Plasmid DNA gene therapy by electroporation: Principles and recent advances

Current Gene Therapy

Volumn 11, Issue 6, 2011, Pages 447-456

  Murakami, Tatsufumi ^a   Sunada, Yoshihide ^a  

^a KAWASAKI MEDICAL SCHOOL   (Japan)

Author keywords

DNA vaccine; Electro gene therapy; Electroporation; Heart; Plasmid DNA; Skeletal muscles; Skin

Indexed keywords

BETA GALACTOSIDASE; CYTOKINE; DNA VACCINE; DYSTROPHIN; ERYTHROPOIETIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GLUCAGON LIKE PEPTIDE 1; GRANULOCYTE COLONY STIMULATING FACTOR; GROWTH HORMONE; GROWTH HORMONE RELEASING FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN G1; INTERLEUKIN 12; INTERLEUKIN 27; KERATINOCYTE GROWTH FACTOR; PLACENTAL GROWTH FACTOR; PLASMID DNA; SCATTER FACTOR; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RECEPTOR; VASCULOTROPIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GENE THERAPY; CANCER IMMUNOTHERAPY; CORNEA; DIABETES MELLITUS; DNA IMMUNIZATION; DRUG TOLERABILITY; ELECTROPHORESIS; ELECTROPORATION; GENE EXPRESSION; GENE GUN; GROWTH HORMONE DEFICIENCY; HEART; HEPATITIS C; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOGENICITY; INFLUENZA; KIDNEY; LIVER; LUNG; MELANOMA; MEMBRANE PERMEABILITY; MUSCULAR DYSTROPHY; NEOPLASM; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; OSTEOARTHROPATHY; PAPILLOMAVIRUS INFECTION; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PROSTATE CANCER; RESPIRATORY TRACT DISEASE; SKELETAL MUSCLE; SKIN; SOLID TUMOR; WOUND HEALING;

ANIMALS; BIOLISTICS; ELECTROPORATION; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; KIDNEY; LIVER; LUNG; MALE; MELANOMA; MUSCLE, SKELETAL; PLASMIDS; PROSTATIC NEOPLASMS; SKIN; VACCINES, DNA;

EID: 82055208192     PISSN: 15665232     EISSN: 18755631     Source Type: Journal    
DOI: 10.2174/156652311798192860     Document Type: Article

References (126)

1. Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J 1982; 1(7): 841-5.
2. Mir LM, Orlowski S, Belehradek J, Jr., Paoletti C. Electrochemotherapy potentiation of antitumour effect of bleomycin by local electric pulses. Eur J Cancer 1991; 27(1): 68-72.
3. Okino M, Mohri H. Effects of a high-voltage electrical impulse and an anticancer drug on in vivo growing tumors. Jpn J Cancer Res 1987; 78(12): 1319-21.
4. Titomirov AV, Sukharev S, Kistanova E. In vivo electroporation and stable transformation of skin cells of newborn mice by plasmid DNA. Biochim Biophys Acta 1991; 1088(1): 131-4.
5. Heller R, Jaroszeski M, Atkin A, et al. In vivo gene electroinjection and expression in rat liver. FEBS Lett 1996; 389(3): 225-8.
6. Suzuki T, Shin BC, Fujikura K, Matsuzaki T, Takata K. Direct gene transfer into rat liver cells by in vivo electroporation. FEBS Lett 1998; 425(3): 436-40.
7. Nishi T, Yoshizato K, Yamashiro S, et al. High-efficiency in vivo gene transfer using intraarterial plasmid DNA injection following in vivo electroporation. Cancer Res 1996; 56(5): 1050-5.
8. Muramatsu T, Shibata O, Ryoki S, Ohmori Y, Okumura J. Foreign gene expression in the mouse testis by localized in vivo gene transfer. Biochem Biophys Res Commun 1997; 233(1): 45-9.
9. Muramatsu T, Mizutani Y, Ohmori Y, Okumura J. Comparison of three nonviral transfection methods for foreign gene expression in early chicken embryos in ovo. Biochem Biophys Res Commun 1997; 230(2): 376-80.
