Theory and in vivo application of electroporative gene delivery

Molecular Therapy

Volumn 2, Issue 3, 2000, Pages 178-187

  Somiari, Stella ^a   Glasspool Malone, Jill ^a   Drabick, Joseph J ^b   Gilbert, Richard A ^c   Heller, Richard ^c   Jaroszeski, Mark J ^c   Malone, Robert W ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b WALTER REED ARMY MEDICAL CENTER   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA;

ELECTROPORATION; GENETIC TRANSFECTION; METHODOLOGY; PLASMID; REVIEW; TRANSGENE;

ELECTROPORATION; PLASMIDS; TRANSFECTION; TRANSGENES;

EID: 0034268548     PISSN: 15250016     EISSN: None     Source Type: Journal    
DOI: 10.1006/mthe.2000.0124     Document Type: Review

References (90)

1. Malone, R. W. (1999). Present and future status of gene therapy. In Advanced Gene Delivery (A. Rolland, Ed.). Harwood Academic Press.
2. Coster, H. G. A. (1965). Quantitative analysis of the voltage-current relationships of fixed charge membranes and the associated property of "punch-through." Biophys. J. 5: 669-686.
3. Sale, A. J., and Hamilton, W. A. (1967). Effects of high electric fields on micro-organisms. 1. Killing of bacteria and yeasts. Biochim. Biophys. Acta 148: 781-788.
4. Sale, A. J., and Hamilton, W. A. (1968). Effects of high electric fields on micro-organisms. 3. Lysis of erythrocytes and protoplasts. Biochim. Biophys. Acta 163: 37-43.
5. Neumann, E., Schaefer-Ridder, M., Wang, Y., and Hofschneider, P. H. (1982). Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J. 1: 841-845.
6. Potter, H., Weir, L., and Leder, P. (1984). Enhancer-dependent expression of human kappa immunoglobulin genes introduced into mouse pre-B lymphocytes by electroporation. Proc. Natl. Acad. Sci. USA 81: 7161-7165.
7. Fromm, M., Taylor, L. P., and Walbot, V. (1985). Expression of genes transferred into monocot and dicot plant cells by electroporation. Proc. Natl. Acad. Sci. USA 82: 5824-5828.
8. Toneguzzo, F., and Keating, A. (1986). Stable expression of selectable genes introduced into human hematopoietic stem cells by electric field-mediated DNA transfer. Proc. Natl. Acad. Sci. USA 83: 3496-3499.
9. Tur-Kaspa, R., Teicher, L., Levine, B. J., Skoultchi, A. I., and Shafritz, D. A. (1986). Use of electroporation to introduce biologically active foreign genes into primary rat hepatocytes. Mol. Cell Biol. 6: 716-718.
10. Dower, W. J., Miller, J. F., and Ragsdale, C. W. (1988). High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 16: 6127-6145.
11. Fiedler, S., and Wirth, R. (1988). Transformation of bacteria with plasmid DNA by electroporation. Anal. Biochem. 170: 38-44.
12. Taketo, A. (1988). DNA transfection of Escherichia coli by electroporation. Biochim. Biophys. Acta 949: 318-324.
13. Heller, R., Gilbert, R., and Jaroszeski, M. J. (1999). In vivo gene delivery. Adv. Drug Deliv. Rev. 35: 131-137.
14. Foung, S. K., and Perkins, S. (1989). Electric field-induced cell fusion and human monoclonal antibodies. J. Immunol. Methods 116: 117-122.
15. Heller, R., and Grasso, R. J. (1989). Transfer of human membrane surface components by incorporating human cells into intact animal tissue by cell-tissue electrofusion in vivo. Biochim. Biophys. Acta 1024: 185-188.
16. Jaroszeski, M. J., Gilbert, R., Fallon, P. G., and Heller, R. (1994). Mechanically facilitated cell-cell electrofusion. Biophys. J. 67: 1574-1581.
