Intradermal naked plasmid DNA immunization: Mechanisms of action

Expert Review of Vaccines

Volumn 10, Issue 8, 2011, Pages 1169-1182

  Elnekave, Mazal ^a   Furmanov, Karina ^a   Hovav, Avi Hai ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

antigen expression; antigen presentation; dendritic cells; DNA vaccines; immunity; intradermal immunization; plasmid; skin; T cells

Indexed keywords

ANTIGEN; CD40 LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NAKED DNA; PLASMID DNA; TOLL LIKE RECEPTOR 9;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CROSS PRESENTATION; DENDRITIC CELL; DNA IMMUNIZATION; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNITY; IMMUNOGENICITY; NEEDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SENSITIVITY ANALYSIS; SKIN; SYRINGE; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; HUMANS; INJECTIONS, INTRADERMAL; PLASMIDS; SKIN; VACCINATION; VACCINES, DNA;

EID: 80052042858     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.11.66     Document Type: Review

References (157)

1. Henri S, Guilliams M, Poulin LF, et al. Disentangling the complexity of the skin dendritic cell network. Immunol. Cell Biol. 88(4), 366-375 (2010)
2. Romani N, Clausen BE, Stoitzner P. Langerhans cells and more: langerin-expressing dendritic cell subsets in the skin. Immunol. Rev. 234(1), 120-141 (2010)
3. Meyer T, Stockfleth E, Christophers E. Immune response profiles in human skin. Br. J. Dermatol. 157(Suppl. 2), 1-7 (2007) (Pubitemid 350179621)
4. Nestle FO, Di Meglio P, Qin JZ, Nickoloff BJ. Skin immune sentinels in health and disease. Nat. Rev. Immunol. 9(10), 679-691 (2009)
5. Choi MJ, Maibach HI. Topical vaccination of DNA antigens: topical delivery of DNA antigens. Skin Pharmacol. Appl. Skin Physiol. 16(5), 271-282 (2003) (Pubitemid 36980748)
6. Peachman KK, Rao M, Alving CR. Immunization with DNA through the skin. Methods 31(3), 232-242 (2003) (Pubitemid 37162796)
7. Tang DC, DeVit M, Johnston SA. Genetic immunization is a simple method for eliciting an immune response. Nature 356(6365), 152-154 (1992)
8. Mumper RJ, Cui Z. Genetic immunization by jet injection of targeted pDNA-coated nanoparticles. Methods 31(3), 255-262 (2003) (Pubitemid 37162798)
9. Fynan EF, Webster RG, Fuller DH, Haynes JR, Santoro JC, Robinson HL. DNA vaccines: protective immunizations by parenteral, mucosal, and gene-gun inoculations. Proc. Natl Acad. Sci. USA 90(24), 11478-11482 (1993) (Pubitemid 24008662)
10. Chen CH, Ji H, Suh KW, Choti MA, Pardoll DM, Wu TC. Gene gun-mediated DNA vaccination induces antitumor immunity against human papillomavirus type 16 E7-expressing murine tumor metastases in the liver and lungs. Gene Ther. 6(12), 1972-1981 (1999) (Pubitemid 30076867)
11. Babiuk S, Baca-Estrada ME, Foldvari M, et al. Electroporation improves the efficacy of DNA vaccines in large animals. Vaccine 20(27-28), 3399-3408 (2002) (Pubitemid 35245823)
12. Selby M, Goldbeck C, Pertile T, Walsh R, Ulmer J. Enhancement of DNA vaccine potency by electroporation in vivo. J. Biotechnol. 83(1-2), 147-152 (2000)
13. Widera G, Austin M, Rabussay D, et al. Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J. Immunol. 164(9), 4635-4640 (2000) (Pubitemid 30238062)
14. Bins AD, Jorritsma A, Wolkers MC, et al. A rapid and potent DNA vaccination strategy defined by in vivo monitoring of antigen expression. Nat. Med. 11(8), 899-904 (2005) (Pubitemid 41161124)
15. Escobar-Chavez JJ, Bonilla-Martinez D, Villegas-Gonzalez MA, Molina-Trinidad E, Casas-Alancaster N, Revilla-Vazquez AL. Microneedles: a valuable physical enhancer to increase transdermal drug delivery. J. Clin. Pharmacol. 51(7), 964-977 (2010)