10. Oshima Y, Sakamoto T, Yamanaka I, et al. Targeted gene transfer to corneal endothelium in vivo by electric pulse. Gene Ther 1998; 5(10): 1347-54.
11. Aihara H, Miyazaki J. Gene transfer into muscle by electroporation in vivo. Nat Biotechnol 1998; 16(9): 867-70.
12. Rols MP, Delteil C, Golzio M, et al. In vivo electrically mediated protein and gene transfer in murine melanoma. Nat Biotechnol 1998; 16(2): 168-71.
13. Tsujie M, Isaka Y, Nakamura H, Imai E, Hori M. Electroporationmediated gene transfer that targets glomeruli. J Am Soc Nephrol 2001; 12(5): 949-54.
14. Ohashi S, Kubo T, Kishida T, et al. Successful genetic transduction in vivo into synovium by means of electroporation. Biochem Biophys Res Commun 2002; 293(5): 1530-5.
15. Matsumoto T, Komori K, Shoji T, et al. Successful and optimized in vivo gene transfer to rabbit carotid artery mediated by electronic pulse. Gene Ther 2001; 8(15): 1174-9.
16. Dean DA. Electroporation of the vasculature and the lung. DNA Cell Biol 2003; 22(12): 797-806.
17. Dean DA, Machado-Aranda D, Blair-Parks K, Yeldandi AV, Young JL. Electroporation as a method for high-level nonviral gene transfer to the lung. Gene Ther 2003; 10(18): 1608-15.
18. De Vry J, Martinez-Martinez P, Losen M, et al. In vivo electroporation of the central nervous system: a non-viral approach for targeted gene delivery. Prog Neurobiol 2010; 92(3): 227-44.
19. Escoffre JM, Portet T, Wasungu L, Teissie J, Dean D, Rols MP. What is (still not) known of the mechanism by which electroporation mediates gene transfer and expression in cells and tissues. Mol Biotechnol 2009; 41(3): 286-95.
20. Satkauskas S, Bureau MF, Puc M, et al. Mechanisms of in vivo DNA electrotransfer: respective contributions of cell electropermeabilization and DNA electrophoresis. Mol Ther 2002; 5(2): 133-40.
21. Zaharoff DA, Henshaw JW, Mossop B, Yuan F. Mechanistic analysis of electroporation-induced cellular uptake of macromolecules. Exp Biol Med (Maywood) 2008; 233(1): 94-105.
22. Antov Y, Barbul A, Mantsur H, Korenstein R. Electroendocytosis: exposure of cells to pulsed low electric fields enhances adsorption and uptake of macromolecules. Biophys J 2005; 88(3): 2206-23.
23. Hojman P. Basic principles and clinical advancements of muscle electrotransfer. Curr Gene Ther 2010; 10(2): 128-38.
24. Andre FM, Gehl J, Sersa G, et al. Efficiency of high- and lowvoltage pulse combinations for gene electrotransfer in muscle, liver, tumor, and skin. Hum Gene Ther 2008; 19(11): 1261-71.
25. Bureau MF, Gehl J, Deleuze V, Mir LM, Scherman D. Importance of association between permeabilization and electrophoretic forces for intramuscular DNA electrotransfer. Biochim Biophys Acta 2000; 1474(3): 353-9.
26. Mir LM. Nucleic acids electrotransfer-based gene therapy (electrogenetherapy): past, current, and future. Mol Biotechnol 2009; 43(2): 167-76.
27. Golzio M, Teissie J, Rols MP. Direct visualization at the single-cell level of electrically mediated gene delivery. Proc Natl Acad Sci USA 2002; 99(3): 1292-7.
28. Mignet N, Vandermeulen G, Pembouong G, et al. Cationic and anionic lipoplexes inhibit gene transfection by electroporation in vivo. J Gene Med 2010; 12(6): 491-500.
29. Faurie C, Rebersek M, Golzio M, et al. Electro-mediated gene transfer and expression are controlled by the life-time of DNA/membrane complex formation. J Gene Med 2010; 12(1): 117-25.
30. Vaughan EE, Dean DA. Intracellular trafficking of plasmids during transfection is mediated by microtubules. Mol Ther 2006; 13(2): 422-8.
