Electroporation for Electrochemotherapy and Gene Therapy

When a cell is exposed to an electric field, a transmembrane voltage is induced on the membrane. If this voltage exceeds a certain value, this leads to a significant increase of the electric conductivity and the permeability of the membrane. Typically, each increases by several orders of magnitude. Formation of a state of increased permeability of the membrane caused by an exposure to the electric field is called electroporation (also electropermeabilization). As the result of the increasedpermeability of themembrane,molecules that are otherwise deprived of transport mechanisms can be transported across the membrane. With appropriate duration and amplitude of the electric field, themembrane returns into its normal state after the end of the exposure to the electric field (reversible electroporation). However, if the exposure is too long or the amplitude of the electric field is too high, the membrane does not reseal after the end of the exposure, leading to cell death (irreversible electroporation). Reversible ‘‘electrical breakdown’’ of the membrane has first been reported by Stampfli in 1958, but for some time this report has been mostly unnoticed. Nearly a decade later, Sale

[1]  A. Mark,et al.  Simulation of the spontaneous aggregation of phospholipids into bilayers. , 2001, Journal of the American Chemical Society.

[2]  D Miklavcic,et al.  Tumor blood flow modifying effect of electrochemotherapy with bleomycin. , 1999, Anticancer research.

[3]  S. Szala,et al.  Electrotransfer of gene encoding endostatin into normal and neoplastic mouse tissues: Inhibition of primary tumor growth and metastatic spread , 2002, Cancer Gene Therapy.

[4]  M. Rols,et al.  Temperature effects on electrotransfection of mammalian cells. , 1994, Nucleic acids research.

[5]  ELECTRIC FIELD-INDUCED TRANSMEMBRANE POTENTIAL DEPENDS ON CELL DENSITY AND ORGANIZATION , 2004 .

[6]  L. Mir,et al.  Systemic Antitumor Effects of Electrochemotherapy Combined with Histoincompatible Cells Secreting Interleukin‐2 , 1995, Journal of immunotherapy with emphasis on tumor immunology : official journal of the Society for Biological Therapy.

[7]  L. Mir Bases and rationale of the electrochemotherapy , 2006 .

[8]  R. Orentas,et al.  Electrofusion of a weakly immunogenic neuroblastoma with dendritic cells produces a tumor vaccine. , 2001, Cellular immunology.

[9]  Damijan Miklavcic,et al.  Quantitative model of small molecules uptake after in vitro cell electropermeabilization. , 2003, Bioelectrochemistry.

[10]  H. Aihara,et al.  Gene transfer into muscle by electroporation in vivo. , 1998, Nature biotechnology.

[11]  L. Mir,et al.  Electrochemotherapy: variable anti-tumor effect on different tumor models , 1994 .

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

[13]  Damijan Miklavcic,et al.  The effect of high frequency electric pulses on muscle contractions and antitumor efficiency in vivo for a potential use in clinical electrochemotherapy. , 2005, Bioelectrochemistry.

[14]  Siewert J Marrink,et al.  Molecular dynamics simulations of hydrophilic pores in lipid bilayers. , 2004, Biophysical journal.

[15]  L. Mir,et al.  Mechanisms of in vivo DNA electrotransfer: respective contributions of cell electropermeabilization and DNA electrophoresis. , 2002, Molecular therapy : the journal of the American Society of Gene Therapy.

[16]  M. Rols,et al.  Ionic-strength modulation of electrically induced permeabilization and associated fusion of mammalian cells. , 1989, European journal of biochemistry.

[17]  D. Miklavčič,et al.  Electrochemotherapy with bleomycin. The first clinical experience in malignant melanoma patients , 1995 .

[18]  L. Cruzeiro-Hansson,et al.  Passive ion permeability of lipid membranes modelled via lipid-domain interfacial area. , 1988, Biochimica et biophysica acta.

[19]  D. Miklavcic,et al.  Effective treatment of cutaneous and subcutaneous malignant tumours by electrochemotherapy. , 1998, British Journal of Cancer.

[20]  M. Čemažar,et al.  Cytotoxicity of different platinum (II) analogues to human tumour cell lines in vitro and murine tumour in vivo alone or combined with electroporation. , 2006, Anticancer research.

[21]  E Neumann,et al.  Control by pulse parameters of electric field-mediated gene transfer in mammalian cells. , 1994, Biophysical journal.