17. Zheng, Q. A., and Chang, D. C. (1991). High-efficiency gene transfection by in situ electroporation of cultured cells. Biochim. Biophys. Acta 1088: 104-110.
18. Sukharev, S. I., Klenchin, V. A., Serov, S. M., Chernomordik, L. V., and Chizmadzhev, Y. A. (1992). Electroporation and electrophoretic DNA transfer into cells. The effect of DNA interaction with electropores. Biophys. J. 63: 1320-1327.
19. Gehl, J., and Mir, L. M. (1999). Determination of optimal parameters for in vivo gene transfer by electroporation, using a rapid in vivo test for cell permeabilization. Biochem. Biophys. Res. Commun. 261: 377-380.
20. Gehl, J., et al. (1999). In vivo electroporation of skeletal muscle: Threshold, efficacy and relation to electric field distribution. Biochim. Biophys. Acta 1428: 233-240.
21. Mathiesen, I. (1999). Electropermeabilization of skeletal muscle enhances gene transfer in vivo. Gene Ther. 6: 508-514.
22. Suzuki, T., Shin, B. C., Fujikura, K., Matsuzaki, T., and Takata, K. (1998). Direct gene transfer into rat liver cells by in vivo electroporation. FEBS Lett. 423: 436-440.
23. Mir, L. M., Bureau, M. F., Rangara, R., Schwartz, B., and Scherman, D. (1998). Long-term, high level in vivo gene expression after electric pulse-mediated gene transfer into skeletal muscle. Crit. Rev. Acad. Sci. III 321: 893-899.
24. Titomirov, A. V., Sukharev, S., and Kistanova, E. (1991). In vivo electroporation and stable transformation of skin cells of newborn mice by plasmid DNA. Biochim. Biophys. Acta 1088: 131-134.
25. Zhang, L., Li, L., Hoffmann, G. A., and Hoffman, R. M. (1996). Depth-targeted efficient gene delivery and expression in the skin by pulsed electric fields: An approach to gene therapy of skin aging and other diseases. Biochem. Biophys. Res. Commun. 220: 633-636.
26. Heller, R., et al. (1996). In vivo gene electroinjection and expression in rat liver. FEBS Lett. 389: 225-228.
27. Nishi, T., et al. (1996). High-efficiency in vivo gene transfer using intraarterial plasmid DNA injection following in vivo electroporation. Cancer Res. 56: 1050-1055.
28. Gaylor, D. C., Prakah-Asante, K., and Lee, R. C. (1988). Significance of cell size and tissue structure in electrical trauma. J. Theor. Biol. 133: 223-237.
29. Neumann, E., Kakorin, S., and Toensing, K. (1999). Fundamentals of electroporative delivery of drugs and genes. Bioelectrochem. Bioenerg. 48: 3-16.
30. Weaver, J. C., and Chimadzev, Y. A. (1996). Theory of electroporation: A review. Bioelectrochem. Bioenerg. 41: 135-160.
31. Teissie, J., and Rols, M. P. (1992). Time course of electropermeabilization. In Charge and Field Effects in Biosystems-3 (M. J. Allen, S. F. Cleary, A. E. Sowers, and D. Shillady, Eds.). Birkhauser Press, Boston.
32. Vanbever, R., Leroy, M. A., and Preat, V. (1998). Transdermal permeation of neutral molecules by skin electroporation. J. Controlled Release 54: 243-250.
33. Johnson, P. G., Gallo, S. A., Hui, S. W., and Oseroff, A. R. (1998). A pulsed electric field enhances cutaneous delivery of methylene blue in excised full-thickness porcine skin. J. Invest. Dermatol. 111: 457-463.
34. Neumann, E., Kakorin, S., Tsoneva, I., Nikolova, B., and Tomov, T. (1996). Calcium-mediated DNA adsorption to yeast cells and kinetics of cell transformation by electroporation. Biophys. J. 71: 868-877.
