Genetic immunization with plasmid DNA mediated by electrotransfer

Human Gene Therapy

Volumn 22, Issue 7, 2011, Pages 789-798

  Rochard, Alice ^a,b,c   Scherman, Daniel ^a,b,c   Bigey, Pascal ^a,b,c  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c PSL RESEARCH UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA VACCINE; IMMUNOLOGICAL ADJUVANT; NAKED DNA; PLASMID DNA;

AUTOIMMUNE DISEASE; CELLULAR IMMUNITY; DNA IMMUNIZATION; ELECTRIC FIELD; ELECTROPORATION; GENE EXPRESSION; GENETIC IMMUNIZATION; HUMAN; HUMORAL IMMUNITY; NEOPLASM; NONHUMAN; REVIEW; TARGET ORGAN; TRANSGENE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; AUTOIMMUNE DISEASES; CLINICAL TRIALS, PHASE I AS TOPIC; COMMUNICABLE DISEASES; DNA; ELECTROPORATION; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; IMMUNIZATION; NEOPLASMS; PLASMIDS; TRANSGENES; VACCINES, DNA;

EID: 79960345182     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2011.092     Document Type: Review

References (111)

1. Abdulhaqq, S.A., and Weiner, D.B. (2008). DNA vaccines: developing new strategies to enhance immune response. Immunol. Res. 42, 219-232.
2. Alexandrenne, C., Wijkhuisen, A., Dkhissi, F., et al. (2009). Generating antibodies against the native form of the human prion protein (hPrp) in wild-type animals: a comparison between DNA and protein immunizations. J. Immunol. Methods 341, 41-49.
3. Alexandrenne, C., Wijkhuisen, A., Dkhissi, F., et al. (2010). Electrotransfer of cDNA coding for a heterologous prion protein generates autoantibodies against native murine prion protein in wild-type mice. DNA Cell. Biol. 2010 29, 121-131.
4. Ashok, M.S., and Rangarajan, P.N. (2002). Protective efficacy of a plasmid DNA encoding Japanese encephalitis virus envelope protein fused to tissue plasminogen activator signal sequences: studies in a murine intracerebral virus challenge model. Vaccine 20, 1563-1570. (Pubitemid 34169796)
5. Babiuk, L.A., Pontarollo, R., Babiuk, S., et al. (2003). Induction of immune responses by DNA vaccines in large animals. Vaccine 21, 649-658. (Pubitemid 36091974)
6. Bachy, M., Boudet, F., Bureau, M., et al. (2001). Electric pulses increase the immunogenicity of an influenza DNA vaccine injected intramuscularly in the mouse Vaccine 19, 1688-1693. (Pubitemid 32175729)
7. Bei, R., and Scardino, A. (2010). TAA polyepitope DNA-based vaccines: a potential tool for cancer therapy. J. Biomed. Bio-technol. 2010, ID102758.
8. Bettan, M., Emmanuel, F., Darteil, R., et al. (2000). High-level protein secretion into blood circulation after electric pulse-mediated gene transfer into skeletal muscle. Mol. Ther. 2, 204-210.
9. Bian, C., Zhang, F., Wang, F., et al. (2010). Development of retinol-binding protein 4 immunocolloidal gold fast test strip using high-sensitivity monoclonal antibodies generated by DNA immunization. Acta Biochem. Biophys. Sin. 42, 847-853.
10. Bigey, P., Gnidehou, S., Dorichamou, J., et al. (2011). The NTS-DBL2X region of VAR2CSA induces cross-reactive antibodies that inhibit adhesion of several Plasmodium falciparum isolates to chondroitin-sulfate A. J. Infect. Dis., in press.
11. Bodles-Brakhop, A.M., Heller, R., and Draghia-Akli, R. (2009). Electroporation for the delivery of DNA-based vaccines and immunotherapeutics: current clinical developments. Mol. Ther. 17, 585-592.
12. Capone, S., Zampaglione, I., Vitelli, A., et al. (2006). Modulation of the immune response induced by gene electrotransfer of a hepatitis C virus DNA vaccine in nonhuman primates. J. Immunol. 177, 7462-7471. (Pubitemid 44715117)
13. Chen, A., Ahlén, G., Brenndörfer, E.D., et al. (2011). Hetero-logous T cells can help restore function in dysfunctional hepatitis C virus nonstructural 3/4A-specific T cells during therapeutic vaccination. J. Immunol. 186, 5107-5118.