[22]  A. Dalgleish,et al.  Human tumour and dendritic cell hybrids generated by electrofusion: potential for cancer vaccines. , 2000, Biochimica et biophysica acta.

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

[24]  M. Jaroszeski,et al.  Gene therapy with dominant-negative Stat3 suppresses growth of the murine melanoma B16 tumor in vivo. , 1999, Cancer research.

[25]  S. Orlowski,et al.  Electrochemotherapy on liver tumours in rabbits. , 1998, British Journal of Cancer.

[26]  T. Tomov Quantitative dependence of electroporation on the pulse parameters , 1995 .

[27]  G. Trinchieri,et al.  Interleukin-12 and the regulation of innate resistance and adaptive immunity , 2003, Nature Reviews Immunology.

[28]  M. Prausnitz,et al.  Electrical impedance spectroscopy for rapid and noninvasive analysis of skin electroporation. , 2000, Methods in molecular medicine.

[29]  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.

[30]  D Miklavcic,et al.  Cell membrane electropermeabilization by symmetrical bipolar rectangular pulses. Part II. Reduced electrolytic contamination. , 2001, Bioelectrochemistry.

[31]  R. Cortese,et al.  Efficient and regulated erythropoietin production by naked DNA injection and muscle electroporation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[32]  T. Tsong,et al.  Voltage-induced conductance in human erythrocyte membranes. , 1979, Biochimica et biophysica acta.

[33]  H. Itoh,et al.  Time courses of cell electroporation as revealed by submicrosecond imaging of transmembrane potential. , 1993, Biophysical journal.

[34]  D Miklavcic,et al.  Electrochemotherapy with cisplatin: clinical experience in malignant melanoma patients. , 2000, Clinical cancer research : an official journal of the American Association for Cancer Research.

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

[36]  D. V. van Bekkum,et al.  A comparison of efficacy and toxicity between electroporation and adenoviral gene transfer , 2002, BMC Molecular Biology.

[37]  Damijan Miklavčič,et al.  Time course of transmembrane voltage induced by time-varying electric fields—a method for theoretical analysis and its application , 1998 .

[38]  A E Sowers,et al.  Kinetics and mechanism of cell membrane electrofusion. , 1992, Biophysical journal.

[39]  F André,et al.  DNA electrotransfer: its principles and an updated review of its therapeutic applications , 2004, Gene therapy.

[40]  L. Mir,et al.  Electrochemotherapy with CDDP on LPB sarcoma: comparison of the anti-tumor effectiveness in immunocompotent and immunodeficient mice , 1997 .

[41]  J Teissié,et al.  Control by osmotic pressure of voltage-induced permeabilization and gene transfer in mammalian cells. , 1998, Biophysical journal.

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

[43]  M. Rols,et al.  Electrochemotherapy of cutaneous metastases in malignant melanoma , 2000, Melanoma research.

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

[45]  Shulin Li,et al.  Regression of High-Grade Malignancy in Mice by Bleomycin and Interleukin-12 Electrochemogenetherapy , 2006, Clinical Cancer Research.

[46]  Mounir Tarek,et al.  Membrane electroporation: a molecular dynamics simulation. , 2005, Biophysical journal.

[47]  D. Scherman,et al.  High-level protein secretion into blood circulation after electric pulse-mediated gene transfer into skeletal muscle. , 2000, Molecular therapy : the journal of the American Society of Gene Therapy.

[48]  H. Pauly,et al.  Über die Impedanz einer Suspension von kugelförmigen Teilchen mit einer Schale , 1959 .

[49]  M J Jaroszeski,et al.  Novel electrode designs for electrochemotherapy. , 1997, Biochimica et biophysica acta.

[50]  C. Kanthou,et al.  The endothelial cytoskeleton as a target of electroporation-based therapies , 2006, Molecular Cancer Therapeutics.

[51]  D. Scherman,et al.  Regulatable systemic production of monoclonal antibodies by in vivo muscle electroporation , 2004, Genetic vaccines and therapy.

[52]  G. Tozer,et al.  Electroporation of human microvascular endothelial cells: evidence for an anti-vascular mechanism of electrochemotherapy , 2001, British Journal of Cancer.

[53]  T. Sakata,et al.  Application of in vivo electroporation to cancer gene therapy. , 2003, Current gene therapy.

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

[55]  Damijan Miklavčič,et al.  Electric Field-Induced Transmembrane Potential Depends on Cell Density and Organizatio , 1998 .

