Molecular delivery of plasmids for genetic vaccination

Current Pharmaceutical Biotechnology

Volumn 14, Issue 6, 2013, Pages 615-622

  Mazid, Romiza ^a   Tan, Melvin X ^a   Danquah, Michael K ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b CURTIN UNIVERSITY   (Australia)

Author keywords

Clinical trial; Immunology; Plasmid; Polymer; Vaccine

Indexed keywords

APEX; CHITOSAN; DNA VACCINE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; LIFETIDE SW5; NANOPARTICLE; ONCEPT; POLYGLACTIN; UNCLASSIFIED DRUG; WEST NILE INNOVATOR;

ABSENCE OF SIDE EFFECTS; ANTIGEN PRESENTING CELL; ARTICLE; ELECTROPORATION; ENCAPSULATION; GENETIC IMMUNIZATION; GENETIC TRANSFECTION; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; INFECTIOUS HEMATOPOIETIC NECROSIS; INFECTIOUS PANCREATIC NECROSIS VIRUS; MELANOMA; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); WEST NILE FEVER;

ANIMALS; DNA; GENE TRANSFER TECHNIQUES; HUMANS; PLASMIDS; POLYMERS; VACCINATION; VACCINES, DNA;

EID: 84888265601     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920101131400226     Document Type: Article

References (115)

1. Fricke, J.; Pohlmann, K.; Tatge, F.; Lang, R.; Faber, B.; Luttmann, R., A multi-bioreactor system for optimal production of malaria vaccines with Pichia pastoris. Biotechnol. J., 2011, 6 (4), 437-451.
2. Porter, D. W.; Thompson, F. M.; Berthoud, T. K.; Hutchings, C. L.; Andrews, L.; Biswas, S.; Poulton, I.; Prieur, E.; Correa, S.; Rowland, R.; Lang, T.; Williams, J.; Gilbert, S. C.; Sinden, R. E.; Todryk, S.; Hill, A. V., A human Phase I/IIa malaria challenge trial of a polyprotein malaria vaccine. Vaccine, 2011, 29, 7514-22.
3. Danquah, M. K.; Liu, S.; Ho, J.; Forde, G. M.; Wang, L.; Coppel, R. L., Rapid production of a plasmid DNA encoding a malaria vaccine candidate via amino-functionalized poly(GMA-co-EDMA) monolith. AIChE J., 2008, 54 (11), 2990-2998.
4. Corey, L.; Nabel, G. J.; Dieffenbach, C.; Gilbert, P.; Haynes, B. F.; Johnston, M.; Kublin, J.; Lane, H. C.; Pantaleo, G.; Picker, L. J.; Fauci, A. S., HIV-1 Vaccines and Adaptive Trial Designs. Sci. Transl. Med., 2011, 3 (79), 79ps13.
5. Porichis, F.; Kaufmann, D. E., HIV-specific CD4 T cells and immune control of viral replication. Curr. Opin. HIV AIDS, 2011, 6 (3), 174-180.
6. Blanco, J. C.; Boukhvalova, M. S.; Shirey, K. A.; Prince, G. A.; Vogel, S. N., New insights for development of a safe and protective RSV vaccine. Hum. Vaccin., 2010, 6 (6), 482-492.
7. Groothuis, J. R.; Hoopes, J. M.; Jessie, V. G., Prevention of serious respiratory syncytial virus-related illness. I: Disease pathogenesis and early attempts at prevention. Adv. Ther., 2011, 28 (2), 91-109.
8. Seale, H.; Kaur, R.; Wang, Q.; Yang, P.; Zhang, Y.; Wang, X.; Li, X.; Zhang, H.; Zhang, Z.; MacIntyre, C. R., Acceptance of a vaccine against pandemic influenza A (H1N1) virus amongst healthcare workers in Beijing, China. Vaccine, 2011, 29 (8), 1605-1610.