31. Young JL, Zimmer WE, Dean DA. Smooth muscle-specific gene delivery in the vasculature based on restriction of DNA nuclear import. Exp Biol Med (Maywood) 2008; 233(7): 840-8.
32. Degiulio JV, Kaufman CD, Dean DA. The SP-C promoter facilitates alveolar type II epithelial cell-specific plasmid nuclear import and gene expression. Gene Ther 2010; 17(4): 541-9.
33. Wang Z, Troilo PJ, Wang X, et al. Detection of integration of plasmid DNA into host genomic DNA following intramuscular injection and electroporation. Gene Ther 2004; 11(8): 711-21.
34. Tjelle TE, Salte R, Mathiesen I, Kjeken R. A novel electroporation device for gene delivery in large animals and humans. Vaccine 2006; 24(21): 4667-70.
35. Heller R, Cruz Y, Heller LC, Gilbert RA, Jaroszeski MJ. Electrically mediated delivery of plasmid DNA to the skin, using a multielectrode array. Hum Gene Ther 2010; 21(3): 357-62.
36. Bettan M, Emmanuel F, Darteil R, et al. High-level protein secretion into blood circulation after electric pulse-mediated gene transfer into skeletal muscle. Mol Ther 2000; 2(3): 204-10.
37. Murakami T, Nishi T, Kimura E, et al. Full-length dystrophin cDNA transfer into skeletal muscle of adult mdx mice by electroporation. Muscle Nerve 2003; 27(2): 237-41.
38. Bureau MF, Naimi S, Torero Ibad R, et al. Intramuscular plasmid DNA electrotransfer: biodistribution and degradation. Biochim Biophys Acta 2004; 1676(2): 138-48.
39. Corovic S, Zupanic A, Kranjc S, et al. The influence of skeletal muscle anisotropy on electroporation: in vivo study and numerical modeling. Med Biol Eng Comput 2010; 48(7): 637-48.
40. Trollet C, Scherman D, Bigey P. Delivery of DNA into muscle for treating systemic diseases: advantages and challenges. Methods Mol Biol 2008; 423: 199-214.
41. Mir LM, Bureau MF, Gehl J, et al. High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc Natl Acad Sci U S A 1999; 96(8): 4262-7.
42. Muramatsu T, Arakawa S, Fukazawa K, et al. In vivo gene electroporation in skeletal muscle with special reference to the duration of gene expression. Int J Mol Med 2001; 7(1): 37-42.
43. Tone CM, Cardoza DM, Carpenter RH, Draghia-Akli R. Long-term effects of plasmid-mediated growth hormone releasing hormone in dogs. Cancer Gene Ther 2004; 11(5): 389-96.
44. Peng B, Zhao Y, Lu H, Pang W, Xu Y. In vivo plasmid DNA electroporation resulted in transfection of satellite cells and lasting transgene expression in regenerated muscle fibers. Biochem Biophys Res Commun 2005; 338(3): 1490-8.
45. Arruda VR, Hagstrom JN, Deitch J, et al. Posttranslational modifications of recombinant myotube-synthesized human factor IX. Blood 2001; 97(1): 130-8.
46. Gothelf A, Gehl J. Gene electrotransfer to skin; review of existing literature and clinical perspectives. Curr Gene Ther 2010; 10(4): 287-99.
47. Zhang L, Nolan E, Kreitschitz S, Rabussay DP. Enhanced delivery of naked DNA to the skin by non-invasive in vivo electroporation. Biochim Biophys Acta 2002; 1572(1): 1-9.
48. Heller LC, Jaroszeski MJ, Coppola D, McCray AN, Hickey J, Heller R. Optimization of cutaneous electrically mediated plasmid DNA delivery using novel electrode. Gene Ther 2007; 14(3): 275-80.
49. Gothelf A, Eriksen J, Hojman P, Gehl J. Duration and level of transgene expression after gene electrotransfer to skin in mice. Gene Ther 2010; 17(7): 839-45.
50. Vandermeulen G, Richiardi H, Escriou V, et al. Skin-specific promoters for genetic immunisation by DNA electroporation. Vaccine 2009; 27(32): 4272-7.
51. Liu F, Huang L. Electric gene transfer to the liver following systemic administration of plasmid DNA. Gene Ther 2002; 9(16): 1116-9.