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

[57]  A. Sanfeld,et al.  A Viscoelastic Approach to the Hydrodynamic Stability of Membranes , 1982 .

[58]  M. Jaroszeski,et al.  Treatment of B16 mouse melanoma with the combination of electropermeabilization and chemotherapy. Bioelectrochem , 1995 .

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

[60]  D Miklavcic,et al.  The effect of pulse repetition frequency on the uptake into electropermeabilized cells in vitro with possible applications in electrochemotherapy. , 2002, Bioelectrochemistry.

[61]  C. Collins,et al.  Standard operating procedures of the electrochemotherapy: Instructions for the use of bleomycin or cisplatin administered either systemically or locally and electric pulses delivered by the CliniporatorTM by means of invasive or non-invasive electrodes , 2006 .

[62]  L. Mir,et al.  [Electrochemotherapy, a new antitumor treatment: first clinical trial]. , 1991, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[63]  W. Hamilton,et al.  Effects of high electric fields on microorganisms: II. Mechanism of action of the lethal effect , 1967 .

[64]  Torben Skovsgaard,et al.  Vascular reactions to in vivo electroporation: characterization and consequences for drug and gene delivery. , 2002, Biochimica et biophysica acta.

[65]  L. Mir,et al.  Cell membrane electropermeabilization by symmetrical bipolar rectangular pulses. Part I. Increased efficiency of permeabilization. , 2001, Bioelectrochemistry.

[66]  M Cemazar,et al.  Tumour blood flow changes induced by application of electric pulses. , 1999, European journal of cancer.

[67]  D. Miklavčič,et al.  Effect of Electric-Field Intensity on Electropermeabilization and Electrosensitmty of Various Tumor-Cell Lines In Vitro , 1998 .

[68]  H. Mekid,et al.  In vivo cell electrofusion , 2000, Biochimica et Biophysica Acta (BBA) - General Subjects.

[69]  D Miklavcic,et al.  Antitumor effectiveness of electrochemotherapy with cis-diamminedichloroplatinum(II) in mice. , 1995, Cancer research.

[70]  D. H. Michael,et al.  Electrohydrodynamic instability in plane layers of fluid , 1970, Journal of Fluid Mechanics.

[71]  J. Gehl,et al.  Efficient palliation of haemorrhaging malignant melanoma skin metastases by electrochemotherapy , 2000, Melanoma research.

[72]  Franci Demsar,et al.  CONTRAST ENHANCED MRI ASSESSMENT OF TUMOR BLOOD VOLUME AFTER APPLICATION OF ELECTRIC PULSES , 1998 .

[73]  Y. Glinka,et al.  Electroporation-enhanced nonviral gene transfer for the prevention or treatment of immunological, endocrine and neoplastic diseases. , 2006, Current gene therapy.

[74]  M. Bureau,et al.  High-efficiency gene transfer into skeletal muscle mediated by electric pulses. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[75]  M Cemazar,et al.  Reduced blood flow and oxygenation in SA-1 tumours after electrochemotherapy with cisplatin , 2002, British Journal of Cancer.

[76]  O Orwar,et al.  Characterization of single-cell electroporation by using patch-clamp and fluorescence microscopy. , 2000, Biophysical journal.

[77]  D Miklavcic,et al.  A validated model of in vivo electric field distribution in tissues for electrochemotherapy and for DNA electrotransfer for gene therapy. , 2000, Biochimica et biophysica acta.

[78]  D. Chang,et al.  Cell poration and cell fusion using an oscillating electric field. , 1989, Biophysical journal.

[79]  J. Leonard,et al.  Effects of single-dose interleukin-12 exposure on interleukin-12-associated toxicity and interferon-gamma production. , 1997, Blood.

[80]  D. Miklavčič,et al.  SIGNIFICANCE OF TREATMENT ENERGY IN CELL ELECTROPERMEABILIZATION , 1998 .

[81]  J Teissié,et al.  Time courses of mammalian cell electropermeabilization observed by millisecond imaging of membrane property changes during the pulse. , 1999, Biophysical journal.

[82]  M. Shibata,et al.  Massive apoptotic cell death in chemically induced rat urinary bladder carcinomas following in situ HSVtk electrogene transfer , 2003, The journal of gene medicine.

[83]  Richard Heller,et al.  Electrochemotherapy, electrogenetherapy, and transdermal drug delivery : electrically mediated delivery of molecules to cells , 2000 .