9. Shoji, Y.; Chichester, J. A.; Jones, M.; Manceva, S. D.; Damon, E.; Mett, V.; Musiychuk, K.; Bi, H.; Farrance, C.; Shamloul, M.; Kushnir, N.; Sharma, S.; Yusibov, V., Plant-based rapid production of recombinant subunit hemagglutinin vaccines targeting H1N1 and H5N1 influenza. Hum. Vaccin., 2011, 7, 41-50.
10. Chai, J. G., Cancer vaccination reprograms regulatory T cells into helper CD4 T cells to promote antitumor CD8 T-cell responses. Immunotherapy, 2011, 3 (5), 601-604.
11. Mansour, M., Next generation of therapeutic cancer vaccines require smart vaccine design. Hum Vaccin 2010, 6 (12), 959-61.
12. Sasada, T.; Itoh, K., [Current status and future perspective of cancer vaccine development]. Gan To Kagaku Ryoho, 2011, 38 (4), 503-508.
13. Alpar, H. O.; Papanicolaou, I.; Bramwell, V. W., Strategies for DNA vaccine delivery. Expert. Opin. Drug Deliv., 2005, 2 (5), 829-842.
14. Xiang, S. D.; Selomulya, C.; Ho, J.; Apostolopoulos, V.; Plebanski, M., Delivery of DNA vaccines: an overview on the use of biodegradable polymeric and magnetic nanoparticles. Wiley Interdiscip Rev. Nanomed Nanobiotechnol., 2010, 2 (3), 205-218.
15. Wolff, J. A.; Malone, R. W.; Williams, P.; Chong, W.; Acsadi, G.; Jani, A.; Felgner, P. L., Direct gene transfer into mouse muscle in vivo. Science, 1990, 247 (4949 Pt 1), 1465-1468.
16. Shedlock, D. J.; Weiner, D. B., DNA vaccination: antigen presentation and the induction of immunity. J. Leukoc. Biol., 2000, 68 (6), 793-806.
17. Donnelly, U. J. B. a. L.M.A., Immunization with polynucleotides: A novel approach to vaccination. The Immunologist, 1993, 2, 22-26.
18. Kawabata, K.; Takakura, Y.; Hashida, M., The fate of plasmid DNA after intravenous injection in mice: involvement of scavenger receptors in its hepatic uptake. Pharm. Res., 1995, 12 (6), 825-830.
19. Lewis, P. J.; Babiuk, L. A., DNA vaccines: a review. Adv. Virus Res., 1999, 54, 129-188.
20. Luten, J.; van Nostrum, C. F.; De Smedt, S. C.; Hennink, W. E., Biodegradable polymers as non-viral carriers for plasmid DNA delivery. J. Control Release, 2008, 126 (2), 97-110.
21. Pack, D. W.; Hoffman, A. S.; Pun, S.; Stayton, P. S., Design and development of polymers for gene delivery. Nat. Rev. Drug Discov., 2005, 4 (7), 581-593.
22. Gregoriadis, G., DNA vaccines: a role for liposomes. Curr. Opin. Mol. Ther., 1999, 1 (1), 39-42.
23. Gregoriadis, G.; Bacon, A.; Caparros-Wanderley, W.; McCormack, B., A role for liposomes in genetic vaccination. Vaccine, 2002, 20 Suppl 5, B1-B9.
24. Kataoka, K.; Harada, A.; Nagasaki, Y., Block copolymer micelles for drug delivery: design, characterization and biological significance. Adv. Drug Del. Rev., 2001, 47 (1), 113-131.
25. Torchilin, V. P., Targeted polymeric micelles for delivery of poorly soluble drugs. Cellular Mol. Life Sci., 2004, 61 (19), 2549-2559.
26. Singh, A.; Suri, S.; Roy, K., In-situ crosslinking hydrogels for combinatorial delivery of chemokines and siRNA-DNA carrying microparticles to dendritic cells. Biomaterials, 2009, 30 (28), 5187-5200.
27. Toussaint, J. F.; Dubois, A.; Dispas, M.; Paquet, D.; Letellier, C.; Kerkhofs, P., Delivery of DNA vaccines by agarose hydrogel implants facilitates genetic immunization in cattle. Vaccine, 2007, 25 (7), 1167-1174.