14. Chen, M.W., Cheng, T.J., Huang, Y., et al. (2008). A consensus- hemagglutinin-based DNA vaccine that protects mice against divergent H5N1 influenza viruses. Proc. Natl. Acad. Sci. U.S.A. 105, 13538-13543.
15. Chen, Y., Zhang, T., Li, T., et al. (2005). Preparation and characterization of a monoclonal antibody against CKLF1 using DNA immunization with in vivo electroporation. Hybridoma 24, 305-308. (Pubitemid 41811149)
16. Chiarella, P., Massi, E., De Robertis, M., et al. (2008). Electro-poration of skeletal muscle induces danger signal release and antigen-presenting cell recruitment independently of DNA vaccine administration. Expert Opin. Biol. Ther. 8, 1645-1657.
17. Chua, K.Y., Ramos, J.D., and Cheong, N. (2008). Production of monoclonal antibody by DNA immunization with electro-poration. Methods Mol. Biol. 423, 509-520.
18. Chua, K.Y., Kuo, I.C., and Huang, C.H. (2009). DNA vaccines for the prevention and treatment of allergy. Curr. Opin. Allergy Clin. Immunol. 9, 50-54.
19. Curcio, C., Khan, A.S., Amici, A., et al. (2008). DNA immunization using constant-current electroporation affords long-term protection from autochthonous mammary carcinomas in cancer-prone transgenic mice. Cancer Gene Ther. 15, 108-114.
20. Dai, Y., Zhu, Y., Harn, D.A., et al. (2009). DNA vaccination by electroporation and boosting with recombinant proteins enhances the efficacy of DNA vaccines for Schistosomiasis japon-ica. Clin. Vaccine Immunol. 16, 1796-1803.
21. Daud, A.I., DeConti, R.C., Andrews, S., et al. (2008). Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma. J. Clin. Oncol. 26, 5896-5903.
22. Dobaño, C., Sedegah, M., Rogers, W.O., et al. (2009). Plasmo-dium: mammalian codon optimization of malaria plasmid DNA vaccines enhances antibody responses but not T cell responses nor protective immunity. Exp. Parasitol. 122, 112-123.
23. Donate, A., Coppola, D., Cruz, Y., and Heller, R. (2011). Evaluation of a novel non-penetrating electrode for use in DNA vaccination. PLoS One 6(4), e19181.
24. Doria-Rose, N.A., and Haigwood. N.L. (2003). DNA vaccine strategies: candidates for immune modulation and immunization regimens. Methods 31, 207-216. (Pubitemid 37162793)
25. Dupuy, L.C., Richards, M.J., Ellefsen, B., et al. (2011). A DNA vaccine for venezuelan equine encephalitis virus delivered by intramuscular electroporation elicits high levels of neutralizing antibodies in multiple animal models and provides protective immunity to mice and nonhuman primates. Clin. Vaccine Immunol. 18, 707-716.
26. Fissolo, N., Montalban, X., and Comabella, M. (2010). DNA-based vaccines for multiple sclerosis: Current status and future directions. Clin. Immunol. doi:10.1016/j.clim.2010.11.011
27. Foecking, M.K., and Hofstetter, H. (1986). Powerful and versatile enhancer/promoter unit for mammalian expression vectors. Gene 45, 101-105. (Pubitemid 17169237)
28. Frelin, L., Ahlen, G., Alheim, M., et al. (2004). Codon optimization and mRNA amplification effectively enhances the im-munogenicity of the hepatitis C virus nonstructural 3/4A gene. Gene Ther. 11, 522-533. (Pubitemid 38443519)
29. Geissler, M., Bruss, V., Michalak, S., et al. (1999). Intracellular retention of hepatitis B virus surface proteins reduces interleukin-2 augmentation after genetic immunizations. J. Virol. 73, 4284-4292. (Pubitemid 29189875)
30. Goldspink, G. (2003). Skeletal muscle as an artificial endocrine tissue. Best Pract. Res. Clin. Endocrinol. Metab. 17, 211-222.
31. Gothelf, A., and Gehl, J. (2010). Gene electrotransfer to skin; review of the existing literature and clinical perspectives. Curr. Gene Ther. 10, 287-299.
