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Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research

J. Gehl

Department of Oncology, Herlev Hospital in University of Copenhagen, Herlev, Denmark

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First published: 21 March 2003
Cited by: 370
J. Gehl, Department of Oncology 54B1, Herlev Hospital in University of Copenhagen, Herlev Ringvej 75, 2730 Herlev, Denmark.

Abstract

Electroporation designates the use of short high‐voltage pulses to overcome the barrier of the cell membrane. By applying an external electric field, which just surpasses the capacitance of the cell membrane, transient and reversible breakdown of the membrane can be induced. This transient, permeabilized state can be used to load cells with a variety of different molecules, either through simple diffusion in the case of small molecules, or through electrophoretically driven processes allowing passage through the destabilized membrane – as is the case for DNA transfer. Initially developed for gene transfer, electroporation is now in use for delivery of a large variety of molecules: From ions to drugs, dyes, tracers, antibodies, and oligonucleotides to RNA and DNA. Electroporation has proven useful both in vitro, in vivo and in patients, where drug delivery to malignant tumours has been performed. Whereas initial electroporation procedures caused considerable cell damage, developments over the past decades have led to sophistication of equipment and optimization of protocols. The electroporation procedures used in many laboratories could be optimized with limited effort. This review (i) outlines the theory of electroporation, (ii) discusses factors of importance for optimization of electroporation protocols for mammalian cells, (iii) addresses particular concerns when using electroporation in vivo, e.g. effects on blood flow and considerations regarding choice of electrodes, (iv) describes DNA electrotransfer with emphasis on use in the in vivo setting, and (v) sums up data on safety and efficacy of electroporation used to enhance delivery of chemotherapy to tumours in cancer patients.

Number of times cited: 370

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  • , Quantification of propidium iodide delivery using millisecond electric pulses: Experiments, Biochimica et Biophysica Acta (BBA) - Biomembranes, 1828, 4, (1322), (2013).
  • , Myocardial Gene Transfer: Routes and Devices for Regulation of Transgene Expression by Modulation of Cellular Permeability, Human Gene Therapy, 10.1089/hum.2012.241, 24, 4, (375-392), (2013).
  • , Long-lasting response to electrochemotherapy in melanoma patients with cutaneous metastasis, BMC Cancer, 13, 1, (2013).
  • , Suppression of persistent atrial fibrillation by genetic knockdown of caspase 3: a pre-clinical pilot study, European Heart Journal, 34, 2, (147), (2013).
  • , Suppression of epileptiform activity by a single short-duration electric field in rat hippocampus in vitro, Journal of Neurophysiology, 109, 11, (2720), (2013).
  • , Advances in siRNA delivery to T-cells: potential clinical applications for inflammatory disease, cancer and infection, Biochemical Journal, 10.1042/BJ20130950, 455, 2, (133-147), (2013).
  • , High-density distributed electrode network, a multi-functional electroporation method for delivery of molecules of different sizes, Scientific Reports, 3, 1, (2013).
  • , Cyanines in photodynamic reaction assisted by reversible electroporation—in vitro study on human breast carcinoma cells, Photodiagnosis and Photodynamic Therapy, 10, 4, (490), (2013).
  • , Micro-/nanofluidics based cell electroporation, Biomicrofluidics, 7, 1, (011301), (2013).
  • , Supramolecular design of biocompatible nanocontainers based on amphiphilic derivatives of a natural compound isosteviol, Physical Chemistry Chemical Physics, 15, 39, (16725), (2013).
  • , Bacteria tracking by in vivo magnetic resonance imaging, BMC Biology, 11, 1, (63), (2013).
  • , Multiparametric functional nuclear magnetic resonance imaging shows alterations associated with plasmid electrotransfer in mouse skeletal muscle, The Journal of Gene Medicine, 14, 9-10, (598-608), (2012).
  • , Optically absorbing nanoparticle mediated cell membrane permeabilization, Optics Letters, 37, 21, (4474), (2012).