28. Noh, S. M.; Kim, W.-K.; Kim, S. J.; Kim, J. M.; Baek, K.-H.; Oh, Y.-K., Enhanced cellular delivery and transfection efficiency of plasmid DNA using positively charged biocompatible colloidal gold nanoparticles. Biochimica et Biophysica Acta (BBA)-General Subjects, 2007, 1770 (5), 747-752.
29. Edelstein, M. L.; Abedi, M. R.; Wixon, J., Gene therapy clinical trials worldwide to 2007--an update. J. Gene Med., 2007, 9 (10), 833-842.
30. Edelstein, M. L.; Abedi, M. R.; Wixon, J.; Edelstein, R. M., Gene therapy clinical trials worldwide 1989-2004-an overview. J. Gen. Med., 2004, 6 (6), 597-602.
31. Bhavsar, M. D.; Amiji, M. M., Polymeric nano-and microparticle technologies for oral gene delivery. Exp. Opin. Drug Deliv., 2007, 4 (3), 197-213.
32. Ho, J.; Danquah, M.; Huang, Y.; Liu, S., The Role of Colloidal Delivery Systems in DNA Genetic Therapeutics. In Colloids in Biotechnology, CRC Press: 2010; pp 177-196.
33. Wu, G. Y.; Wu, C. H., Receptor-mediated gene delivery and expression in vivo. J. Biol. Chem., 1988, 263 (29), 14621-14624.
34. Nguyen, D. N.; Raghavan, S. S.; Tashima, L. M.; Lin, E. C.; Fredette, S. J.; Langer, R. S.; Wang, C., Enhancement of poly(orthoester) microspheres for DNA vaccine delivery by blending with poly(ethylenimine). Biomaterials, 2008, 29(18), 2783-2793.
35. Wagner, E.; Ogris, M.; Zauner, W., Polylysine-based transfection systems utilizing receptor-mediated delivery. Adv. Drug Deliv. Rev., 1998, 30 (1-3), 97-113.
36. Godbey, W. T.; Wu, K. K.; Mikos, A. G., Poly(ethylenimine) and its role in gene delivery. J. Control Release, 1999, 60 (2-3), 149-160.
37. Boussif, O.; Lezoualc'h, F.; Zanta, M.A.; Mergny, M.D.; Scherman, D.; Demeneix, B.; Behr, J.P., A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. USA, 1995, 92 (16), 7297-7301.
38. Fischer, D.; Bieber, T.; Li, Y.; Elsässer, H.-P.; Kissel, T., A Novel Non-Viral Vector for DNA Delivery Based on Low Molecular Weight, Branched Polyethylenimine: Effect of Molecular Weight on Transfection Efficiency and Cytotoxicity. Pharmaceut. Res.,1999, 16 (8), 1273-1279.
39. Schipper, N. G.; Varum, K. M.; Artursson, P., Chitosans as absorption enhancers for poorly absorbable drugs. 1: Influence of molecular weight and degree of acetylation on drug transport across human intestinal epithelial (Caco-2) cells. Pharm. Res., 1996, 13 (11), 1686-1692.
40. He, P.; Davis, S. S.; Illum, L., In vitro evaluation of the mucoadhesive properties of chitosan microspheres. Int. J. Pharmaceut. 1998, 166 (1), 75-88.
41. MacLaughlin, F. C.; Mumper, R. J.; Wang, J.; Tagliaferri, J. M.; Gill, I.; Hinchcliffe, M.; Rolland, A. P., Chitosan and depolymerized chitosan oligomers as condensing carriers for in vivo plasmid delivery. J. Controlled Rel., 1998, 56 (1-3), 259-272.
42. Esfand, R.; Tomalia, D. A., Poly(amidoamine) (PAMAM) dendrimers: from biomimicry to drug delivery and biomedical applications. Drug Discov. Today, 2001, 6 (8), 427-436.
43. Capan, Y.; Woo, B. H.; Gebrekidan, S.; Ahmed, S.; DeLuca, P. P., Preparation and Characterization of Poly (D, L-Lactide-Co-Glycolide) Microspheres for Controlled Release of Poly(L-Lysine) Complexed Plasmid DNA. Pharmaceut. Res., 1999, 16 (4), 509-513.