32. Gray, N.K., and Wickens, M. (1998). Control of translation initiation in animals. Annu. Rev. Cell. Dev. Biol. 14, 399-458. (Pubitemid 29001460)
33. Grønevik, E., Mathiesen, I., and Lømo, T. (2004). Early events of electroporation-mediated intramuscular DNA vaccination potentiate Th1-directed immune responses. J. Gene Med. 7, 1246-1254. (Pubitemid 41335176)
34. Haller, B.K., Bra°ve, A., Wallgard, E., et al. (2010). Therapeutic efficacy of a DNA vaccine targeting the endothelial tip cell antigen delta-like ligand 4 in mammary carcinoma. Oncogene 29, 4276-4286.
35. Harrison, R. A., and Bianco, A.E. (2000). DNA immunization with Onchocerca volvulus genes, Ov-tmy-1 and OvB20: sero-logical and parasitological outcomes following intramuscular or GeneGun delivery in a mouse model of onchocerciasis. Parasite Immunol. 22, 249-257. (Pubitemid 30261314)
36. Heller, L.C., and Heller, R. (2010). Electroporation gene therapy preclinical and clinical trials for melanoma. Curr. Gene Ther. 10, 312-317.
37. Heller, L.C., Ugen, K., and Heller, R. (2005). Electroporation for targeted gene transfer. Expert Opin. Drug. Deliv. 2, 255-268. (Pubitemid 41130881)
38. Hirao, L.A., Wu, L., Satishchandran, A., et al. (2010). Comparative analysis of immune responses induced by vaccination with SIV antigens by recombinant Ad5 vector or plasmid DNA in rhesus macaques. Mol. Ther. 18, 1568-1576.
39. Hirao, L.A., Draghia-Akli, R., Prigge, J.T., et al. (2011). Multi-valent smallpox DNA vaccine delivered by intradermal elec-troporation drives protective immunity in nonhuman primates against lethal monkeypox challenge. J. Infect. Dis. 203(1), 95-102.
40. Hojman, P. (2010). Basic principles and clinical advancements of muscle electrotransfer. Curr. Gene Ther. 10, 128-138.
41. Isagi, K., Kawase, A., Matono, M., et al. (2009). Enhanced CTL response by controlled intracellular trafficking of antigen in dendritic cells following DNA vaccination. J. Control. Release 135, 227-233.
42. Joseph-Pietras, D., Gao, Y., Zojer, N., et al. (2010). DNA vaccines to target the cancer testis antigen PASD1 in human multiple myeloma. Leukemia 24, 1951-1959.
43. Kim, C.Y., Kang, E.S., Kim, S.B., et al. (2008). Increased in vivo immunological potency of HB-110, a novel therapeutic HBV DNA vaccine, by electroporation. Exp. Mol. Med. 40, 669-676.
44. Kim, S.Y., Lee, J.H., Shin, H.S., et al. (2002). The human elongation factor 1 alpha (EF-1 alpha) first intron highly enhances expression of foreign genes from the murine cytomegalovirus promoter. J. Biotechnol. 93, 183-187.
45. Kirman, J.R., and Seder, R.A. (2003). DNA vaccination: the answer to stable, protective T-cell memory? Curr. Opin. Immunol. 15, 471-476. (Pubitemid 36930085)
46. Klinman D.M., Yamshchikov, G., and Ishigatsubo, Y. (1997). Contribution of CpG motifs to the immunogenicity of DNA vaccines. J. Immunol. 1997 158, 3635-3639. (Pubitemid 127488716)
47. Klinman, D.M., Klaschik, S., Sato, T., and Tross, D. (2009). CpG oligonucleotides as adjuvants for vaccines targeting infectious diseases. Adv. Drug. Deliv. Rev. 61, 248-255.
48. Kozak, M. (2002). Pushing the limits of the scanning mechanism for initiation of translation. Gene 299, 1-34. (Pubitemid 35379825)
49. Krieg, A.M. (2002). CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20, 709-760. (Pubitemid 34293438)
50. Kutzler, M.A., and Weiner, D.B. (2008). DNA vaccines: ready for prime time? Nat. Rev. Genet. 9, 776-788.
51. Laddy, D.J., Yan, J., Kutzler, M., et al. (2008). Heterosubtypic protection against pathogenic human and avian influenza viruses via in vivo electroporation of synthetic consensus DNA antigens. PLoS One 3(6), e2517.
