Electroporation in DNA vaccination protocols against cancer

Current Drug Metabolism

Volumn 14, Issue 3, 2013, Pages 291-299

  Chiarella, Pieranna ^a,b   Fazio, Vito Michele ^b,c   Signori, Emanuela ^a,b  

^a CNR   (Italy)

^b UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^c CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

Author keywords

Cancer; DNA vaccine; Electroporation; Immune response; Tumour antigen

Indexed keywords

DNA VACCINE;

BREAST CANCER; COLON CANCER; COLORECTAL CANCER; DRUG EFFICACY; DRUG SAFETY; ELECTROPORATION; HUMAN; IMMUNOGENICITY; MELANOMA; NONHUMAN; PROSTATE CANCER; REVIEW; TUMOR IMMUNITY; UTERINE CERVIX CARCINOMA IN SITU; VACCINATION;

ANIMALS; CANCER VACCINES; ELECTROCHEMOTHERAPY; HUMANS; NEOPLASMS; VACCINES, DNA;

EID: 84877960546     PISSN: 13892002     EISSN: 18755453     Source Type: Journal    
DOI: 10.2174/1389200211314030004     Document Type: Review

References (89)

1. Neumann, E.; Schaefer-Ridder, M.; Wang, Y.; Hofschneider, P. H. Gene transfer into mouse lyoma cells by electroporation in high electric fields. Embo. J., 1982, 1(7), 841-5.
2. 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. (Pubitemid 18038276)
3. Mir, L. M. Nucleic acids electrotransfer-based gene therapy (electrogenetherapy): past, current, and future. Mol. Biotechnol., 2009, 43 (2), 167-76.
4. Cemazar, M.; Tamzali, Y.; Sersa, G.; Tozon, N.; Mir, L. M.; Miklavcic, D.; Lowe, R.; Teissie, J. Electrochemotherapy in veterinary oncology. J. Vet. Intern. Med., 2008, 22 (4), 826-31. (Pubitemid 352039161)
5. Dunn, G. P.; Old, L. J.; Schreiber, R. D. The three Es of cancer immunoediting. Annu. Rev. Immunol., 2004, 22, 329-60. (Pubitemid 38680426)
6. List, A. F.; Spier, C. M.; Miller, T. P.; Grogan, T. M. Deficient tumor-infiltrating T-lymphocyte response in malignant lymphoma: relationship to HLA expression and host immunocompetence. Leukemia, 1993, 7(3), 398-403. (Pubitemid 23093098)
7. Stopeck, A. T.; Gessner, A.; Miller, T. P.; Hersh, E. M.; Johnson, C. S.; Cui, H.; Frutiger, Y.; Grogan, T. M. Loss of B7.2 (CD86) and intracellular adhesion molecule 1 (CD54) expression is associated with decreased tumor-infiltrating T lymphocytes in diffuse Bcell large-cell lymphoma. Clin. Cancer Res., 2000, 6 (10), 3904-9.
8. Bushway, M.; Cycon, K. A.; Mulvaney, K.; Murphy, S. P. Coordinate loss of MHC class II expression in the diffuse large B cell lymphoma cell line OCI-Ly2 is due to a novel mutation in RFXAP. Immunogenetics, 2010, 62 (2), 109-16.
9. Khanna, R. Tumour surveillance: missing peptides and MHC molecules. Immunol. Cell Biol., 1998, 76 (1), 20-6. (Pubitemid 28194693)
10. Dunn, G. P.; Old, L. J.; Schreiber, R. D. The immunobiology of cancer immunosurveillance and immunoediting. Immunity, 2004, 21 (2), 137-48. (Pubitemid 39094044)
11. Zou, W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer, 2005, 5 (4), 263-74. (Pubitemid 40488632)
12. Van Den Berg, J. H.; Oosterhuis, K.; Beijnen, J. H.; Nuijen, B.; Haanen, J. B. DNA vaccination in oncology: current status, opportunities and perspectives. Curr. Clin. Pharmacol., 2010, 5(3), 218-25.
13. Liu, M. A. Gene-based vaccines: Recent developments. Curr. Opin. Mol. Ther., 2010, 12 (1), 86-93.