  • , Review of micro/nano technologies and theories for electroporation of biological cells, Science China Physics, Mechanics and Astronomy, 55, 6, (996), (2012).
  • , Electrochemotherapy for Non-Melanoma Head and Neck Cancers, Annals of Surgery, 255, 6, (1158), (2012).
  • , Physically facilitating drug-delivery systems, Therapeutic Delivery, 3, 1, (125), (2012).
  • , Calcium influx determines the muscular response to electrotransfer, American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 302, 4, (R446), (2012).
  • , Electrochemotherapy of chest wall breast cancer recurrence, Cancer Treatment Reviews, 38, 5, (379), (2012).
  • , High-Throughput Transfection of Differentiated Primary Neurons from Rat Forebrain, Journal of Biomolecular Screening, 17, 5, (692), (2012).
  • , Novel methods for renal tissue ablation, Current Opinion in Urology, 22, 5, (379), (2012).
  • , Single Nanosecond Pulsed Electric Field Effects on Embryonic Development of the Medaka Fish, IEEE Transactions on Plasma Science, 40, 10, (2379), (2012).
  • , What you always needed to know about electroporation based DNA vaccines, Human Vaccines & Immunotherapeutics, 8, 11, (1694), (2012).
  • , Spatial Distribution of Transgenic Protein After Gene Electrotransfer to Porcine Muscle, Human Gene Therapy Methods, 23, 6, (387), (2012).
  • , INFLUENCE OF CELLULAR PROPERTIES ON THE ELECTRIC FIELD DISTRIBUTION AROUND A SINGLE CELL, Progress In Electromagnetics Research B, 39, (141), (2012).
  • , Serum interleukin-6 as a prognostic biomarker in patients with metastatic melanoma, Melanoma Research, 22, 4, (287), (2012).
  • , Genetic suppression of atrial fibrillation using a dominant-negative ether-a-go-go–related gene mutant, Heart Rhythm, 9, 2, (265), (2012).
  • , Cellular microinjection for therapeutic and research applications, Mems for Biomedical Applications, 10.1533/9780857096272.4.432, (432-448), (2012).
  • , Cell Death Induced by Subnanosecond Pulsed Electric Fields at Elevated Temperatures, IEEE Transactions on Plasma Science, 10.1109/TPS.2012.2208202, 40, 10, (2334-2347), (2012).
  • , Interactions of a Hydrophobically Modified Polycation with Zwitterionic Lipid Membranes, Langmuir, 28, 1, (676), (2012).
  • , The Capacitance and Electromechanical Coupling of Lipid Membranes Close to Transitions: The Effect of Electrostriction, Biophysical Journal, 103, 5, (918), (2012).
  • , Size of the pores created by an electric pulse: Microsecond vs millisecond pulses, Biochimica et Biophysica Acta (BBA) - Biomembranes, 1818, 12, (3032), (2012).
  • , Droplet electroporation in microfluidics for efficient cell transformation with or without cell wall removal, Lab on a Chip, 12, 21, (4483), (2012).
  • , Electroporation for Medical Use in Drug and Gene Electrotransfer, Advances in Electrochemical Science and Engineering, (369-388), (2012).
  • , Variable electric fields for high throughput electroporation protocol design in curvilinear coordinates, Biotechnology and Bioengineering, 109, 8, (2168-2171), (2012).
  • , Comparing ion conductance recordings of synthetic lipid bilayers with cell membranes containing TRP channels, Biochimica et Biophysica Acta (BBA) - Biomembranes, 1818, 5, (1123), (2012).
  • , Treatment planning of electroporation-based medical interventions: electrochemotherapy, gene electrotransfer and irreversible electroporation, Physics in Medicine and Biology, 10.1088/0031-9155/57/17/5425, 57, 17, (5425-5440), (2012).
  • , Electro-manipulation of biological cells in microdevices, IEEE Transactions on Dielectrics and Electrical Insulation, 19, 4, (1261), (2012).