52. Sakai M, Nishikawa M, Thanaketpaisarn O, Yamashita F, Hashida M. Hepatocyte-targeted gene transfer by combination of vascularly delivered plasmid DNA and in vivo electroporation. Gene Ther 2005; 12(7): 607-16.
53. Jaichandran S, Yap ST, Khoo AB, Ho LP, Tien SL, Kon OL. In vivo liver electroporation: optimization and demonstration of therapeutic efficacy. Hum Gene Ther 2006; 17(3): 362-75.
54. Yazawa K, Isaka Y, Takahara S, et al. Direct transfer of hepatocyte growth factor gene into kidney suppresses cyclosporin A nephrotoxicity in rats. Nephrol Dial Transplant 2004; 19(4): 812-6.
55. Mizui M, Isaka Y, Takabatake Y, et al. Transcription factor Ets-1 is essential for mesangial matrix remodeling. Kidney Int 2006; 70(2): 298-305.
56. Fujii N, Isaka Y, Takabatake Y, et al. Targeting of interstitial cells using a simple gene-transfer strategy. Nephrol Dial Transplant 2006; 21(10): 2745-53.
57. Gazdhar A, Bilici M, Pierog J, et al. In vivo electroporation and ubiquitin promoter--a protocol for sustained gene expression in the lung. J Gene Med 2006; 8(7): 910-8.
58. Pringle IA, McLachlan G, Collie DD, et al. Electroporation enhances reporter gene expression following delivery of naked plasmid DNA to the lung. J Gene Med 2007; 9(5): 369-80.
59. Kaufman CD, Geiger RC, Dean DA. Electroporation- and mechanical ventilation-mediated gene transfer to the lung. Gene Ther 2010; 17(9): 1098-104.
60. Harrison RL, Byrne BJ, Tung L. Electroporation-mediated gene transfer in cardiac tissue. FEBS Lett 1998; 435(1): 1-5.
61. Wang Y, Bai Y, Price C, et al. Combination of electroporation and DNA/dendrimer complexes enhances gene transfer into murine cardiac transplants. Am J Transplant 2001; 1(4): 334-8.
62. Marshall WG, Jr., Boone BA, Burgos JD, et al. Electroporationmediated delivery of a naked DNA plasmid expressing VEGF to the porcine heart enhances protein expression. Gene Ther 2010; 17(3): 419-23.
63. Fedorov VV, Nikolski VP, Efimov IR. Effect of electroporation on cardiac electrophysiology. Methods Mol Biol 2008; 423: 433-48.
64. Hao J, Li SK, Kao WW, Liu CY. Gene delivery to cornea. Brain Res Bull 2010; 81(2-3): 256-61.
65. Blair-Parks K, Weston BC, Dean DA. High-level gene transfer to the cornea using electroporation. J Gene Med 2002; 4(1): 92-100.
66. Hao J, Li SK, Liu CY, Kao WW. Electrically assisted delivery of macromolecules into the corneal epithelium. Exp Eye Res 2009; 89(6): 934-41.
67. Babiuk S, Baca-Estrada ME, Foldvari M, et al. Electroporation improves the efficacy of DNA vaccines in large animals. Vaccine 2002; 20(27-28): 3399-408.
68. Otten G, Schaefer M, Doe B, et al. Enhancement of DNA vaccine potency in rhesus macaques by electroporation. Vaccine 2004; 22(19): 2489-93.
69. Simon AJ, Casimiro DR, Finnefrock AC, et al. Enhanced in vivo transgene expression and immunogenicity from plasmid vectors following electrostimulation in rodents and primates. Vaccine 2008; 26(40): 5202-9.
70. Widera G, Austin M, Rabussay D, et al. Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J Immunol 2000; 164(9): 4635-40.
71. Zucchelli S, Capone S, Fattori E, et al. Enhancing B- and T-cell immune response to a hepatitis C virus E2 DNA vaccine by intramuscular electrical gene transfer. J Virol 2000; 74(24): 11598-607.
72. Bodles-Brakhop AM, Heller R, Draghia-Akli R. Electroporation for the delivery of DNA-based vaccines and immunotherapeutics: current clinical developments. Mol Ther 2009; 17(4): 585-92.