14. Signori, E.; Iurescia, S.; Massi, E.; Fioretti, D.; Chiarella, P.; De Robertis, M.; Rinaldi, M.; Tonon, G.; Fazio, V. M. DNA vaccination strategies for anti-tumour effective gene therapy protocols. Cancer Immunol. Immunother., 2010, 59 (10), 1583-91.
15. Doria-Rose, N. A.; Haigwood, N. L. DNA vaccine strategies: candidates for immune modulation and immunization regimens. Methods, 2003, 31(3), 207-16. (Pubitemid 37162793)
16. Ciafre, S. A.; Rinaldi, M.; Gasparini, P.; Seripa, D.; Bisceglia, L.; Zelante, L.; Farace, M. G.; Fazio, V. M. Stability and functional effectiveness of phosphorothioate modified duplex DNA and synthetic 'mini-genes'. Nucleic Acids Res., 1995, 23(20), 4134-42.
17. Pulsawat, P.; Piboonpocanun, S.; Sirivichayakul, S.; Buranapraditkun, S.; Jacquet, A.; Shimada, M.; Okuda, K.; Ruxrungtham, K. Production and immunogenicity of hypoallergenic codonoptimized DNA vaccine encoding mature Der p 1 allergen. J. Investig. Allergol. Clin. Immunol., 2010, 20 (7), 582-90.
18. Chiarella, P.; Massi, E.; De Robertis, M.; Fazio, V. M.; Signori, E., Strategies for effective naked-DNA vaccination against infectious diseases. Recent Pat Antiinfect. Drug Discov., 2008, 3 (2), 93-101.
19. Belyakov, I. M.; Wyatt, L. S.; Ahlers, J. D.; Earl, P.; Pendleton, C. D.; Kelsall, B. L.; Strober, W.; Moss, B.; Berzofsky, J. A. Induction of a mucosal cytotoxic T-lymphocyte response by intrarectal immunization with a replication-deficient recombinant vaccinia virus expressing human immunodeficiency virus 89.6 envelope protein. J. Virol., 1998, 72(10), 8264-72. (Pubitemid 28421824)
20. Sasaki, S.; Takeshita, F.; Xin, K. Q.; Ishii, N.; Okuda, K. Adjuvant formulations and delivery systems for DNA vaccines. Methods, 2003, 31(3), 243-54. (Pubitemid 37162797)
21. Elsabahy, M.; Nazarali, A.; Foldvari, M. Non-Viral Nucleic Acid Delivery: Key Challenges and Future Directions. Curr. Drug Deliv., 2011, 8(3), 235-44.
22. Aihara, H.; Miyazaki, J. Gene transfer into muscle by electroporation in vivo. Nat. Biotechnol.,1998, 16 (9), 867-70. (Pubitemid 28405859)
23. Suzuki, T.; Shin, B. C.; Fujikura, K.; Matsuzaki, T.; Takata, K. Direct gene transfer into rat liver cells by in vivo electroporation. FEBS Lett., 1998, 425(3), 436-40. (Pubitemid 28178847)
24. Mir, L. M.; Bureau, M. F.; Gehl, J.; Rangara, R.; Rouy, D.; Caillaud, J. M.; Delaere, P.; Branellec, D.; Schwartz, B.; Scherman, D. High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc. Natl. Acad. Sci. USA, 1999, 96 (8), 4262-7. (Pubitemid 29190324)
25. Ayuni, E. L.; Gazdhar, A.; Giraud, M. N.; Kadner, A.; Gugger, M.; Cecchini, M.; Caus, T.; Carrel, T. P.; Schmid, R. A.; Tevaearai, H. T. In vivo electroporation mediated gene delivery to the beating heart. PLoS One, 2010, 5(12), e14467.
26. Blair-Parks, K.; Weston, B. C.; Dean, D. A. High-level gene transfer to the cornea using electroporation. J. Gene Med., 2002, 4(1), 92-100. (Pubitemid 40277160)
27. Heller, R.; Jaroszeski, M.; Atkin, A.; Moradpour, D.; Gilbert, R.; Wands, J.; Nicolau, C. In vivo gene electroinjection and expression in rat liver. FEBS Lett., 1996, 389(3), 225-8. (Pubitemid 26251823)
28. Martin, J. B.; Young, J. L.; Benoit, J. N.; Dean, D. A. Gene transfer to intact mesenteric arteries by electroporation. J. Vasc. Res., 2000, 37(5), 372-80.