44. Lunsford, L.; McKeever, U.; Eckstein, V.; Hedley, M., Tissue Distribution and Persistence in Mice of Plasmid DNA Encapsulated in a PLGA-Based Microsphere Delivery Vehicle. J. Drug Targeting, 2000, 8 (1), 39-50.
45. Jilek, S.; Merkle, H. P.; Walter, E., DNA-loaded biodegradable microparticles as vaccine delivery systems and their interaction with dendritic cells. Adv. Drug Deliv. Rev., 2005, 57 (3), 377-390.
46. Lu, Y.; Ouyang, K.; Fang, J.; Zhang, H.; Wu, G.; Ma, Y.; Zhang, Y.; Hu, X.; Jin, L.; Cao, R.; Fan, H.; Li, T.; Liu, J., Improved efficacy of DNA vaccination against prostate carcinoma by boosting with recombinant protein vaccine and by introduction of a novel adjuvant epitope. Vaccine, 2009, 27 (39), 5411-5418.
47. Walter, E.; Dreher, D.; Kok, M.; Thiele, L.; Kiama, S. G.; Gehr, P.; Merkle, H. P., Hydrophilic poly(DL-lactide-co-glycolide) microspheres for the delivery of DNA to human-derived macrophages and dendritic cells. J. Control Release, 2001, 76 (1-2), 149-68.
48. Wang, C.; Ge, Q.; Ting, D.; Nguyen, D.; Shen, H. R.; Chen, J.; Eisen, H. N.; Heller, J.; Langer, R.; Putnam, D., Molecularly engineered poly(ortho ester) microspheres for enhanced delivery of DNA vaccines. Nat. Mater., 2004, 3 (3), 190-196.
49. Hui Rong, S.; Brian, B.; Steve, N.; Devang, S.; Jorge, H.; John, B., Poly(ortho Esters). In Scaffolding in Tissue Engineering, CRC Press: 2005; pp 91-108.
50. Heller, J.; Barr, J., Poly(ortho esters)--from concept to reality. Biomacromolecules, 2004, 5 (5), 1625-1632.
51. Heller, J.; Barr, J.; Ng, S. Y.; Abdellauoi, K. S.; Gurny, R., Poly(ortho esters): synthesis, characterization, properties and uses. Adv. Drug Deliv. Rev., 2002, 54 (7), 1015-1039.
52. Bailey, E. E., KoleskeJ. V, Alkylene Oxides and Their Polymers Marcel Dekker: New York, 1991; Vol. 35.
53. Huang, F. W.; Wang, H. Y.; Li, C.; Wang, H. F.; Sun, Y. X.; Feng, J.; Zhang, X. Z.; Zhuo, R. X., PEGylated PEI-based biodegradable polymers as non-viral gene vectors. Acta Biomater., 2010, 6 (11), 4285-4295.
54. Wortmann, A.; Vohringer, S.; Engler, T.; Corjon, S.; Schirmbeck, R.; Reimann, J.; Kochanek, S.; Kreppel, F., Fully detargeted polyethylene glycol-coated adenovirus vectors are potent genetic vaccines and escape from pre-existing anti-adenovirus antibodies. Mol. Ther., 2008, 16 (1), 154-162.
55. Ahlin Grabnar, P.; Kristl, J., The manufacturing techniques of drug-loaded polymeric nanoparticles from preformed polymers. J. Microencapsul., 2011, 28 (4), 323-335.
56. Rao, J. P.; Geckeler, K. E., Polymer nanoparticles: Preparation techniques and size-control parameters. Progress Polym. Sci., 2011, 36 (7), 887-913.
57. Alarcon, J. B.; Waine, G. W.; McManus, D. P., DNA Vaccines: Technology and Application as Anti-parasite and Anti-microbial Agents. In Adv. Parasitol., J.R. Baker, R. M.; Rollinson, D., Eds. Academic Press: 1999; Vol. Volume 42, pp 343-410.