52. LeBlanc, R., Vasquez, Y., Hannaman, D., and Kumar, N. (2008). Markedly enhanced immunogenicity of a Pfs25 DNA-based malaria transmission-blocking vaccine by in vivo electro-poration. Vaccine 26, 185-192. (Pubitemid 350266127)
53. Lee, A.H., Suh, Y.S., Sung, J.H., et al. (1997). Comparison of various expression plasmids for the induction of immune response by DNA immunization. Mol. Cells 7, 495-501. (Pubitemid 127476205)
54. Liang, P.H., Zhang, K.Q., Xu, G.L., et al. (2010). Construction of a DNA vaccine encoding Flk-1 extracellular domain and C3d fusion gene and investigation of its suppressing effect on tumor growth. Cancer Immunol. Immunother. 59, 93-101.
55. Liu, J., Kjeken, R., Mathiesen, I., and Barouch, D. (2008). Recruitment of antigen-presenting cells to the site of inoculation and augmentation of human immunodeficiency virus type 1 DNA vaccine immunogenicity by in vivo electroporation. J. Virol. 82, 5643-5649. (Pubitemid 351705271)
56. Liu, M.A. (2010). Immunologic basis of vaccine vectors. Immunity 33, 504-515.
57. Liu, M.A. (2011). DNA vaccines: an historical perspective and view to the future. Immunol. Rev. 239, 62-84.
58. Livingston, B.D., Little, S.F., Luxembourg, A., et al. (2010). Comparative performance of a licensed anthrax vaccine versus electroporation based delivery of a PA encoding DNA vaccine in rhesus macaques. Vaccine 28, 1056-1061.
59. Lladser, A., Ljungberg, K., Tufvesson, H., et al. (2010). In-tradermal DNA electroporation induces surviving-specific CTLs, suppresses angiogenesis and confers protection against mouse melanoma. Cancer Immunol. Immunother. 59, 81-92.
60. Low, L., Mander, A., McCann, K., et al. (2009). DNA vaccination with electroporation induces increased antibody responses in patients with prostate cancer. Hum. Gene Ther. 20, 1269-1278.
61. Lu, Q.L., Bou-Gharios, G., and Partridge, T.A. (2003). Non-viral gene delivery in skeletal muscle: a protein factory. Gene Ther. 10, 131-142. (Pubitemid 36582585)
62. Luckay, A., Sidhu, M.K., Kjeken, R., et al. (2007). Effect of plas-mid DNA vaccine design and in vivo electroporation on the resulting vaccine-specific immune responses in rhesus macaques. J. Virol. 81, 5257-5269. (Pubitemid 46744435)
63. Makrides, S.C. (2003). Vectors for gene expression in mammalian cells. New Comprehensive Biochem. 38, 9-26.
64. Mallilankaraman, K., Shedlock, D.J., Bao, H., et al. (2011). A DNA vaccine against chikungunya virus is protective in mice and induces neutralizing antibodies in mice and nonhuman primates. PLoS Negl. Trop. Dis. 5, e928.
65. Mariana, I., Kawalekar, O., Shedlock, D.J., et al. (2010). DNA vaccines for targeting bacterial infections. Expert Rev. Vaccines 9, 747-763.
66. Marino, M., Scuderi, F., Provenzano, C., and Bartoccioni, E. (2011). Skeletal muscle cells: from local inflammatory response to active immunity. Gene Ther. 18, 109-116.
67. Martinon, F., Kaldma, K., Sikut, R., et al. (2009). Persistent immune responses induced by a human immunodeficiency virus DNA vaccine delivered in association with electroporation in the skin of nonhuman primates. Hum. Gene Ther. 20, 1291-1307.
68. Miller, M., Rekas, G., Dyball, K., et al. (2004). The efficacy of electroporated plasmid vaccines correlates with long-term antigen production in vivo. Vaccine 22, 2517-2523. (Pubitemid 38757354)
69. Mir, L.M., and Orlowski, S. (1999). Mechanisms of electro-chemotherapy. Adv. Drug Deliv. Rev. 35, 107-118.
70. Mir, L.M., Bureau, M.F., Gehl, J., et al. (1999). High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc. Natl. Acad. Sci. U. S. A. 96, 4262-4267. (Pubitemid 29190324)
71. Muthumani, G., Laddy, D.J., Sundaram, S.G., et al. (2009). Co-immunization with an optimized plasmid-encoded immune stimulatory interleukin, high-mobility group box 1 protein, results in enhanced interferon-gamma secretion by antigen-specific CD8 T cells. Immunology 128(Suppl 1):e612-620.
72. Nicolas, J.F., and Guy, B. (2008). Intradermal, epidermal and transcutaneous vaccination: from immunology to clinical practice. Expert Rev. Vaccines 7, 1201-1214.