29. Chiarella, P.; Massi, E.; De Robertis, M.; Sibilio, A.; Parrella, P.; Fazio, V. M.; Signori, E. Electroporation of skeletal muscle induces danger signal release and antigen-presenting cell recruitment independently of DNA vaccine administration. Expert Opin. Biol. Ther., 2008, 8(11), 1645-57.
30. Escoffre, J. M.; Portet, T.; Wasungu, L.; Teissie, J.; Dean, D.; Rols, M. P. 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.
31. Bureau, M. F.; Gehl, J.; Deleuze, V.; Mir, L. M.; Scherman, D. Importance of association between permeabilization and electrophoretic forces for intramuscular DNA electrotransfer. Biochim. Biophys. Acta, 2000, 1474 (3), 353-9. (Pubitemid 30209876)
32. Gehl, J.; Sorensen, T. H.; Nielsen, K.; Raskmark, P.; Nielsen, S. L.; Skovsgaard, T.; Mir, L. M. In vivo electroporation of skeletal muscle: threshold, efficacy and relation to electric field distribution. Biochim. Biophys. Acta, 1999, 1428(2-3), 233-40. (Pubitemid 29352271)
33. McMahon, J. M.; Signori, E.; Wells, K. E.; Fazio, V. M.; Wells, D. J. Optimisation of electrotransfer of plasmid into skeletal muscle by pretreatment with hyaluronidase-increased expression with reduced muscle damage. Gene Ther., 2001, 8(16), 1264-70. (Pubitemid 32780815)
34. Babiuk, S.; Baca-Estrada, M. E.; Foldvari, M.; Middleton, D. M.; Rabussay, D.; Widera, G.; Babiuk, L. A. Increased gene expression and inflammatory cell infiltration caused by electroporation are both important for improving the efficacy of DNA vaccines. J. Biotechnol., 2004, 110(1), 1-10. (Pubitemid 38510249)
35. Hojman, P.; Gissel, H.; Andre, F. M.; Cournil-Henrionnet, C.; Eriksen, J.; Gehl, J.; Mir, L. M. Physiological effects of high-and low-voltage pulse combinations for gene electrotransfer in muscle. Hum Gene Ther 2008, 19(11), 1249-60.
36. Widera, G.; Austin, M.; Rabussay, D.; Goldbeck, C.; Barnett, S. W.; Chen, M.; Leung, L.; Otten, G. R.; Thudium, K.; Selby, M. J.; Ulmer, J. B. Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J. Immunol., 2000, 164(9), 4635-40. (Pubitemid 30238062)
37. Mathiesen, I. Electropermeabilization of skeletal muscle enhances gene transfer in vivo. Gene Ther., 1999, 6(4), 508-14. (Pubitemid 29192659)
38. Tsang, C.; Babiuk, S.; Van Drunen Littel-Van Den Hurk, S.; Babiuk, L. A.; Griebel, P. A single DNA immunization in combination with electroporation prolongs the primary immune response and maintains immune memory for six months. Vaccine, 2007, 25(30), 5485-94. (Pubitemid 47039264)
39. Buchan, S.; Gronevik, E.; Mathiesen, I.; King, C. A.; Stevenson, F. K.; Rice, J. Electroporation as a "prime/boost" strategy for naked DNA vaccination against a tumor antigen. J. Immunol., 2005, 174 (10), 6292-8. (Pubitemid 40663821)
40. Bachy, M.; Boudet, F.; Bureau, M.; Girerd-Chambaz, Y.; Wils, P.; Scherman, D.; Meric, C. Electric pulses increase the immunogenicity of an influenza DNA vaccine injected intramuscularly in the mouse. Vaccine, 2001, 19 (13-14), 1688-93. (Pubitemid 32175729)
41. Capone, S.; Zampaglione, I.; Vitelli, A.; Pezzanera, M.; Kierstead, L.; Burns, J.; Ruggeri, L.; Arcuri, M.; Cappelletti, M.; Meola, A.; Ercole, B. B.; Tafi, R.; Santini, C.; Luzzago, A.; Fu, T. M.; Colloca, S.; Ciliberto, G.; Cortese, R.; Nicosia, A.; Fattori, E.; Folgori, A. Modulation of the immune response induced by gene electrotransfer of a hepatitis C virus DNA vaccine in nonhuman primates. J. Immunol., 2006, 177(10), 7462-71. (Pubitemid 44715117)