58. Davis, H. L.; Whalen, R. G.; Demeneix, B. A., Direct gene transfer into skeletal muscle in vivo: factors affecting efficiency of transfer and stability of expression. Hum. Gene Ther., 1993, 4 (2), 151-159.
59. Davis, H. L.; Michel, M. L.; Mancini, M.; Schleef, M.; Whalen, R. G., Direct gene transfer in skeletal muscle: plasmid DNA-based immunization against the hepatitis B virus surface antigen. Vaccine, 1994, 12 (16), 1503-1509.
60. Pouton, C. W.; Seymour, L. W., Key issues in non-viral gene delivery. Adv. Drug Deliv. Rev., 2001, 46 (1-3), 187-203.
61. Bos, J. D., The skin as an organ of immunity. Clin. Exp. Immunol., 1997, 107 Suppl 1, 3-5.
62. Condon, C.; Watkins, S. C.; Celluzzi, C. M.; Thompson, K.; Falo, L. D., Jr., DNA-based immunization by in vivo transfection of dendritic cells. Nat. Med., 1996, 2 (10), 1122-1128.
63. Fynan, E. F.; Webster, R. G.; Fuller, D. H.; Haynes, J. R.; Santoro, J. C.; Robinson, H. L., DNA vaccines: protective immunizations by parenteral, mucosal, and gene-gun inoculations. Proc. Natl. Acad., Sci. USA, 1993, 90 (24), 11478-11482.
64. Webster, R. G.; Fynan, E. F.; Santoro, J. C.; Robinson, H., Protection of ferrets against influenza challenge with a DNA vaccine to the haemagglutinin. Vaccine, 1994, 12 (16), 1495-1498.
65. Yang, N. S.; Burkholder, J.; Roberts, B.; Martinell, B.; McCabe, D., In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment. Proc. Natl. Acad. Sci. USA, 1990, 87 (24), 9568-9572.
66. Ciernik, I. F.; Krayenbuhl, B. H.; Carbone, D. P., Puncture-mediated gene transfer to the skin. Hum. Gene Ther., 1996, 7 (8), 893-899.
67. Sardesai, N. Y.; Weiner, D. B., Electroporation delivery of DNA vaccines: prospects for success. Curr. Opin. Immunol., 2011, 23 (3), 421-429.
68. 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.
69. Holmgren, J.; Czerkinsky, C., Mucosal immunity and vaccines. Nat. Med., 2005, 11 (4 Suppl), S45-S53.
70. Alpar, H. O.; Ozsoy, Y.; Bowen, J.; Eyles, J. E.; Conway, B. R.; Williamson, E. D., Potential of particulate carriers for the mucosal delivery of DNA vaccines. Biochem. Soc. Trans., 1997, 25 (2), 337S.
71. Etchart, N.; Buckland, R.; Liu, M. A.; Wild, T. F.; Kaiserlian, D., Class I-restricted CTL induction by mucosal immunization with naked DNA encoding measles virus haemagglutinin. J. Gen. Virol. 1997, 78 (Pt 7), 1577-1580.
72. Goyal, A. K.; Khatri, K.; Mishra, N.; Vyas, S. P., New patents on mucosal delivery of vaccines. Exp. Opin. Therap. Patents, 2008, 18 (11), 1271-1288.
73. Asakura, Y.; Hinkula, J.; Leandersson, A. C.; Fukushima, J.; Okuda, K.; Wahren, B., Induction of HIV-1 Specific Mucosal Immune Responses by DNA Vaccination. Scand. J. Immunol., 1997, 46 (4), 326-330.
74. Alpar, H. O.; Somavarapu, S.; Atuah, K. N.; Bramwell, V. W., Biodegradable mucoadhesive particulates for nasal and pulmonary antigen and DNA delivery. Adv. Drug Delivery Rev., 2005, 57 (3), 411-430.
75. Estes, M. K.; Ball, J. M.; Crawford, S. E.; O'Neal, C.; Opekun, A. A.; Graham, D. Y.; Conner, M. E., Virus-like particle vaccines for mucosal immunization. Adv. Exp. Med. Biol., 1997, 412, 387-395.