73. Neumann, E., Schaefer-Ridder, M., Wang, Y., and Hofschneider, P.H. (1982). Gene transfer into mouse lyoma cells by electro-poration in high electric fields. EMBO J. 1, 841-845.
74. Nyström, J., Chen, A., Frelin, L., et al. (2010). Improving on the ability of endogenous hepatitis B core antigen to prime cyto-toxic T lymphocytes. J. Infect. Dis. 201, 1867-1879.
75. O'Hagan, D.T., Singh, M., and Ulmer, J.B. (2006). Microparticles based technologies for vaccines. Methods 40, 10-19.
76. Ohkawara, T., Koyama, Y., Onodera, S., et al. (2011). DNA vaccination targeting macrophage migration inhibitory factor prevents murine experimental colitis. Clin. Exp. Immunol. 163, 113-122.
77. Okahara, F., Itoh, K., Ebihara, M., et al. (2005). Production of research grade antibody by in vivo electroporation of DNA-encoding target protein. Anal. Biochem. 336, 138-140. (Pubitemid 39593511)
78. Orlandi, F., Guevara-Patiño, J.A., Merghoub, T., et al. (2011). Combination of epitope-optimized DNA vaccination and passive infusion of monoclonal antibody against HER2/neu leads to breast tumor regression in mice. Vaccine 29, 3646-3654.
79. Otten, G., Schaefer, M., Doe, B., et al. (2004). Enhancement of DNA vaccine potency in rhesus macaques by electroporation. Vaccine 22, 2489-2493. (Pubitemid 38757348)
80. Perez, N., Bigey, P., Scherman, D., et al. (2004). Regulatable systemic production of monoclonal antibodies by in vivo muscle electroporation. Genet. Vaccines Ther. 2, 2.
81. Peruzzi, D., Mori, F., Conforti, A., et al. (2009). MMP11: a novel target antigen for cancer immunotherapy. Clin. Cancer Res. 15, 4104-4113.
82. Peruzzi, D., Gavazza, A., Mesiti, G., et al. (2010). A vaccine targeting telomerase enhances survival of dogs affected by B-cell lymphoma. Mol. Ther. 18, 1559-1567.
83. Prud'homme, G.J., Draghia-Akli, R., and Wang, Q. (2007). Plasmid-based gene therapy of diabetes mellitus. Gene Ther. 14, 553-564. (Pubitemid 46444529)
84. Rice, J., Ottensmeier, C.H., and Stevenson, F.K. (2008). DNA vaccines: precision tools for activating effective immunity against cancer. Nat. Rev. Cancer. 8, 108-120. (Pubitemid 351161331)
85. Rolla, S., Ria, F., Occhipinti, S., et al. (2010). Erbb2 DNA vaccine combined with regulatory T cell deletion enhances antibody response and reveals latent low-avidity T cells: potential and limits of its therapeutic efficacy. J. Immunol. 184, 6124-6132.
86. Rottinghaus, S.T., Poland, G.A., Jacobson, R.M., et al. (2003). Hepatitis B DNA vaccine induces protective antibody responses in human non-responders to conventional vaccination. Vaccine 21, 4604-4608. (Pubitemid 37315782)
87. Ruffini, P.A., Grødeland, G., Fredriksen, A.B., and Bogen, B. (2010). Human chemokine MIP1a increases efficiency of targeted DNA fusion vaccines. Vaccine 29, 191-199.
88. Sardesai, N.Y., and Weiner, D.B. (2011). electroporation delivery of DANN vaccines: prospects for success. Curr. Opin. Immunol. doi:10.1016/j.coi.2011. 03.008.
89. Scheerlinck, J.P., Karlis, J., Tjelle, T.E., et al. (2004). In vivo elec-troporation improves immune responses to DNA vaccination in sheep. Vaccine 22, 1820-1825. (Pubitemid 38447230)
90. Shedlock, D.J., Talbott, K.T., Cress, C., et al. (2011). A highly optimized DNA vaccine confers complete protective immunity against high-dose lethal lymphocytic chor-iomeningitis virus challenge. Vaccine doi:10.1016/j.vaccine.2010.12.064.
91. Shimada, M., Yoshizaki, S., Jounai, N., et al. (2010). DNA vaccine expressing HIV-1 gp120/immunoglobulin fusion protein enhances cellular immunity. Vaccine 28, 4920-4927.
92. Stevenson, F.K., Ottensmeier, C.H., and Rice, J. (2010). DNA vaccines against cancer come of age. Curr. Opin. Immunol. 22, 264-270.