  • , Utility of electrochemotherapy in melanoma treatment, Current Opinion in Oncology, 24, 2, (155), (2012).
  • , Numerical simulation of molecular uptake via electroporation, Bioelectrochemistry, 82, 1, (10), (2011).
  • , Second Harmonic Generation for time-resolved monitoring of membrane pore dynamics subserving electroporation of neurons, Biomedical Optics Express, 2, 2, (305), (2011).
  • , Calcium Electrotransfer for Termination of Transgene Expression in Muscle, Human Gene Therapy, 22, 6, (753), (2011).
  • , Management of cutaneous metastases using electrochemotherapy, Acta Oncologica, 50, 5, (621), (2011).
  • , Identification of In Vitro Electropermeabilization Equivalent Pulse Protocols, Technology in Cancer Research & Treatment, 10, 5, (465), (2011).
  • , Comparison of electroporation and Chariot™ for delivery of β-galactosidase into mammalian cells: strategies to use trehalose in cell preservation, In Vitro Cellular & Developmental Biology - Animal, 47, 3, (195), (2011).
  • , The Actin Cytoskeleton Has an Active Role in the Electrotransfer of Plasmid DNA in Mammalian Cells, Molecular Therapy, 10.1038/mt.2010.303, 19, 5, (913-921), (2011).
  • , Gene Delivery Using Physical Methods, Challenges in Delivery of Therapeutic Genomics and Proteomics, 10.1016/B978-0-12-384964-9.00003-7, (83-126), (2011).
  • , Improved electroporation parameters of delivering silver nanoparticles into living C666 cells for surface-enhanced Raman scattering, Journal of Physics: Conference Series, 277, (012045), (2011).
  • , Distinguishing splanchnic nerve and chromaffin cell stimulation in mouse adrenal slices with fast-scan cyclic voltammetry, American Journal of Physiology-Cell Physiology, 300, 1, (C49), (2011).
  • , Efficiency of Cellular Delivery of Antisense Peptide Nucleic Acid by Electroporation Depends on Charge and Electroporation Geometry, Oligonucleotides, 21, 1, (29), (2011).
  • , Targeted Gene-and-host Progenitor Cell Therapy for Nonunion Bone Fracture Repair, Molecular Therapy, 19, 1, (53), (2011).
  • , Vesicle deformation and poration under strong dc electric fields, Physical Review E, 83, 6, (2011).
  • , Minimum Energy Path to Membrane Pore Formation and Rupture, Physical Review Letters, 106, 16, (2011).
  • , Enhancement of electric field-mediated gene delivery through pretreatment of tumors with a hyperosmotic mannitol solution, Cancer Gene Therapy, 18, 1, (26), (2011).
  • , Dynamics and control of the two-pulse protocol in electroporation: Numerical exploration, Mathematical Biosciences, 232, 1, (24), (2011).
  • , Electro-gene transfer to skin using a noninvasive multielectrode array, Journal of Controlled Release, 151, 3, (256), (2011).
  • 2011 33rd Annual International Conference of the IEEE Engineering in Medicine and Biology Society Boston, MA 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE , (2011). 978-1-4577-1589-1 978-1-4244-4121-1 978-1-4244-4122-8 Electrochemotherapy of solid tumors — Preclinical and clinical experience , (2011). 728 731 6090165 , 10.1109/IEMBS.2011.6090165 http://ieeexplore.ieee.org/document/6090165/
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  • , Electro‐mediated gene transfer and expression are controlled by the life‐time of DNA/membrane complex formation, The Journal of Gene Medicine, 12, 1, (117-125), (2009).
  • , Electrochemotherapy for cutaneous and subcutaneous tumor lesions: a novel therapeutic approach, Dermatologic Therapy, 23, 6, (651-661), (2010).