42. Gronevik, E.; Mathiesen, I.; Lomo, T. Early events of electroporation-mediated intramuscular DNA vaccination potentiate Th1-directed immune responses. J. Gene Med., 2005, 7 (9), 1246-54. (Pubitemid 41335176)
43. Golzio, M.; Escoffre, J. M.; Portet, T.; Mauroy, C.; Teissie, J.; Dean, D. S.; Rols, M. P. Observations of the mechanisms of electromediated DNA uptake from vesicles to tissues. Curr. Gene Ther., 2010, 10(4), 256-66.
44. Bodles-Brakhop, A. M.; 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.
45. Tjelle, T. E.; Rabussay, D.; Ottensmeier, C.; Mathiesen, I.; Kjeken, R. Taking electroporation-based delivery of DNA vaccination into humans: a generic clinical protocol. Methods Mol. Biol., 2008, 423, 497-507.
46. Belehradek, M.; Domenge, C.; Luboinski, B.; Orlowski, S.; Belehradek, J., Jr.; Mir, L. M. Electrochemotherapy, a new antitumor treatment. First clinical phase I-II trial. Cancer, 1993, 72(12), 3694-700. (Pubitemid 24000606)
47. Heller, L. C.; Heller, R. Electroporation gene therapy preclinical and clinical trials for melanoma. Curr. Gene Ther., 2010, 10(4), 312-7.
48. Daud, A. I.; DeConti, R. C.; Andrews, S.; Urbas, P.; Riker, A. I.; Sondak, V. K.; Munster, P. N.; Sullivan, D. M.; Ugen, K. E.; Messina, J. L.; Heller, R. Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J. Clin. Oncol., 2008, 26(36), 5896-903.
49. Hojman, P. Gene transfer to muscle tissues: moving into clinical use. In: Clinical Aspects of Electroporation, 2011, pp.177-188.
50. Goethelf, A.; Ghel, J. Gene electrotransfer to skin. In: Clinical Aspects of Electroporation 2011, pp.190-202.
51. Rinaldi, M.; Catapano, A. L.; Parrella, P.; Ciafre, S. A.; Signori, E.; Seripa, D.; Uboldi, P.; Antonini, R.; Ricci, G.; Farace, M. G.; Fazio, V. M. Treatment of severe hypercholesterolemia in apolipoprotein E-deficient mice by intramuscular injection of plasmid DNA. Gene Ther., 2000, 7(21), 1795-801.
52. Signori, E.; Rinaldi, M.; Fioretti, D.; Iurescia, S.; Seripa, D.; Perrone, G.; Norata, G. D.; Catapano, A. L.; Fazio, V. M. ApoE gene delivery inhibits severe hypercholesterolemia in newborn ApoEKO mice. Biochem. Biophys. Res. Commun., 2007, 361(2), 543-8. (Pubitemid 47193118)
53. Tripathy, S. K.; Svensson, E. C.; Black, H. B.; Goldwasser, E.; Margalith, M.; Hobart, P. M.; Leiden, J. M. Long-term expression of erythropoietin in the systemic circulation of mice after intramuscular injection of a plasmid DNA vector. Proc. Natl. Acad. Sci. U. S. A., 1996, 93(20), 10876-80. (Pubitemid 26333084)
54. Ma, J. X.; Yang, Z.; Chao, J.; Chao, L. Intramuscular delivery of rat kallikrein-binding protein gene reverses hypotension in transgenic mice expressing human tissue kallikrein. J. Biol. Chem., 1995, 270(1), 451-5.
55. Tsurumi, Y.; Takeshita, S.; Chen, D.; Kearney, M.; Rossow, S. T.; Passeri, J.; Horowitz, J. R.; Symes, J. F.; Isner, J. M. Direct intramuscular gene transfer of naked DNA encoding vascular endothelial growth factor augments collateral development and tissue perfusion. Circulation, 1996, 94(12), 3281-90. (Pubitemid 26427500)
56. Liu, M. A., DNA vaccines: an historical perspective and view to the future. Immunol. Rev., 2011, 239(1), 62-84.
57. Gehl, J.; Mir, L. M. Determination of optimal parameters for in vivo gene transfer by electroporation, using a rapid in vivo test for cell permeabilization. Biochem. Biophys. Res. Commun., 1999, 261(2), 377-80. (Pubitemid 29392484)