16. Coulman SA, Barrow D, Anstey A, et al. Minimally invasive cutaneous delivery of macromolecules and plasmid DNA via microneedles. Curr. Drug Deliv. 3(1), 65-75 (2006)
17. Raz E, Carson DA, Parker SE, et al. Intradermal gene immunization: the possible role of DNA uptake in the induction of cellular immunity to viruses. Proc. Natl Acad. Sci. USA 91(20), 9519-9523 (1994) (Pubitemid 24297946)
18. Hengge UR, Walker PS, Vogel JC. Expression of naked DNA in human, pig, and mouse skin. J. Clin. Invest. 97(12), 2911-2916 (1996) (Pubitemid 26197107)
19. Manthorpe M, Cornefert-Jensen F, Hartikka J, et al. Gene therapy by intramuscular injection of plasmid DNA: studies on firefly luciferase gene expression in mice. Hum. Gene Ther. 4(4), 419-431 (1993) (Pubitemid 24308310)
20. Loke SL, Stein CA, Zhang XH, et al. Characterization of oligonucleotide transport into living cells. Proc. Natl Acad. Sci. USA 86(10), 3474-3478 (1989) (Pubitemid 19141813)
21. Benimetskaya L, Loike JD, Khaled Z, et al. Mac-1 (CD11b/CD18) is an oligodeoxynucleotide-binding protein. Nat. Med. 3(4), 414-420 (1997) (Pubitemid 27145683)
22. Basner-Tschakarjan E, Mirmohammadsadegh A, Baer A, Hengge UR. Uptake and trafficking of DNA in keratinocytes: evidence for DNA-binding proteins. Gene Ther. 11(9), 765-774 (2004) (Pubitemid 38659755)
23. Laktionov PP, Dazard JE, Vives E, et al. Characterisation of membrane oligonucleotide-binding proteins and oligonucleotide uptake in keratinocytes. Nucleic Acids Res. 27(11), 2315-2324 (1999) (Pubitemid 29245650)
24. Budker V, Budker T, Zhang G, Subbotin V, Loomis A, Wolff JA. Hypothesis: naked plasmid DNA is taken up by cells in vivo by a receptor-mediated process. J. Gene Med. 2(2), 76-88 (2000)
25. Wittrup A, Sandgren S, Lilja J, et al. Identification of proteins released by mammalian cells that mediate DNA internalization through proteoglycan-dependent macropinocytosis. J. Biol. Chem. 282(38), 27897-27904 (2007) (Pubitemid 47529516)
26. Lechardeur D, Lukacs GL. Intracellular barriers to non-viral gene transfer. Curr. Gene Ther. 2(2), 183-194 (2002)
27. Lam AP, Dean DA. Progress and prospects: nuclear import of nonviral vectors. Gene Ther. 17(4), 439-447 (2010)
28. Wolff JA, Budker V. The mechanism of naked DNA uptake and expression. Adv. Genet. 54, 3-20 (2005)
29. Bevan MJ. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143(5), 1283-1288 (1976)
30. Greenfield EA, Nguyen KA, Kuchroo VK. CD28/B7 costimulation: a review. Crit. Rev. Immunol. 18(5), 389-418 (1998) (Pubitemid 28447017)
31. Zhu FG, Reich CF, Pisetsky DS. The role of the macrophage scavenger receptor in immune stimulation by bacterial DNA and synthetic oligonucleotides. Immunology 103(2), 226-234 (2001) (Pubitemid 32521352)
32. Rottembourg D, Filippi CM, Bresson D, et al. Essential role for TLR9 in prime but not prime-boost plasmid DNA vaccination to activate dendritic cells and protect from lethal viral infection. J. Immunol. 184(12), 7100-7107 (2010)
33. Pavlenko M, Leder C, Moreno S, Levitsky V, Pisa P. Priming of CD8+ T-cell responses after DNA immunization is impaired in TLR9- and MyD88-deficient mice. Vaccine 25(34), 6341-6347 (2007) (Pubitemid 47088755)
34. Sato Y, Roman M, Tighe H, et al. Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science 273 (5273), 352-354 (1996) (Pubitemid 26250262)
35. Unterholzner L, Keating SE, Baran M, et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11(11), 997-1004 (2010)