[84]  E. Neumann,et al.  Electro-optics of membrane electroporation in diphenylhexatriene-doped lipid bilayer vesicles. , 1996, Biophysical chemistry.

[85]  J. Teissié,et al.  Cutaneous tumor treatment by electrochemotherapy : preliminary clinical results in horse sarcoids , 2001 .

[86]  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.

[87]  J. Gimsa,et al.  Analytical description of the transmembrane voltage induced on arbitrarily oriented ellipsoidal and cylindrical cells. , 2001, Biophysical journal.

[88]  M. Rols,et al.  Modulation of electrically induced permeabilization and fusion of Chinese hamster ovary cells by osmotic pressure. , 1990, Biochemistry.

[89]  D Miklavcic,et al.  Analytical description of transmembrane voltage induced by electric fields on spheroidal cells. , 2000, Biophysical journal.

[90]  J. Teissié,et al.  Electroinsertion of Glycophorin A in Interdigitation-Fusion Giant Unilamellar Lipid Vesicles* , 1997, The Journal of Biological Chemistry.

[91]  T. Tomonaga,et al.  Synergistic antitumor effect of antiangiogenic factor genes on colon 26 produced by low-voltage electroporation , 2004, Cancer Gene Therapy.

[92]  E. Tekle,et al.  Electroporation by using bipolar oscillating electric field: an improved method for DNA transfection of NIH 3T3 cells. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[93]  D. Scherman,et al.  Delivery of electric pulses for DNA electrotransfer to mouse muscle does not induce the expression of stress related genes , 2004, Cell Biology and Toxicology.

[94]  D Miklavcic,et al.  The importance of electric field distribution for effective in vivo electroporation of tissues. , 1998, Biophysical journal.

[95]  J Teissié,et al.  Electrochemotherapy of horses. A preliminary clinical report. , 2002, Bioelectrochemistry.

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

[97]  D. Miklavčič,et al.  Requirements for a clinical electrochemotherapy device-electroporator , 2005 .

[98]  Mojca Pavlin,et al.  Dependence of induced transmembrane potential on cell density, arrangement, and cell position inside a cell system , 2002, IEEE Transactions on Biomedical Engineering.

[99]  D. Miklavčič,et al.  Electrochemotherapy with cisplatin in the treatment of tumor cells resistant to cisplatin. , 1998, Anticancer research.

[100]  Xinjian Zhang,et al.  Regression of tumor growth and induction of long-term antitumor memory by interleukin 12 electro-gene therapy. , 2002, Journal of the National Cancer Institute.

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

[102]  U. Zimmermann,et al.  CD19+ B lymphocytes are the major source of human antibody-secreting hybridomas generated by electrofusion. , 2001, Journal of immunological methods.

[103]  D. Chang,et al.  High efficiency gene transfection by electroporation using a radio-frequency electric field. , 1991, Biochimica et biophysica acta.

[104]  E. Tekle,et al.  Selective and asymmetric molecular transport across electroporated cell membranes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[105]  G. Pucihar,et al.  Numerical Determination of Transmembrane Voltage Induced on Irregularly Shaped Cells , 2006, Annals of Biomedical Engineering.

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

[107]  D. Wells,et al.  Electroporation for gene transfer to skeletal muscles: current status. , 2004, BioDrugs : clinical immunotherapeutics, biopharmaceuticals and gene therapy.

[108]  Damijan Miklavčič,et al.  Biomedical applications of electric pulses with special emphasis on antitumor electrochemotherapy , 1995 .

[109]  J. Gehl,et al.  Enhancement of cytotoxicity by electropermeabilization: an improved method for screening drugs , 1998, Anti-cancer drugs.

[110]  S. Orlowski,et al.  First clinical trial of cat soft-tissue sarcomas treatment by electrochemotherapy. , 1997, British Journal of Cancer.

[111]  K. Schoenbach,et al.  The effect of pulsed electric fields on biological cells: experiments and applications , 1997 .

[112]  W. Webb,et al.  Optical imaging of cell membrane potential changes induced by applied electric fields. , 1986, Biophysical journal.

[113]  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.

[114]  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.

[115]  M. Jaroszeski,et al.  In vivo electroporation of plasmids encoding GM-CSF or interleukin-2 into existing B16 melanomas combined with electrochemotherapy induces long-term antitumour immunity , 2000, Melanoma research.

[116]  Linhong Li,et al.  Rapid, in vivo, evaluation of antiangiogenic and antineoplastic gene products by nonviral transfection of tumor cells , 2004, Cancer Gene Therapy.