58. 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.
59. Hojman, P.; Zibert, J. R.; Gissel, H.; Eriksen, J.; Gehl, J. Gene expression profiles in skeletal muscle after gene electrotransfer. BMC Mol. Biol., 2007, 8, 56.
60. Radkevich-Brown, O.; Piechocki, M. P.; Back, J. B.; Weise, A. M.; Pilon-Thomas, S.; Wei, W. Z. Intratumoral DNA electroporation induces anti-tumor immunity and tumor regression. Cancer Immunol. Immunother., 2010, 59(3), 409-17.
61. Mahvi, D. M.; Henry, M. B.; Albertini, M. R.; Weber, S.; Meredith, K.; Schalch, H.; Rakhmilevich, A.; Hank, J.; Sondel, P. Intratumoral injection of IL-12 plasmid DNA-results of a phase I/IB clinical trial. Cancer Gene Ther., 2007, 14(8), 717-23. (Pubitemid 47080365)
62. Prud'homme, G. J.; Glinka, Y.; Khan, A. S.; Draghia-Akli, R. Electroporation-enhanced nonviral gene transfer for the prevention or treatment of immunological, endocrine and neoplastic diseases. Curr. Gene Ther., 2006, 6(2), 243-73.
63. Roos, A. K.; 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. (Pubitemid 43056897)
64. Drabick, J. J.; Glasspool-Malone, J.; King, A.; Malone, R. W. Cutaneous transfection and immune responses to intradermal nucleic acid vaccination are significantly enhanced by in vivo electropermeabilization. Mol. Ther., 2001, 3(2), 249-55. (Pubitemid 32509828)
65. Hooper, J. W.; Golden, J. W.; Ferro, A. M.; King, A. D. Smallpox DNA vaccine delivered by novel skin electroporation device protects mice against intranasal poxvirus challenge. Vaccine, 2007, 25(10), 1814-23. (Pubitemid 46176327)
66. Babiuk, S.; Baca-Estrada, M. E.; Foldvari, M.; Baizer, L.; Stout, R.; Storms, M.; Rabussay, D.; Widera, G.; Babiuk, L. Needle-free topical electroporation improves gene expression from plasmids administered in porcine skin. Mol. Ther., 2003, 8(6), 992-8. (Pubitemid 38072312)
67. Hirao, L. A.; Wu, L.; Khan, A. S.; Satishchandran, A.; Draghia-Akli, R.; Weiner, D. B. Intradermal/subcutaneous immunization by electroporation improves plasmid vaccine delivery and potency in pigs and rhesus macaques. Vaccine, 2008, 26(3), 440-8.
68. Gothelf, A.; Mahmood, F.; Dagnaes-Hansen, F.; Gehl, J. Efficacy of transgene expression in porcine skin as a function of electrode choice. Bioelectrochem., 2011, 82(2), 95-102.
69. Hirao, L. A.; Draghia-Akli, R.; Prigge, J. T.; Yang, M.; Satishchandran, A.; Wu, L.; Hammarlund, E.; Khan, A. S.; Babas, T.; Rhodes, L.; Silvera, P.; Slifka, M.; Sardesai, N. Y.; Weiner, D. B. Multivalent smallpox DNA vaccine delivered by intradermal electroporation drives protective immunity in nonhuman primates against lethal monkeypox challenge. J. Infect. Dis., 2011, 203(1), 95-102.
70. 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.
71. Roos, A. K.; Eriksson, F.; Timmons, J. A.; Gerhardt, J.; Nyman, U.; Gudmundsdotter, L.; Brave, A.; Wahren, B.; Pisa, P. Skin electroporation: effects on transgene expression, DNA persistence and local tissue environment. PLoS One, 2009, 4(9), e7226.
72. Roos, A. K.; Eriksson, F.; Walters, D. C.; Pisa, P.; King, A. D. Optimization of skin electroporation in mice to increase tolerability of DNA vaccine delivery to patients. Mol. Ther., 2009, 17(9), 1637-42.