35. Neumann, E., Sowers, A. E., and Jordan, C. A. (1989). Electroporation and Electrofusion in Cell Biology. Plenum Press, New York.
36. Calvin, N. M., and Hanawalt, P. C. (1988). High-efficiency transformation of bacterial cells by electroporation. J. Bacteriol. 170: 2796-2801.
37. Rols, M. P., and Teissie, J. (1990). Electropermeabilization of mammalian cells. Quantitative analysis of the phenomenon. Biophys. J. 58: 1089-1098.
38. Belehradek, J. J., Orlowski, S., Ramirez, L. H., Pron, G., Poddevin, B., and Mir, L. M. (1994). Electropermeabilization of cells in tissues assessed by the qualitative and quantitative electroloading of bleomycin. Biochim. Biophys. Acta 1190: 155-163.
39. Fear, E. C., and Stuchly, M. A. (1998). Biological cells with gap junctions in low-frequency electric fields. IEEE Trans. Biomed. Eng. 45: 856-866.
40. Gilbert, R. A., Jaroszeski, M. J., and Heller, R. (1997). Novel electrode designs for electrochemotherapy. Biochim. Biophys. Acta 1334: 9-14.
41. Jaroszeski, M. J., and Gilbert, R. (1999). In vivo gene delivery by electroporation. Adv. Drug Deliv. 35: 131-137.
42. Heller, R., et al. (1998). Treatment of cutaneous and subcutaneous tumors with electrochemotherapy using intralesional bleomycin. Cancer 83: 148-157.
43. Heller, R., Gilber, R., and Jaroszeski, M. (2000). Clinical trials for solid tumors using electrochemotherapy. In Electrochemotherapy, Electrogenetherapy, and Transdermal Delivery by Electroporaiton, pp. 137-156. Humana Press, Totowa, NJ.
44. Reiss, M., Jastreboff, M. M., Bertino, J. R., and Narayanan, R. (1986). DNA-mediated gene transfer into epidermal cells using electroporation. Biochem. Biophys. Res. Commun. 137: 244-249.
45. Muramatsu, T., and Park, H. M. (1997). In vivo electroporation: A new physical method for transferring genes to animal cells. Exp. Med. 15: 265-268. [in Japanese]
46. Muramatsu, T., Nakamura, A., and Park, H. M. (1998). In vivo electroporation: A powerful and convenient means of nonviral gene transfer to tissues of living animals. Int. J. Mol. Med. 1: 55-62.
47. Vicat, J. M., et al. (2000). Muscle transfection by electroporation with high-voltage and short-pulse currents provides high-level and long-lasting gene expression. Hum. Gene Ther. 11: 909-916.
48. Wolff, J. A., et al. (1990). Direct gene transfer into mouse muscle in vivo. Science 247: 1465-1468.
49. Lin, H., Parmacek, M. S., Morle, G., Boiling, S., and Leiden, J. M. (1990). Expression of recombinant genes in myocardium in vivo after direct injection of DNA. Circulation 82: 2217-2221.
50. Acsadi, G., et al. (1991). Direct gene transfer and expression into rat heart in vivo. New Biol. 3: 71-81.
51. Kitsis, R. N., Buttrick, P. M., McNally, E. M., Kaplan, M. L., and Leinwand, L. A. (1991). Hormonal modulation of a gene injected into rat heart in vivo. Proc. Natl. Acad. Sci. USA 88: 4138-4142.
52. von Harsdorf, R., Schott, R. J., Shen, Y. T., Vatner, S. F., Mahdavi, V., and Nadal-Ginard, B. (1993). Gene injection into canine myocardium as a useful model for studying gene expression in the heart of large mammals. Circ. Res. 72: 688-695.
53. Sikes, M. L., O'Malley, B. W. J., Finegold, M. J., and Ledley, F. D. (1994). In vivo gene transfer into rabbit thyroid follicular cells by direct DNA injection. Hum. Gene Ther. 5: 837-844.