73. Roos AK, Moreno S, Leder C, Pavlenko M, King A, Pisa P. Enhancement of cellular immune response to a prostate cancer DNA vaccine by intradermal electroporation. Mol Ther 2006; 13(2): 320-7.
74. Ahmad S, Casey G, Sweeney P, Tangney M, O'Sullivan GC. Prostate stem cell antigen DNA vaccination breaks tolerance to selfantigen and inhibits prostate cancer growth. Mol Ther 2009; 17(6): 1101-8.
75. Heller L, Pottinger C, Jaroszeski MJ, Gilbert R, Heller R. In vivo electroporation of plasmids encoding GM-CSF or interleukin-2 into existing B16 melanomas combined with electrochemotherapy induces long-term antitumour immunity. Melanoma Res 2000; 10(6): 577-83.
76. Horton HM, Lalor PA, Rolland AP. IL-2 plasmid electroporation: from preclinical studies to phase I clinical trial. Methods Mol Biol 2008; 423: 361-72.
77. Lohr F, Lo DY, Zaharoff DA, et al. Effective tumor therapy with plasmid-encoded cytokines combined with in vivo electroporation. Cancer Res 2001; 61(8): 3281-4.
78. Lucas ML, Heller L, Coppola D, Heller R. IL-12 plasmid delivery by in vivo electroporation for the successful treatment of established subcutaneous B16.F10 melanoma. Mol Ther 2002; 5(6): 668-75.
79. Zhu S, Lee DA, Li S. IL-12 and IL-27 sequential gene therapy via intramuscular electroporation delivery for eliminating distal aggressive tumors. J Immunol 2010; 184(5): 2348-54.
80. Nakai N, Kishida T, Hartmann G, et al. Mitf silencing cooperates with IL-12 gene transfer to inhibit melanoma in mice. Int Immunopharmacol 2010; 10(4): 540-5.
81. Vidic S, Markelc B, Sersa G, et al. MicroRNAs targeting mutant K-ras by electrotransfer inhibit human colorectal adenocarcinoma cell growth in vitro and in vivo. Cancer Gene Ther 2010; 17(6): 409-19.
82. Reed SD, Fulmer A, Buckholz J, et al. Bleomycin/interleukin-12 electrochemogene therapy for treating naturally occurring spontaneous neoplasms in dogs. Cancer Gene Ther 2010; 17(7): 457-64.
83. Long YC, Jaichandran S, Ho LP, Tien SL, Tan SY, Kon OL. FVIII gene delivery by muscle electroporation corrects murine hemophilia A. J Gene Med 2005; 7(4): 494-505.
84. Maruyama H, Ataka K, Gejyo F, et al. Long-term production of erythropoietin after electroporation-mediated transfer of plasmid DNA into the muscles of normal and uremic rats. Gene Ther 2001; 8(6): 461-8.
85. Gothelf A, Hojman P, Gehl J. Therapeutic levels of erythropoietin (EPO) achieved after gene electrotransfer to skin in mice. Gene Ther 2010; 17(9): 1077-84.
86. Oliveira NA, Cecchi CR, Higuti E, et al. Long-term human growth hormone expression and partial phenotypic correction by plasmidbased gene therapy in an animal model of isolated growth hormone deficiency. J Gene Med 2010; 12(7): 580-5.
87. Khan AS, Draghia-Akli R, Shypailo RJ, Ellis KI, Mersmann H, Fiorotto ML. A comparison of the growth responses following intramuscular GHRH plasmid administration versus daily growth hormone injections in young pigs. Mol Ther 2010; 18(2): 327-33.
88. Bodles-Brakhop AM, Brown PA, Pope MA, Draghia-Akli R. Double- blinded, Placebo-controlled plasmid GHRH trial for cancerassociated anemia in dogs. Mol Ther 2008; 16(5): 862-70.
89. Rissanen TT, Yla-Herttuala S. Current status of cardiovascular gene therapy. Mol Ther 2007; 15(7): 1233-47.
90. Nishikage S, Koyama H, Miyata T, Ishii S, Hamada H, Shigematsu H. In vivo electroporation enhances plasmid-based gene transfer of basic fibroblast growth factor for the treatment of ischemic limb. J Surg Res 2004; 120(1): 37-46.