[117]  J. Kuratsu,et al.  Combination electro-gene therapy using herpes virus thymidine kinase and interleukin-12 expression plasmids is highly efficient against murine carcinomas in vivo. , 2004, Molecular therapy : the journal of the American Society of Gene Therapy.

[118]  James C. Weaver,et al.  Determination of the electric field and anomalous heating caused by exponential pulses with aluminum electrodes in electroporation experiments , 1996 .

[119]  Tadej Kotnik,et al.  Sensitivity of transmembrane voltage induced by applied electric fields—A theoretical analysis , 1997 .

[120]  J Bernhardt,et al.  On the generation of potential differences across the membranes of ellipsoidal cells in an alternating electrical field , 1973, Biophysik.

[121]  J Teissié,et al.  Elimination of free-living amoebae in fresh water with pulsed electric fields. , 2002, Water research.

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

[123]  M Cemazar,et al.  Electrochemotherapy: potentiation of local antitumour effectiveness of cisplatin in dogs and cats. , 2001, Anticancer research.

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

[125]  F. Conti,et al.  Reversible electrical breakdown of squid giant axon membrane. , 1981, Biochimica et biophysica acta.

[126]  D. Miklavčič,et al.  Anti-tumor effectiveness of electrochemotherapy with bleomycin is increased by TNF-alpha on SA-1 tumors in mice. , 1997, Cancer letters.

[127]  M. Rols,et al.  In vivo electrically mediated protein and gene transfer in murine melanoma , 1998, Nature Biotechnology.

[128]  R. Heller Treatment of cutaneous nodules using electrochemotherapy. , 1995, The Journal of the Florida Medical Association.

[129]  Damijan Miklavčič,et al.  Electrochemotherapy – An easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: Results of ESOPE (European Standard Operating Procedures of Electrochemotherapy) study , 2006 .

[130]  M. Shibata,et al.  Suppression of murine mammary carcinoma growth and metastasis by HSVtk/GCV gene therapy using in vivo electroporation , 2002, Cancer Gene Therapy.

[131]  D. Miklavčič,et al.  Electrochemotherapy with bleomycin in SA‐1 tumor‐bearing mice—natural resistance and immune responsiveness , 1996, Anti-cancer drugs.

[132]  D. Miklavčič,et al.  © 1999 Cancer Research Campaign Article no. bjoc.1998.0222 , 2022 .

[133]  G. Serša,et al.  Electrochemotherapy : animal model work review. , 2000, Methods in molecular medicine.

[134]  A. Sowers Membrane electrofusion: a paradigm for study of membrane fusion mechanisms. , 1993, Methods in enzymology.

[135]  I. Sugár A theory of the electric field-induced phase transition of phospholipid bilayers. , 1979, Biochimica et biophysica acta.

[136]  V. Préat,et al.  Transdermal Delivery of Metoprolol by Electroporation , 1994, Pharmaceutical Research.

[137]  C. Nicolau,et al.  Electroinsertion of full length recombinant CD4 into red blood cell membrane. , 1990, Biochimica et biophysica acta.

[138]  D. Freyssenet,et al.  High-efficiency gene electrotransfer into skeletal muscle: description and physiological applicability of a new pulse generator. , 2002, Biochemical and biophysical research communications.

[139]  Justin Teissié,et al.  Direct monitoring of the field strength during electropulsation , 1998 .

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

[141]  L. Mir,et al.  Transient electropermeabilization of cells in culture. Increase of the cytotoxicity of anticancer drugs. , 1988, Biochemical pharmacology.

[142]  E Neumann,et al.  Mechanism of electroporative dye uptake by mouse B cells. , 1998, Biophysical journal.

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

[144]  H. Yamagishi,et al.  Electrochemo-gene therapy of cancer: intratumoral delivery of interleukin-12 gene and bleomycin synergistically induced therapeutic immunity and suppressed subcutaneous and metastatic melanomas in mice. , 2003, Molecular therapy : the journal of the American Society of Gene Therapy.

[145]  M Cemazar,et al.  Improvement of combined modality therapy with cisplatin and radiation using electroporation of tumors. , 2000, International journal of radiation oncology, biology, physics.

[146]  J. Leonard,et al.  Effects of Single-Dose Interleukin-12 Exposure on Interleukin-12–Associated Toxicity and Interferon-γ Production , 1997 .