73. Donate, A.; Coppola, D.; Cruz, Y.; Heller, R. Evaluation of a novel non-penetrating electrode for use in DNA vaccination. PLoS One, 2011, 6(4), e19181.
74. Gothelf, A.; Gehl, J. Gene electrotransfer to skin; review of existing literature and clinical perspectives. Curr. Gene Ther., 2010, 10(4), 287-99.
75. Chiarella, P.; Fazio, V. M.; Signori, E. Application of electroporation in DNA vaccination protocols. Curr. Gene Ther., 2010, 10(4), 281-6.
76. Quaglino, E.; Iezzi, M.; Mastini, C.; Amici, A.; Pericle, F.; Di Carlo, E.; Pupa, S. M.; De Giovanni, C.; Spadaro, M.; Curcio, C.; Lollini, P. L.; Musiani, P.; Forni, G.; Cavallo, F. Electroporated DNA vaccine clears away multifocal mammary carcinomas in her-2/neu transgenic mice. Cancer Res., 2004, 64(8), 2858-64. (Pubitemid 38500626)
77. Curcio, C.; Khan, A. S.; Amici, A.; Spadaro, M.; Quaglino, E.; Cavallo, F.; Forni, G.; Draghia-Akli, R. DNA immunization using constant-current electroporation affords long-term protection from autochthonous mammary carcinomas in cancer-prone transgenic mice. Cancer Gene Ther., 2008, 15(2), 108-14.
78. Lladser, A.; Ljungberg, K.; Tufvesson, H.; Tazzari, M.; Roos, A. K.; Quest, A. F.; Kiessling, R. Intradermal DNA electroporation induces survivin-specific CTLs, suppresses angiogenesis and confers protection against mouse melanoma. Cancer Immunol. Immunother., 2009, 59(1), 81-92.
79. Heller, L.; Pottinger, C.; Jaroszeski, M. J.; 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. (Pubitemid 32011981)
80. Lucas, M. L.; 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. (Pubitemid 34624563)
81. Pavlin, D.; Cemazar, M.; Kamensek, U.; Tozon, N.; Pogacnik, A.; Sersa, G. Local and systemic antitumor effect of intratumoral and peritumoral IL-12 electrogene therapy on murine sarcoma. Cancer Biol. Ther., 2009, 8(22), 2114-22.
82. Signori, E.; Iurescia, S.; Massi, E.; Fioretti, D.; Chiarella, P.; De Robertis, M.; Rinaldi, M.; Tonon, G.; Fazio, V. M. DNA vaccination strategies for anti-tumour effective gene therapy protocols. Cancer Immunol. Immunother., 2010, 59(10), 1583-91.
83. Harrop, R.; John, J.; Carroll, M. W. Recombinant viral vectors: cancer vaccines. Adv. Drug Deliv. Rev., 2006, 58(8), 931-47. (Pubitemid 44709263)
84. USDA licenses DNA vaccine for treatment of melanoma in dogs. J. Am. Vet. Med. Assoc., 2010, 236(5), 495.
85. Peruzzi, D.; Mesiti, G.; Ciliberto, G.; La Monica, N.; Aurisicchio, L. Telomerase and HER-2/neu as targets of genetic cancer vaccines in dogs. Vaccine, 2010, 28(5), 1201-8.
86. Peruzzi, D.; Gavazza, A.; Mesiti, G.; Lubas, G.; Scarselli, E.; Conforti, A.; Bendtsen, C.; Ciliberto, G.; La Monica, N.; Aurisicchio, L. A vaccine targeting telomerase enhances survival of dogs affected by B-cell lymphoma. Mol. Ther., 2010, 18(8), 1559-67.
87. U.S. National institutes of health service. http://clinicaltrials.gov (Accessed March 9, 2011).
88. Tjelle, T. E.; Salte, R.; Mathiesen, I.; Kjeken, R. A novel electroporation device for gene delivery in large animals and humans. Vaccine, 2006, 24(21), 4667-70. (Pubitemid 43776760)
89. Low, L.; Mander, A.; McCann, K.; Dearnaley, D.; Tjelle, T.; Mathiesen, I.; Stevenson, F.; Ottensmeier, C. H. DNA vaccination with electroporation induces increased antibody responses in patients with prostate cancer. Hum. Gene Ther., 2009, 20(11), 1269-78.