76. Toebe, C. S.; Clements, J. D.; Cardenas, L.; Jennings, G. J.; Wiser, M. F., Evaluation of immunogenicity of an oral Salmonella vaccine expressing recombinant Plasmodium berghei merozoite surface protein-1. Am. J. Trop. Med. Hyg., 1997, 56 (2), 192-199.
77. Jones, D. H.; Corris, S.; McDonald, S.; Clegg, J. C.; Farrar, G. H., Poly(DL-lactide-co-glycolide)-encapsulated plasmid DNA elicits systemic and mucosal antibody responses to encoded protein after oral administration. Vaccine, 1997, 15 (8), 814-817.
78. Jones, D. H.; Partidos, C. D.; Steward, M. W.; Farrar, G. H., Oral delivery of poly(lactide-co-glycolide) encapsulated vaccines. Behring Inst. Mitt., 1997, (98), 220-228.
79. O'Hagan, D. T.; Singh, M.; Ulmer, J. B., Microparticle-based technologies for vaccines. Methods, 2006, 40 (1), 10-19.
80. Venkatesan, N.; Vyas, S. P., Polysaccharide coated liposomes for oral immunization--development and characterization. Int. J. Pharm., 2000, 203 (1-2), 169-177.
81. Neutra, M. R.; Kozlowski, P. A., Mucosal vaccines: the promise and the challenge. Nat. Rev. Immunol., 2006, 6 (2), 148-158.
82. Davis, S. S., Nasal vaccines. Adv Drug Deliv Rev 2001, 51 (1-3), 21-42.
83. Partidos, C. D., Intranasal vaccines: forthcoming challenges. Pharm. Sci. Technol. Today, 2000, 3 (8), 273-281.
84. Klavinskis, L. S.; Barnfield, C.; Gao, L.; Parker, S., Intranasal immunization with plasmid DNA-lipid complexes elicits mucosal immunity in the female genital and rectal tracts. J. Immunol., 1999, 162 (1), 254-262.
85. Mestecky, J.; McGhee, J. R., Immunoglobulin A (IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response. Adv. Immunol., 1987, 40, 153-245.
86. Boyaka, P. N.; Tafaro, A.; Fischer, R.; Fujihashi, K.; Jirillo, E.; McGhee, J. R., Therapeutic manipulation of the immune system: enhancement of innate and adaptive mucosal immunity. Curr. Pharm. Des., 2003, 9 (24), 1965-1972.
87. Davis, S. S.; Illum, L., Absorption enhancers for nasal drug delivery. Clin. Pharmacokinet., 2003, 42 (13), 1107-1128.
88. Di Colo, G.; Zambito, Y.; Zaino, C., Polymeric enhancers of mucosal epithelia permeability: synthesis, transepithelial penetration-enhancing properties, mechanism of action, safety issues. J. Pharm. Sci., 2008, 97 (5), 1652-1680.
89. Vila., A.; Sanchez., A.; Perez., C.; Alonso., M. J., PLA-PEG Nanospheres: New carriers for Transmucosal Delivery of Proteins and Plasmid DNA. Polym. Adv. Technol., 2002, 13, 851-858.
90. Harcourt, J. L.; Anderson, L. J.; Sullender, W.; Tripp, R. A., Pulmonary delivery of respiratory syncytial virus DNA vaccines using macroaggregated albumin particles. Vaccine, 2004, 22 (17-18), 2248-2260.
91. Lombry, C.; Marteleur, A.; Arras, M.; Lison, D.; Louahed, J.; Renauld, J. C.; Preat, V.; Vanbever, R., Local and systemic immune responses to intratracheal instillation of antigen and DNA vaccines in mice. Pharm. Res., 2004, 21 (1), 127-135.
92. Holt, P. G.; Schon-Hegrad, M. A.; Oliver, J.; Holt, B. J.; McMenamin, P. G., A contiguous network of dendritic antigenpresenting cells within the respiratory epithelium. Int. Arch. Allergy Appl. Immunol., 1990, 91 (2), 155-159.