  • , Green fluorescent protein as indicator of nonviral transient transfection efficiency in endometrial and testicular biopsies, Microscopy Research and Technique, 73, 3, (229-233), (2009).
  • , Simultaneous detection of intracellular target and off‐target binding of small molecule cancer drugs at nanomolar concentrations, British Journal of Pharmacology, 160, 4, (958-970), (2010).
  • , Bleomycin/interleukin-12 electrochemogene therapy for treating naturally occurring spontaneous neoplasms in dogs, Cancer Gene Therapy, 17, 7, (457), (2010).
  • , Direct assay of electropermeabilization in a 2D pseudo tissue, Physical Chemistry Chemical Physics, 12, 44, (14670), (2010).
  • , Effect of Mg ions on efficiency of gene electrotransfer and on cell electropermeabilization, Bioelectrochemistry, 10.1016/j.bioelechem.2010.04.001, 79, 2, (265-271), (2010).
  • , Electrochemotherapy is highly effective for the treatment of canine perianal hepatoid adenoma and epithelioma, Acta veterinaria, 60, 2-3, (285), (2010).
  • , Control of pore radius regulation for electroporation-based drug delivery, Communications in Nonlinear Science and Numerical Simulation, 15, 5, (1400), (2010).
  • , Use of SiRNA Oligonucleotides to Study Gene Function, RNA Interference, (50-75), (2010).
  • , Preclinical Analysis of Irreversible Electroporation on Rat Liver Tissues Using a Microfabricated Electroporator, Tissue Engineering Part C: Methods, 10.1089/ten.tec.2009.0803, 16, 6, (1245-1253), (2010).
  • 2010 5th IEEE International Conference on Nano/Micro Engineered and Molecular Systems (NEMS 2010) Xiamen 2010 IEEE 5th International Conference on Nano/Micro Engineered and Molecular Systems IEEE , (2010). 978-1-4244-6543-9 Theoretical and experimental study of electroporation of red blood cells using MEMS technology , (2010). 595 598 5592472 , 10.1109/NEMS.2010.5592472 http://ieeexplore.ieee.org/document/5592472/
  • , Efficient, specific and targeted delivery of genes to the lung, Therapeutic Delivery, 10.4155/tde.10.11, 1, 1, (133-148), (2010).
  • , Electrochemotherapy of Mouse Sarcoma Tumors Using Electric Pulse Trains with Repetition Frequencies of 1 Hz and 5 kHz, The Journal of Membrane Biology, 236, 1, (155), (2010).
  • , Comparison of red blood cell membrane microstructure after different physicochemical influences: Atomic force microscope research, Journal of Critical Care, 25, 3, (539.e1), (2010).
  • , Improved numerical approach for electrical modeling of biological cell clusters, Medical & Biological Engineering & Computing, 48, 4, (311), (2010).
  • , Data-Driven Feedforward Control for Electroporation Mediated Gene Delivery in Gene Therapy, IEEE Transactions on Control Systems Technology, 18, 4, (935), (2010).
  • , Bleomycin/interleukin-12 electrochemogenetherapy for treating naturally occurring spontaneous neoplasms in dogs, Cancer Gene Therapy, 17, 8, (571), (2010).
  • , Conformation dependence of DNA electrophoretic mobility in a converging channel, ELECTROPHORESIS, 31, 16, (2813-2821), (2010).
  • , Electroporation based on hydrodynamic focusing of microfluidics with low dc voltage, Biomedical Microdevices, 12, 1, (35), (2010).
  • , The current-voltage relation for electropores with conductivity gradients, Biomicrofluidics, 4, 1, (013206), (2010).
  • , Comparison and Optimisation of Transfection of Human Dental Follicle Cells, a Novel Source of Stem Cells, with Different Chemical Methods and Electro-poration, Neurochemical Research, 10.1007/s11064-008-9905-4, 34, 7, (1272-1277), (2009).
  • , A 3D in vitro spheroid model as a way to study the mechanisms of electroporation, International Journal of Pharmaceutics, 379, 2, (278), (2009).