91. Ferraro B, Cruz YL, Baldwin M, Coppola D, Heller R. Increased perfusion and angiogenesis in a hindlimb ischemia model with plasmid FGF-2 delivered by noninvasive electroporation. Gene Ther 2010; 17(6): 763-9.
92. Sacramento CB, da Silva FH, Nardi NB, et al. Synergistic effect of vascular endothelial growth factor and granulocyte colonystimulating factor double gene therapy in mouse limb ischemia. J Gene Med 2010; 12(3): 310-9.
93. Branski LK, Pereira CT, Herndon DN, Jeschke MG. Gene therapy in wound healing: present status and future directions. Gene Ther 2007; 14(1): 1-10.
94. Ferraro B, Cruz YL, Coppola D, Heller R. Intradermal delivery of plasmid VEGF(165) by electroporation promotes wound healing. Mol Ther 2009; 17(4): 651-7.
95. Rezende FC, Gomes HC, Lisboa B, Lucca AF, Han SW, Ferreira LM. Electroporation of vascular endothelial growth factor gene in a unipedicle transverse rectus abdominis myocutaneous flap reduces necrosis. Ann Plast Surg 2010; 64(2): 242-6.
96. Lin MP, Marti GP, Dieb R, et al. Delivery of plasmid DNA expression vector for keratinocyte growth factor-1 using electroporation to improve cutaneous wound healing in a septic rat model. Wound Repair Regen 2006; 14(5): 618-24.
97. Liu L, Marti GP, Wei X, et al. Age-dependent impairment of HIF- 1alpha expression in diabetic mice: Correction with electroporation- facilitated gene therapy increases wound healing, angiogenesis, and circulating angiogenic cells. J Cell Physiol 2008; 217(2): 319-27.
98. Ferrer A, Foster H, Wells KE, Dickson G, Wells DJ. Long-term expression of full-length human dystrophin in transgenic mdx mice expressing internally deleted human dystrophins. Gene Ther 2004; 11(11): 884-93.
99. Vilquin JT, Kennel PF, Paturneau-Jouas M, et al. Electrotransfer of naked DNA in the skeletal muscles of animal models of muscular dystrophies. Gene Ther 2001; 8(14): 1097-107.
100. Beshay M, Gazdhar A, Gugger M, Reymond M, Schmid RA. The feasibility of non-viral gene transfer to the diaphragm in vivo. Dev Growth Differ 2009.
101. Inoue A, Takahashi KA, Mazda O, et al. Comparison of antirheumatic effects of local RNAi-based therapy in collagen induced arthritis rats using various cytokine genes as molecular targets. Mod Rheumatol 2009; 19(2): 125-33.
102. Inoue A, Takahashi KA, Mazda O, et al. Electro-transfer of small interfering RNA ameliorated arthritis in rats. Biochem Biophys Res Commun 2005; 336(3): 903-8.
103. Denys A, Thiolat A, Descamps D, et al. Intra-articular electrotransfer of mouse soluble tumour necrosis factor receptor in a murine model of rheumatoid arthritis. J Gene Med 2010; 12(8): 659-68.
104. Bloquel C, Denys A, Boissier MC, et al. Intra-articular electrotransfer of plasmid encoding soluble TNF receptor variants in normal and arthritic mice. J Gene Med 2007; 9(11): 986-93.
105. Mutlu GM, Machado-Aranda D, Norton JE, et al. Electroporationmediated gene transfer of the Na+,K+ -ATPase rescues endotoxininduced lung injury. Am J Respir Crit Care Med 2007; 176(6): 582-90.
106. Gazdhar A, Fachinger P, van Leer C, et al. Gene transfer of hepatocyte growth factor by electroporation reduces bleomycin-induced lung fibrosis. Am J Physiol Lung Cell Mol Physiol 2007; 292(2): L529-36.
107. Matsumoto K, Nagayasu T, Hishikawa Y, et al. Keratinocyte growth factor accelerates compensatory growth in the remaining lung after trilobectomy in rats. J Thorac Cardiovasc Surg 2009; 137(6): 1499-507.
108. Prud'homme GJ, Draghia-Akli R, Wang Q. Plasmid-based gene therapy of diabetes mellitus. Gene Ther 2007; 14(7): 553-64.
