviews in biomedical engineering.

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

[33]  J. Yeow,et al.  Cell electroporation by CNT-featured microfluidic chip. , 2013, Lab on a chip.

[34]  Qiao Jiang,et al.  Enhanced gene delivery and siRNA silencing by gold nanoparticles coated with charge-reversal polyelectrolyte. , 2010, ACS nano.

[35]  W. Monroe,et al.  Silver nanoscale antisense drug delivery system for photoactivated gene silencing. , 2013, ACS nano.

[36]  Salvatore Torquato,et al.  Effective conductivity of periodic arrays of spheres with interfacial resistance , 1997, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[37]  Ravindra P. Joshi,et al.  Ultrashort electrical pulses open a new gateway into biological cells , 2004, Proceedings of the IEEE.

[38]  Koji Asami,et al.  Characterization of biological cells by dielectric spectroscopy , 2002 .

[39]  J. Weaver,et al.  Theory of electroporation: A review , 1996 .

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

[41]  Benjamin S. Goldschmidt,et al.  Gold nanoparticle mediated detection of prostate cancer cells using photoacoustic flowmetry with optical reflectance. , 2010, Journal of biomedical nanotechnology.

[42]  The Development of Electroporation , 2002, Science.

[43]  E. Neumann,et al.  Electroporation and Electrofusion in Cell Biology , 1989, Springer US.

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

[45]  Juergen F Kolb,et al.  Leukemic cell intracellular responses to nanosecond electric fields. , 2004, Biochemical and biophysical research communications.

[46]  M. Giersig,et al.  Multi-walled carbon nanotubes for plasmid delivery into Escherichia coli cells. , 2005, Lab on a chip.

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

[48]  Carbon nanotubes for voltage reduction and throughput enhancement of electrical cell lysis on a lab-on-a-chip. , 2011, Nanotechnology.

[49]  Shu Xiao,et al.  Subnanosecond Electric Pulses Cause Membrane Permeabilization and Cell Death , 2011, IEEE Transactions on Biomedical Engineering.

[50]  Shengnian Wang,et al.  Gold nanoparticles enhanced electroporation for mammalian cell transfection. , 2014, Journal of biomedical nanotechnology.

[51]  Richard O. Williams,et al.  Plasmid DNA as a safe gene delivery vehicle for treatment of chronic inflammatory disease , 2008, Expert opinion on biological therapy.

[52]  Weixiong Wang,et al.  Semicontinuous flow electroporation chip for high-throughput transfection on mammalian cells. , 2009, Analytical chemistry.

[53]  Damijan Miklavcic,et al.  A Time-Dependent Numerical Model of Transmembrane Voltage Inducement and Electroporation of Irregularly Shaped Cells , 2009, IEEE Transactions on Biomedical Engineering.

[54]  G. A. Hofmann,et al.  Electroporation therapy: a new approach for the treatment of head and neck cancer , 1999, IEEE Transactions on Biomedical Engineering.

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

[56]  David R. McKenzie,et al.  The conductivity of lattices of spheres - II. The body centred and face centred cubic lattices , 1978, Proceedings of the Royal Society of London. A. Mathematical and Physical Sciences.

[57]  Maria R. Gumina,et al.  Interaction between carbon nanotubes and mammalian cells: characterization by flow cytometry and application , 2008, Nanotechnology.

[58]  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.

[59]  Pierre Van Rysselberghe,et al.  Remarks concerning the Clausius-Mossotti Law , 1931 .

[60]  Doyle,et al.  Effective cluster model of dielectric enhancement in metal-insulator composites. , 1990, Physical review. B, Condensed matter.

[61]  Enhanced Introduction of Gold Nanoparticles into Vital Acidothiobacillus ferrooxidans by Carbon Nanotube-based Microwave Electroporation , 2004 .

[62]  K. Schoenbach,et al.  Mechanism for membrane electroporation irreversibility under high-intensity, ultrashort electrical pulse conditions. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[63]  Ravindra P. Joshi,et al.  Dynamical modeling of cellular response to short-duration, high-intensity electric fields , 2003 .

[64]  Mojca Pavlin,et al.  Effective conductivity of a suspension of permeabilized cells: a theoretical analysis. , 2003, Biophysical journal.

[65]  James C Weaver,et al.  Three dimensional transport lattice model for describing action potentials in axons stimulated by external electrodes. , 2006, Bioelectrochemistry.

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

[67]  G. A. Hofmann,et al.  Medical applications of electroporation , 2000 .

[68]  Cell manipulation and tissue engineering at the nanoscale , 2005 .

[69]  Achim Goepferich,et al.  Layer-by-layer assembled gold nanoparticles for siRNA delivery. , 2009, Nano letters.

[70]  R. Jaenisch,et al.  Microfluidic Control of Cell Pairing and Fusion , 2009, Nature Methods.