93. Helson, R.; Olszewska, W.; Singh, M.; Megede, J. Z.; Melero, J. A.; O'Hagan, D.; Openshaw, P. J., Polylactide-co-glycolide (PLG) microparticles modify the immune response to DNA vaccination. Vaccine, 2008, 26 (6), 753-761.
94. Lu, D.; Hickey, A. J., Pulmonary vaccine delivery. Expert Rev Vaccine, 2007, 6 (2), 213-226.
95. Liu, M. A., DNA vaccines: an historical perspective and view to the future. Immunol. Rev., 2011, 239 (1), 62-84.
96. Morrow, M. P.; Weiner, D. B., DNA drugs come of age. Sci. Am., 2010, 303 (1), 48-53.
97. Liu, M. A., DNA vaccines: a review. J. Intern. Med., 2003, 253 (4), 402-410.
98. Schalk, J. A.; Mooi, F. R.; Berbers, G. A.; van Aerts, L. A.; Ovelgonne, H.; Kimman, T. G., Preclinical and clinical safety studies on DNA vaccines. Hum. Vaccin., 2006, 2 (2), 45-53.
99. Srivastava, I. K.; Liu, M. A., Gene vaccines. Ann. Intern. Med., 2003, 138 (7), 550-559.
100. Moorthy, V. S.; Pinder, M.; Reece, W. H.; Watkins, K.; Atabani, S.; Hannan, C.; Bojang, K.; McAdam, K. P.; Schneider, J.; Gilbert, S.; Hill, A. V., Safety and immunogenicity of DNA/modified vaccinia virus ankara malaria vaccination in African adults. J. Infect. Dis., 2003, 188 (8), 1239-1244.
101. Mwau, M.; Cebere, I.; Sutton, J.; Chikoti, P.; Winstone, N.; Wee, E. G.; Beattie, T.; Chen, Y. H.; Dorrell, L.; McShane, H.; Schmidt, C.; Brooks, M.; Patel, S.; Roberts, J.; Conlon, C.; Rowland-Jones, S. L.; Bwayo, J. J.; McMichael, A. J.; Hanke, T., A human immunodeficiency virus 1 (HIV-1) clade A vaccine in clinical trials: stimulation of HIV-specific T-cell responses by DNA and recombinant modified vaccinia virus Ankara (MVA) vaccines in humans. J. Gen. Virol., 2004, 85 (Pt 4), 911-919.
102. Rottinghaus, S. T.; Poland, G. A.; Jacobson, R. M.; Barr, L. J.; Roy, M. J., Hepatitis B DNA vaccine induces protective antibody responses in human non-responders to conventional vaccination. Vaccine, 2003, 21 (31), 4604-4608.
103. Hoffman, S. L.; Doolan, D. L.; Sedegah, M.; Wang, R.; Scheller, L. F.; Kumar, A.; Weiss, W. R.; Le, T. P.; Klinman, D. M.; Hobart, P.; Norman, J. A.; Hedstrom, R. C., Toward clinical trials of DNA vaccines against malaria. Immunol. Cell Biol., 1997, 75 (4), 376-381.
104. Wang, R.; Doolan, D. L.; Le, T. P.; Hedstrom, R. C.; Coonan, K. M.; Charoenvit, Y.; Jones, T. R.; Hobart, P.; Margalith, M.; Ng, J.; Weiss, W.R.; Sedegah, M.; de Taisne, C.; Norman, J. A.; Hoffman, S.L., Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science, 1998, 282 (5388), 476-480.
105. Le, T. P.; Coonan, K. M.; Hedstrom, R. C.; Charoenvit, Y.; Sedegah, M.; Epstein, J. E.; Kumar, S.; Wang, R.; Doolan, D. L.; Maguire, J. D.; Parker, S. E.; Hobart, P.; Norman, J.; Hoffman, S. L., Safety, tolerability and humoral immune responses after intramuscular administration of a malaria DNA vaccine to healthy adult volunteers. Vaccine, 2000, 18 (18), 1893-1901.