  • , Rapid and efficient cell labeling with a MRI contrast agent by electroporation in the presence of protamine sulfate, Nanomedicine, 4, 3, (305), (2009).
  • , Electric pulses used in electrochemotherapy and electrogene therapy do not significantly change the expression profile of genes involved in the development of cancer in malignant melanoma cells, BMC Cancer, 9, 1, (2009).
  • , Changes of the Electrode Surface Roughness Induced by High-Voltage Electric Pulses as Revealed by AFM, Acta Physica Polonica A, 115, 6, (1095), (2009).
  • , On-chip testing device for electrochemotherapeutic effects on human breast cells, Biomedical Microdevices, 11, 1, (151), (2009).
  • , Electrochemotherapy as an adjunct or alternative to other treatments for unresectable or in-transit melanoma, Expert Review of Anticancer Therapy, 10.1586/era.09.129, 9, 11, (1611-1630), (2014).
  • , Targeted gene delivery to the lung, Expert Opinion on Drug Delivery, 10.1517/17425240902927841, 6, 6, (567-583), (2009).
  • , Design of Multifunctional Nanomedical Systems, Annals of Biomedical Engineering, 37, 10, (2048), (2009).
  • , Comparison of Electroporation Threshold for Different Cell Lines in vitro, Acta Physica Polonica A, 115, 6, (1056), (2009).
  • , Erythrocyte Membrane Surface after Calibrated Electroporation: Visualization by Atomic Force Microscopy, Bulletin of Experimental Biology and Medicine, 148, 3, (455), (2009).
  • , Selective Enhancement of the Uptake and Bioactivity of a TAT-conjugated Peptide Inhibitor of Glycogen Synthase Kinase-3, Molecular Therapy, 10.1038/mt.2008.271, 17, 3, (500-507), (2009).
  • , Prostate Stem Cell Antigen DNA Vaccination Breaks Tolerance to Self-antigen and Inhibits Prostate Cancer Growth, Molecular Therapy, 10.1038/mt.2009.66, 17, 6, (1101-1108), (2009).
  • , What is (Still not) Known of the Mechanism by Which Electroporation Mediates Gene Transfer and Expression in Cells and Tissues, Molecular Biotechnology, 41, 3, (286), (2009).
  • , Modification of Schwann cell gene expression by electroporation in vivo, Journal of Neuroscience Methods, 176, 2, (96), (2009).
  • , Nanotechnology approaches for gene transfer, Genetica, 137, 1, (47), (2009).
  • , Focal macromolecule delivery in neuronal tissue using simultaneous pressure ejection and local electroporation, Journal of Neuroscience Methods, 177, 2, (273), (2009).
  • , GENE THERAPY, Pharmacology and Therapeutics, 10.1016/B978-1-4160-3291-5.50097-4, (1295-1316), (2009).
  • , Dynamics Modeling and Control of Electroporation-Mediated Gene Delivery, IEEE Transactions on Automation Science and Engineering, 6, 2, (228), (2009).
  • , Non invasive contact electrodes for in vivo localized cutaneous electropulsation and associated drug and nucleic acid delivery, Journal of Controlled Release, 134, 2, (125), (2009).
  • , Transgene expression of human PON1 Q in mice protected the liver against CCl4‐induced injury, The Journal of Gene Medicine, 10, 1, (94-100), (2007).
  • , Field distribution and DNA transport in solid tumors during electric field‐mediated gene delivery, Journal of Pharmaceutical Sciences, 97, 2, (691-711), (2007).
  • , Single‐cell microinjection technology in cell biology, BioEssays, 30, 6, (606-610), (2008).
  • , QUANTITATIVE EVALUATIONS OF MECHANISMS OF RADIOFREQUENCY INTERACTIONS WITH BIOLOGICAL MOLECULES AND PROCESSES, Health Physics, 95, 4, (365), (2008).