54. Yang, J. P., and Huang, L. (1996). Direct gene transfer to mouse melanoma by intra-tumor injection of free DNA. Gene Ther. 3: 542-548.
55. Li, H., Bartlett, R. J., Pastori, R., Kenyon, N. S., Ricord, C., and Alejandro, R. (1997). Gene expression via direct injection of plasmid vector into the thymus. Transplant. Proc. 29: 2220.
56. Hengge, U. R., Walker, P. S., and Vogel, J. C. (1996). Expression of naked DNA in human, pig, and mouse skin. J. Clin. Invest. 97: 2911-2916.
57. Hickman, M. A., et al. (1994). Gene expression following direct injection of DNA into liver. Hum. Gene Ther. 5: 1477-1483.
58. Zhang, G., Vargo, D., Budker, V., Armstrong, N., Knechtle, S., and Wolff, J. A. (1997). Expression of naked plasmid DNA injected into the afferent and efferent vessels of rodent and dog livers. Hum. Gene Ther. 8: 1763-1772.
59. Wolff, J. A., et al. (1992). Expression of naked plasmids by cultured myotubes and entry of plasmids into T tubules and caveolae of mammalian skeletal muscle. J. Cell Sci. 103: 1249-1259.
60. Liu, F., Song, Y., and Liu, D. (1999). Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 6: 1258-1266.
61. Somiari, S., et al. (2000). Increased transfection efficiency of cutaneous transfection using in vivo electroporation in murine and porcine models. In Sub-cutaneous Gene Therapy (L. Taichman, Ed.). Natcher Conference Center, National Institutes of Health, Washington, DC.
62. Aihara, H., and Miyazaki, J. (1998). Gene transfer into muscle by electroporation in vivo. Nat. Biotechnol. 16: 867-870.
63. Rizzuto, G., et al. (1999). Efficient and regulated erythropoietin production by naked DNA injection and muscle electroporation. Proc. Natl. Acad. Sci. USA 96: 6417-6422.
64. Regnier, V., De Morre, N., Jadoul, A., and Preat, V. (1999). Mechanisms of a phosphorothioate oligonucleotide delivery by skin electroporation. Int. J. Pharm. 184: 147-156.
65. Pliquett, U. F., and Gusbeth, C. A. (2000). Perturbation of human skin due to application of high voltage. Bioelectrochemistry 51: 41-51.
66. Heller, R., Gilbert, R., and Jaroszeski, M. J. (1997). Electrochemotherapy: An emerging drug delivery method for the treatment of cancer. Adv. Drug Deliv. Rev. 26: 185-197.
67. Omura, S., Tsuyuki, Y., Ohta, S., Bukawa, H., and Fujita, K. (1999). In vivo antitumor effects of electrochemotherapy in a tongue cancer model. J. Oral Maxillofac. Surg. 57: 965-972.
68. Belehradek, M., Domenge, C., Luboinski, B., Orlowski, S., Belehradek, J. J., and Mir, L. M. (1993). Electrochemotherapy, a new antitumor treatment. First clinical phase I-II trial. Cancer 72: 3694-3700.
69. Dev, S. B., and Hoffman, G. A. (1995). Clinical applications of electroporation. In The Electrical Manipulation of Cells (P. T. Lynch and M. R. Davey, Eds.). Chapman and Hall, New York.
70. Malone, R. W., et al. (1994). Dexamethasone enhancement of gene expression after direct hepatic DNA injection. J. Biol. Chem. 269: 29903-29907.
71. Sato, Y., et al. (1996). Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science 273: 352-354.
72. Roman, M., et al. (1997). Immunostimulatory DNA sequences function as T helper-1-promoting adjuvants. Nat. Med. 3: 849-854.
73. Tsan, M. F., Tacy, N. J., Lindau-Shepard, B. A., and White, J. E. (1997). Protection of rats against oxygen toxicity by tracheal administration of plasmid DNA: Role of endogenous tumor necrosis factor. Proc. Assoc. Am. Physicians 109: 409-419.