109. Glinka Y, Chang Y, Prud'homme GJ. Protective regulatory T cell generation in autoimmune diabetes by DNA covaccination with islet antigens and a selective CTLA-4 ligand. Mol Ther 2006; 14(4): 578-87.
110. Croze F, Prud'homme GJ. Gene therapy of streptozotocin-induced diabetes by intramuscular delivery of modified preproinsulin genes. J Gene Med 2003; 5(5): 425-37.
111. Kumar M, Hunag Y, Glinka Y, Prud'homme GJ, Wang Q. Gene therapy of diabetes using a novel GLP-1/IgG1-Fc fusion construct normalizes glucose levels in db/db mice. Gene Ther 2007; 14(2): 162-72.
112. Soltani N, Kumar M, Glinka Y, Prud'homme GJ, Wang Q. In vivo expression of GLP-1/IgG-Fc fusion protein enhances beta-cell mass and protects against streptozotocin-induced diabetes. Gene Ther 2007; 14(12): 981-8.
113. Murakami T, Arai M, Sunada Y, Nakamura A. VEGF 164 gene transfer by electroporation improves diabetic sensory neuropathy in mice. J Gene Med 2006; 8(6): 773-81.
114. Murakami T, Imada Y, Kawamura M, et al. Placental growth factor- 2 gene transfer by electroporation restores diabetic sensory neuropathy in mice. Exp Neurol 2011; 227(1): 195-202.
115. Low L, Mander A, McCann K, et al. DNA vaccination with electroporation induces increased antibody responses in patients with prostate cancer. Hum Gene Ther 2009; 20(11): 1269-78.
116. Heller LC, Heller R. Electroporation gene therapy preclinical and clinical trials for melanoma. Curr Gene Ther 2010; 10(4): 312-7.
117. Daud AI, DeConti RC, Andrews S, et al. Phase I trial of interleukin- 12 plasmid electroporation in patients with metastatic melanoma. J Clin Oncol 2008; 26(36): 5896-903.
118. Richards JM, Gonzalez R, Schwarzenberger P, et al. Phase I trial of IL-2 plasmid DNA with electroporation in metastatic melanoma. J Clin Oncol 2007; 25(18S): 8578.
119. Kalat M, Kupcu Z, Schuller S, et al. In vivo plasmid electroporation induces tumor antigen-specific CD8+ T-cell responses and delays tumor growth in a syngeneic mouse melanoma model. Cancer Res 2002; 62(19): 5489-94.
120. Sallberg M, Frelin L, Diepolder HM, et al. Activation of T cell responses and reductions in the viral load following therapeutic vaccination using naked DNA delivered by in vivo electroporation in patients with chronic hepatitis C. Mol Ther 2009; 17(Supplement 1): S55.
121. Wallace M, Evans B, Woods S, et al. Tolerability of two sequential electroporation treatments using MedPulser DNA delivery system (DDS) in healthy adults. Mol Ther 2009; 17(5): 922-8.
122. Fuller DH, Loudon P, Schmaljohn C. Preclinical and clinical progress of particle-mediated DNA vaccines for infectious diseases. Methods 2006; 40(1): 86-97.
123. Drape RJ, Macklin MD, Barr LJ, Jones S, Haynes JR, Dean HJ. Epidermal DNA vaccine for influenza is immunogenic in humans. Vaccine 2006; 24(21): 4475-81.
124. Roy MJ, Wu MS, Barr LJ, et al. Induction of antigen-specific CD8+ T cells, T helper cells, and protective levels of antibody in humans by particle-mediated administration of a hepatitis B virus DNA vaccine. Vaccine 2000; 19(7-8): 764-78.
125. Jones S, Evans K, McElwaine-Johnn H, et al. DNA vaccination protects against an influenza challenge in a double-blind randomised placebo-controlled phase 1b clinical trial. Vaccine 2009; 27(18): 2506-12.
126. Cassaday RD, Sondel PM, King DM, et al. A phase I study of immunization using particle-mediated epidermal delivery of genes for gp100 and GM-CSF into uninvolved skin of melanoma patients. Clin Cancer Res 2007; 13(2 Pt 1): 540-9.