  • , PTD-mediated Loading of Tumor-Seeking Lymphocytes with Prodrug-Activating Enzymes, The AAPS Journal, 10, 4, (614), (2008).
  • , Guiding light in nanomedicine, IEEE Nanotechnology Magazine, 2, 1, (19), (2008).
  • , Non-viral gene transfection technologies for genetic engineering of stem cells, European Journal of Pharmaceutics and Biopharmaceutics, 10.1016/j.ejpb.2007.04.021, 68, 1, (90-104), (2008).
  • , Functional Expression of Ion Channels in Mammalian Systems, Protein Science Encyclopedia, (79-109), (2008).
  • , Gene transfer device utilizing micron-spiked electrodes produced by the self-organization phenomenon of Fe-alloy, Lab on a Chip, 8, 7, (1104), (2008).
  • , Electrode commutation sequence for honeycomb arrangement of electrodes in electrochemotherapy and corresponding electric field distribution, Bioelectrochemistry, 74, 1, (26), (2008).
  • , Electrochemotherapy: An emerging cancer treatment, International Journal of Hyperthermia, 24, 3, (263), (2008).
  • , Emerging Technologies and Fourth Generation Issues in Cartilage Repair, Sports Medicine and Arthroscopy Review, 10.1097/JSA.0b013e31818d56b3, 16, 4, (246-254), (2008).
  • , Chapter Seven Electroporation of Planar Lipid Bilayers and Membranes, , 10.1016/S1554-4516(07)06007-3, (165-226), (2008).
  • , Kinetics of Transmembrane Transport of Small Molecules into Electropermeabilized Cells, Biophysical Journal, 95, 6, (2837), (2008).
  • , Ultrasound-based nonviral gene delivery induces bone formation in vivo, Gene Therapy, 15, 4, (257), (2008).
  • , Membrane Electroporation and Emerging Biomedical Applications, Handbook of Membrane Separations, 10.1201/9781420009484.ch26, (741-758), (2009).
  • , Microinjection as a tool of mechanical delivery, Current Opinion in Biotechnology, 19, 5, (506), (2008).
  • , In Situ Bipolar Electroporation for Localized Cell Loading with Reporter Dyes and Investigating Gap Junctional Coupling, Biophysical Journal, 94, 2, (469), (2008).
  • , Microfluidic based single cell microinjection, Lab on a Chip, 8, 8, (1258), (2008).
  • , Shear‐induced intracellular loading of cells with molecules by controlled microfluidics, Biotechnology and Bioengineering, 99, 4, (846-854), (2007).
  • , DNA vaccines against infectious agents: recent strategies for enhancing immune responses, Expert Opinion on Therapeutic Patents, 18, 4, (365), (2008).
  • , ZAP-70 Restoration in Mice by In Vivo Thymic Electroporation, PLoS ONE, 3, 4, (e2059), (2008).
  • , Space and time-resolved gene expression experiments on cultured mammalian cells by a single-cell electroporation microarray, New Biotechnology, 25, 1, (55), (2008).
  • , Nucleofection Is a Valuable Transfection Method for Transient and Stable Transgene Expression in Adipose Tissue‐Derived Stem Cells, STEM CELLS, 25, 3, (790-797), (2006).
  • , Numerical Assessment of Thermal Response Associated With In Vivo Skin Electroporation: The Importance of the Composite Skin model, Journal of Biomechanical Engineering, 129, 3, (330), (2007).
  • , Irreversible Electroporation in Medicine, Technology in Cancer Research & Treatment, 6, 4, (255), (2007).
  • , Methods for genetic modification of megakaryocytes and platelets, Platelets, 10.1080/09537100701288012, 18, 6, (393-408), (2009).
  • , Sine-wave Current for Efficient and Safe In Vivo Gene Transfer, Molecular Therapy, 10.1038/sj.mt.6300261, 15, 10, (1842-1847), (2007).