106. Epstein, J. E.; Charoenvit, Y.; Kester, K. E.; Wang, R.; Newcomer, R.; Fitzpatrick, S.; Richie, T. L.; Tornieporth, N.; Heppner, D. G.; Ockenhouse, C.; Majam, V.; Holland, C.; Abot, E.; Ganeshan, H.; Berzins, M.; Jones, T.; Freydberg, C. N.; Ng, J.; Norman, J.; Carucci, D. J.; Cohen, J.; Hoffman, S. L., Safety, tolerability, and antibody responses in humans after sequential immunization with a PfCSP DNA vaccine followed by the recombinant protein vaccine RTS, S/AS02A. Vaccine, 2004, 22 (13-14), 1592-1603.
107. Martin, J. E.; Pierson, T. C.; Hubka, S.; Rucker, S.; Gordon, I. J.; Enama, M. E.; Andrews, C. A.; Xu, Q.; Davis, B. S.; Nason, M.; Fay, M.; Koup, R. A.; Roederer, M.; Bailer, R. T.; Gomez, P. L.; Mascola, J. R.; Chang, G. J.; Nabel, G. J.; Graham, B. S., A West Nile virus DNA vaccine induces neutralizing antibody in healthy adults during a phase 1 clinical trial. J. Infect. Dis., 2007, 196 (12), 1732-1740.
108. Boyer, J. D.; Ugen, K. E.; Wang, B.; Agadjanyan, M.; Gilbert, L.; Bagarazzi, M.L.; Chattergoon, M.; Frost, P.; Javadian, A.; Williams, W.V.; Refaeli, Y.; Ciccarelli, R. B.; McCallus, D.; Coney, L.; Weiner, D. B., Protection of chimpanzees from highdose heterologous HIV-1 challenge by DNA vaccination. Nat. Med., 1997, 3 (5), 526-532.
109. Le Borgne, S.; Mancini, M.; Le Grand, R.; Schleef, M.; Dormont, D.; Tiollais, P.; Riviere, Y.; Michel, M. L., In vivo induction of specific cytotoxic T lymphocytes in mice and rhesus macaques immunized with DNA vector encoding an HIV epitope fused with hepatitis B surface antigen. Virology, 1998, 240 (2), 304-315.
110. Yasutomi, Y.; Robinson, H. L.; Lu, S.; Mustafa, F.; Lekutis, C.; Arthos, J.; Mullins, J. I.; Voss, G.; Manson, K.; Wyand, M.; Letvin, N. L., Simian immunodeficiency virus-specific cytotoxic Tlymphocyte induction through DNA vaccination of rhesus monkeys. J. Virol., 1996, 70 (1), 678-681.
111. Miller, A. M.; Ozenci, V.; Kiessling, R.; Pisa, P., Immune monitoring in a phase 1 trial of a PSA DNA vaccine in patients with hormone-refractory prostate cancer. J. Immunother., 2005, 28 (4), 389-395.
112. Rice, J.; Ottensmeier, C. H.; Stevenson, F. K., DNA vaccines: precision tools for activating effective immunity against cancer. Nat. Rev. Cancer, 2008, 8 (2), 108-120.
113. Becker, S. I.; Wang, R.; Hedstrom, R. C.; Aguiar, J. C.; Jones, T. R.; Hoffman, S. L.; Gardner, M. J., Protection of mice against Plasmodium yoelii sporozoite challenge with P. yoelii merozoite surface protein 1 DNA vaccines. Infect. Immun., 1998, 66 (7), 3457-3461.
114. Sedegah, M.; Jones, T. R.; Kaur, M.; Hedstrom, R.; Hobart, P.; Tine, J. A.; Hoffman, S. L., Boosting with recombinant vaccinia increases immunogenicity and protective efficacy of malaria DNA vaccine. Proc. Natl. Acad Sci. USA, 1998, 95 (13), 7648-7653.
115. Weiss, W. R.; Ishii, K. J.; Hedstrom, R. C.; Sedegah, M.; Ichino, M.; Barnhart, K.; Klinman, D. M.; Hoffman, S. L., A plasmid encoding murine granulocyte-macrophage colony-stimulating factor increases protection conferred by a malaria DNA vaccine. J. Immunol., 1998, 161 (5), 2325-2332.