74. Vakeva, A. P., Agah, A., Rollins, S. A., Matis, L. A., Li, L., and Stahl, G. L. (1998). Myocardial infarction and apoptosis after myocardial ischemia and reperfusion: Role of the terminal complement components and inhibition by anti-C5 therapy. Circulation 97: 2259-2267.
75. Kirklin, J. K., and McGiffin, D. C. (1999). Control of the inflammatory response in extended myocardial preservation of the donor heart. Ann. Thorac. Surg. 68: 1978-1982.
76. Lehmann, T. G., Koeppel, T. A., Kirschfink, M., Gebhard, M. M., Herfarth, C., Otto, G., and Post, S. (1998). Complement inhibition by soluble complement receptor type 1 improves microcirculation after rat liver transplantation. Transplantation 66: 717-722.
77. Evans, M. J., et al. (1995). In vivo and in vivo inhibition of complement activity by a single-chain Fv fragment recognizing human C5. Mol. Immunol. 32: 1183-1195.
78. Hyers, T. M., Tricomi, S. M., and Liao, J. J. (1992). Inhibition of some human neutrophil functions by the cyclooxygenase inhibitor ketorolac tromethamine. J. Leukocyte Biol. 51: 490-495.
79. Yao, K. A., Roth, A. C., Stephenson, L. L., Suchy, H., and Zamboni, W. A. (1998). Effect of ketorolac tromethamine (Toradol) on ischemia-reperfusion injury in skeletal muscle. J. Reconstr. Microsurg. 14: 211-214.
80. Meyer, K. B., Thompson, M. M., Levy, M. Y., Barron, L. G., and Szoka, F. C. J. (1995). Intratracheal gene delivery to the mouse airway: Characterization of plasmid DNA expression and pharmacokinetics. Gene Ther. 2: 450-460.
81. Rother, R. P., Squinto, S. P., Mason, J. M., and Rollins, S. A. (1995). Protection of retroviral vector particles in human blood through complement inhibition. Hum. Gene Ther. 6: 429-435.
82. Kuriyama, S., et al. (1998). Inhibitory effects of human sera on adenovirus-mediated gene transfer into rat liver. Anticancer Res. 18: 2345-2351.
83. Zelphati, O., Uyechi, L. S., Barron, L. G., and Szoka, F. C. J. (1998). Effect of serum components on the physico-chemical properties of cationic lipid/oligonucleotide complexes and on their interactions with cells. Biochim. Biophys. Acta 1390: 119-133.
84. Zhang, H. G., et al. (1998). Induction of specific T-cell tolerance by adenovirus-transfected, Fas ligand-producing antigen presenting cells. Nat. Biotechnol. 16: 1045-1049.
85. Widera, G., et al. (2000). Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J. Immunol. 164: 4635-4640.
86. Mir, L. M., et al. (1999). High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc. Natl. Acad. Sci. USA 96: 4262-4267.
87. Lazarides, E., and Lindberg, U. (1974). Actin is the naturally occurring inhibitor of deoxyribonuclease I. Proc. Natl. Acad. Sci. USA 71: 4742-4746.
88. Hallick, R. B., Chelm, B. K., Gray, P. W., and Orozco, E. M., Jr. (1977). Use of aurin tricarboxylic acid as an inhibitor of nucleases during nucleic acid isolation. Nucleic Acids Res. 4: 3055-3064.
89. Glasspool-Malone, J., and Malone, R. W. (1999). Marked enhancement of direct respiratory tissue transfection by aurintricarboxylic acid. Hum. Gene Ther. 10: 1703-1713.
90. Rols, M. P., Delteil, C., Golzio, M., Dumond, P., Cros, S., and Teissie, J. (1998). In vivo electrically mediated protein and gene transfer in murine melanoma. Nat. Biotechnol. 16: 168-171.