  • , Methods of optimization of electrical impedance tomography for imaging tissue electroporation, Physiological Measurement, 28, 10, (1135), (2007).
  • , Irreversible Electroporation: A New Ablation Modality — Clinical Implications, Technology in Cancer Research & Treatment, 6, 1, (37), (2007).
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  • , The effect of the histological properties of tumors on transfection efficiency of electrically assisted gene delivery to solid tumors in mice, Gene Therapy, 14, 17, (1261), (2007).
  • , Numerical Calculations of Single-Cell Electroporation with an Electrolyte-Filled Capillary, Biophysical Journal, 92, 10, (3696), (2007).
  • , Sensitive and precise regulation of haemoglobin after gene transfer of erythropoietin to muscle tissue using electroporation, Gene Therapy, 14, 12, (950), (2007).
  • , Probing Cellular Mechanical Responses to Stimuli Using Ballistic Intracellular Nanorheology, Cell Mechanics, 10.1016/S0091-679X(07)83006-8, (113-140), (2007).
  • , Electric field-mediated transport of plasmid DNA in tumor interstitium in vivo, Bioelectrochemistry, 71, 2, (233), (2007).
  • , Increase of the roughness of the stainless-steel anode surface due to the exposure to high-voltage electric pulses as revealed by atomic force microscopy, Bioelectrochemistry, 70, 2, (519), (2007).
  • , Efficacy of Farabloc as an analgesic in primary fibromyalgia, Clinical Rheumatology, 26, 3, (405), (2007).
  • , Ultrastructural modifications of cell membranes induced by “electroporation” on melanoma xenografts, Microscopy Research and Technique, 70, 12, (1041), (2007).
  • , Design of an Irreversible Electroporation System for Clinical Use, Technology in Cancer Research & Treatment, 6, 4, (313), (2007).
  • 2007 IEEE/ICME International Conference on Complex Medical Engineering Beijing, China 2007 IEEE/ICME International Conference on Complex Medical Engineering IEEE , (2007). 978-1-4244-1077-4 978-1-4244-1078-1 The Study on the Treatment of Mice Inoculated S-180 with Electrochemotherapy , (2007). 495 498 4381784 , 10.1109/ICCME.2007.4381784 http://ieeexplore.ieee.org/document/4381784/
  • , Thermal damage reduction associated with in vivo skin electroporation: A numerical investigation justifying aggressive pre-cooling, International Journal of Heat and Mass Transfer, 50, 1-2, (105), (2007).
  • , Nucleofection Is the Most Efficient Nonviral Transfection Method for Neuronal Stem Cells Derived from Ventral Mesencephali with No Changes in Cell Composition or Dopaminergic Fate, STEM CELLS, 24, 12, (2776-2791), (2006).
  • , Magnetic Resonance Imaging of Changes in Muscle Tissues after Membrane Trauma, Annals of the New York Academy of Sciences, 1066, 1, (272-285), (2006).
  • 9th AIAA/ASME Joint Thermophysics and Heat Transfer Conference San Francisco, California 9th AIAA/ASME Joint Thermophysics and Heat Transfer Conference American Institute of Aeronautics and Astronautics Reston, Virigina , (2006). , (2012). 978-1-62410-044-4 10.2514/MJTHT06 , 10.2514/MJTHT06 2016101707080100819 http://arc.aiaa.org/doi/book/10.2514/MJTHT06 The Importance od the Composite Skin Model in Numerical Investigations of the Thermal Response Associated with In Vivo Skin Electroporation , (2006). , (2012). 10.2514/6.2006-2939 , 10.2514/6.2006-2939 2016101707080100819 http://arc.aiaa.org/doi/10.2514/6.2006-2939
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  • , Optimization of an electroporation protocol using the K562 cell line as a model: role of cell cycle phase and cytoplasmic DNAses, Cytotechnology, 51, 3, (141), (2006).
  • , Vaccination for Treatment and Prevention of Cancer in Animal Models, Cancer Immunotherapy, 10.1016/S0065-2776(06)90005-4, (175-213), (2006).