93. Tang, D.C., DeVit, M., and Johnston, S.A. (1992). Genetic immunization is a simple method for eliciting an immune response. Nature 356, 152-154.
94. Trollet, C., Bloquel, C., Scherman, D., and Bigey, P. (2006). Electrotransfer into skeletal muscle for protein expression. Curr. Gene Ther. 6, 561-578. (Pubitemid 44524460)
95. Trollet, C., Scherman, D., and Bigey, P. (2008). Delivery of DNA into muscle for treating systemic diseases: advantages and challenges. Methods Mol. Biol. 423, 199-214.
96. Trollet, C., Pereira, Y., Burgain, A., et al. (2009). Generation of high-titer neutralizing antibodies against botulinum toxins A, B, and E by DNA electrotransfer. Infect. Immun. 77, 2221-2229.
97. Tsang, C., Babiuk, S., Van Drunen Littel-van den Hurk, S., et al. (2007). A single DNA immunization in combination with electroporation prolongs the primary immune response and maintains immune memory for six months. Vaccine 25, 5485-5494. (Pubitemid 47039264)
98. Ulmer, J.B., Donnelly, J.J., Parker, S.E., et al. (1993). Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 259, 1745-1749 (Pubitemid 23114660)
99. Van den Berg, J.H., Nujien, B., Beijnen, J.H., et al. (2009). Optimization of intradermal vaccination by DNA tattooing in human skin. Hum. Gene Ther. 20, 181-189.
100. Vandermeulen, G, Staes, E., Vanderhaeghen, M.L, et al. (2007). Optimisation of intradermal DNA electrotransfer for immunisation. J. Control. Release 124, 81-87. (Pubitemid 350088207)
101. Van Drunen Littel-van den Hurk, S., Babiuk, S.L., and Babiuk, L.A. (2004). Strategies for improved formulation and delivery of DNA vaccines to veterinary target species. Immunol. Rev. 199, 113-125. (Pubitemid 38744520)
102. Van Drunen Littel-van den Hurk, S., Lawman, Z., Wilson, D., et al. (2010). Electroporation enhances immune responses and protection induced by a bovine viral diarrhea virus DNA vaccine in newborn calves with maternal antibodies. Vaccine 28, 6445-6454.
103. Widera, G., Austin, M., Rabussay, D., et al. (2000). Increased DNA vaccine delivery and immunogenicity by electropora-tion in vivo. J. Immunol. 164, 4635-4640. (Pubitemid 30238062)
104. Xu, G.L., Zhang, K.Q., Guo, B., et al. (2010). Induction of protective and therapeutic antitumor immunity by a DNA vaccine with C3d as a molecular adjuvant. Vaccine 28, 7221-7227.
105. Xue, H., Liang, F., Liu, N., et al. (2011). Potent antirheumatic activity of a new DNA vaccine targeted to B7-2/CD28 costi-mulatory signaling pathway in autoimmune arthritis. Hum. Gene Ther. 22, 65-76.
106. Yamaoka, A., Guan, X., Takemoto, S., et al. (2010). Development of a novel Hsp70-based DNA vaccine as a multifunctional antigen delivery system. J. Control. Release 142, 41141-41145.
107. Yang, L., Cheong, N., Wang, D.Y., et al. (2003). Generation of monoclonal antibodies against Blo t 3 using DNA immunization with in vivo electroporation. Clin. Exp. Allergy 33, 663-668. (Pubitemid 36629692)
108. Yin, J., Dai, A., Lecureux, J., et al. (2010). High antibody and cellular responses induced to HIV-1 clade C envelope following DNA vaccines delivered by electroporation. Vaccine doi:10.1016/j.vaccine.2010.12.055.
109. Yu, W.Y., Chuang, T.F., Guichard, C., et al. (2011). Chicken HSP70 DNA vaccine inhibits tumor growth in a canine cancer model. Vaccine 29, 3489-3500.
110. Zheng, L., Wang, F., Yang, Z., et al. (2009). A single immunization with HA DNA vaccine by electroporation induces early protection against H5N1 avian influenza virus challenge in mice. BMC Infect. Dis. 9:17.
111. Zhu, Y., Lu, F., Dai, Y., et al. (2010). Synergistic enhancement of immunogenicity and protection in mice against Schistosoma japonicum with codon optimization and electroporation delivery of SjTPI DNA vaccines. Vaccine 28, 5347-5355.