  • , On the Effect of Prestin on the Electrical Breakdown of Cell Membranes, Biophysical Journal, 10.1529/biophysj.105.064105, 90, 3, (967-974), (2006).
  • 2006 IEEE International Symposium on MicroNanoMechanical and Human Science Nagoya University, Nagoya, Japan 2006 IEEE International Symposium on MicroNanoMechanical and Human Science IEEE , (2006). 1-4244-0717-6 Novel Gene Transduction Procedures in vivo Using the Epstein-Barr Virus-based Artificial Chromosomes , (2006). 1 6 4110329 , 10.1109/MHS.2006.320318 http://ieeexplore.ieee.org/document/4110329/
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  • , Electroporation of Human Embryonic Stem Cells: Small and Macromolecule Loading and DNA Transfection, Biotechnology Progress, 22, 3, (825-834), (2008).
  • , Effect of the intracellular localization of a Gd‐based imaging probe on the relaxation enhancement of water protons, Magnetic Resonance in Medicine, 55, 3, (491-497), (2006).
  • , Successful parallel development and integration of a plasmid-based biologic, container/closure system and electrokinetic delivery device, Vaccine, 24, 21, (4607), (2006).
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  • , Measurement and correlation of acoustic cavitation with cellular bioeffects, Ultrasound in Medicine & Biology, 32, 7, (1111), (2006).
  • , Ex ovo electroporation for gene transfer into older chicken embryos, Developmental Dynamics, 233, 4, (1470-1477), (2005).
  • , Enhanced biotransformations and product recovery in a membrane bioreactor through application of a direct electric current, Biotechnology and Bioengineering, 89, 1, (18-23), (2004).
  • , Gene delivery to embryonic stem cells, Birth Defects Research Part C: Embryo Today: Reviews, 75, 1, (10-18), (2005).
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  • , In vivo NMR imaging evaluation of efficiency and toxicity of gene electrotransfer in rat muscle, Gene Therapy, 12, 19, (1434), (2005).
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  • , Successful sphincter-saving treatment of anorectal malignant melanoma with electrochemotherapy, local excision and adjuvant brachytherapy, Anti-Cancer Drugs, 16, 3, (345), (2005).
  • , Inactivation and Activity of Cholesterol-Dependent Cytolysins: What Structural Studies Tell Us, Structure, 13, 8, (1097), (2005).
  • , Gene Therapy for Type 1 Diabetes, American Journal of Therapeutics, 10.1097/01.mjt.0000178774.39149.2d, 12, 6, (512-528), (2005).
  • , Transient Transfection of Porcine Granulosa Cells after 3D Culture in Barium Alginate Capsules, International Journal of Immunopathology and Pharmacology, 18, 4, (677), (2005).
  • , Anti-HER-2 DNA vaccine protects Syrian hamsters against squamous cell carcinomas, British Journal of Cancer, 10.1038/sj.bjc.6602853, 93, 11, (1250-1256), (2005).
  • , Electric Field‐Induced Cell Membrane Permeabilization and Gene Transfer: Theory and Experiments, Engineering in Life Sciences, 5, 2, (179-186), (2005).
  • , Electroendocytosis: Exposure of Cells to Pulsed Low Electric Fields Enhances Adsorption and Uptake of Macromolecules, Biophysical Journal, 88, 3, (2206), (2005).
  • , Cost efficient and effective gene transfer into the human natural killer cell line, NK92, Journal of Immunological Methods, 296, 1-2, (31), (2005).
  • , Numerical Modeling of In Vivo Plate Electroporation Thermal Dose Assessment, Journal of Biomechanical Engineering, 128, 1, (76), (2005).
  • , Electrode Microchamber for Noninvasive Perturbation of Mammalian Cells With Nanosecond Pulsed Electric Fields, IEEE Transactions on Nanobioscience, 4, 4, (277), (2005).
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