36. Spies B, Hochrein H, Vabulas M, et al. Vaccination with plasmid DNA activates dendritic cells via Toll-like receptor 9 (TLR9) but functions in TLR9-deficient mice. J. Immunol. 171(11), 5908-5912 (2003) (Pubitemid 37467208)
37. Krieg AM. Therapeutic potential of Toll-like receptor 9 activation. Nat. Rev. Drug Discov. 5(6), 471-484 (2006) (Pubitemid 44136959)
38. Hornung V, Ablasser A, Charrel-Dennis M, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458(7237), 514-518 (2009)
39. Babiuk S, Mookherjee N, Pontarollo R, et al. TLR9-/- and TLR9+/+ mice display similar immune responses to a DNA vaccine. Immunology 113(1), 114-120 (2004) (Pubitemid 39178850)
40. Heath WR, Carbone FR. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat. Immunol. 10(12), 1237-1244 (2009)
41. Bennett CL, Clausen BE. DC ablation in mice: promises, pitfalls, and challenges. Trends Immunol. 28(12), 525-531 (2007)
42. Allan RS, Smith CM, Belz GT, et al. Epidermal viral immunity induced by CD8a+ dendritic cells but not by Langerhans cells. Science 301(5641), 1925-1928 (2003) (Pubitemid 37229056)
43. Iezzi G, Frohlich A, Ernst B, et al. Lymph node resident rather than skin-derived dendritic cells initiate specific T cell responses after Leishmania major infection. J. Immunol. 177(2), 1250-1256 (2006) (Pubitemid 44036630)
44. He Y, Zhang J, Donahue C, Falo LD Jr. Skin-derived dendritic cells induce potent CD8(+) T cell immunity in recombinant lentivector-mediated genetic immunization. Immunity 24(5), 643-656 (2006)
45. Allan RS, Waithman J, Bedoui S, et al. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 25(1), 153-162 (2006) (Pubitemid 44066832)
46. Bursch LS, Wang L, Igyarto B, et al. Identification of a novel population of langerin+ dendritic cells. J. Exp. Med. 204(13), 3147-3156 (2007)
47. Ginhoux F, Collin MP, Bogunovic M, et al. Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J. Exp. Med. 204(13), 3133-3146 (2007)
48. Merad M, Ginhoux F, Collin M. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 8(12), 935-947 (2008)
49. Poulin LF, Henri S, de Bovis B, Devilard E, Kissenpfennig A, Malissen B. The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 204(13), 3119-3131 (2007)
50. Nagao K, Ginhoux F, Leitner WW, et al. Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc. Natl Acad. Sci. USA 106(9), 3312-3317 (2009)
51. Bedoui S, Whitney PG, Waithman J, et al. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 10(5), 488-495 (2009)
52. Sille FC, Visser A, Boes M. T cell priming by tissue-derived dendritic cells: new insights from recent murine studies. Cell Immunol. 237(2), 77-85 (2005) (Pubitemid 43117203)
53. Miller LS, Sorensen OE, Liu PT, et al. TGF-a regulates TLR expression and function on epidermal keratinocytes. J. Immunol. 174(10), 6137-6143 (2005) (Pubitemid 40663803)
54. Mempel M, Voelcker V, Kollisch G, et al. Toll-like receptor expression in human keratinocytes: nuclear factor kB controlled gene activation by Staphylococcus aureus is Toll-like receptor 2 but not Toll-like receptor 4 or platelet activating factor receptor dependent. J. Invest. Dermatol. 121(6), 1389-1396 (2003) (Pubitemid 38005491)
55. Arend WP, Palmer G, Gabay C. IL-1, IL-18, and IL-33 families of cytokines. Immunol. Rev. 223, 20-38 (2008) (Pubitemid 351986169)
56. Elnekave M, Furmanov K, Nudel I, Arizon M, Clausen BE, Hovav AH. Directly transfected langerin+ dermal dendritic cells potentiate CD8+ T cell responses following intradermal plasmid DNA immunization. J. Immunol. 185(6), 3463-3471 (2010)
57. Gilliet M, Lande R. Antimicrobial peptides and self-DNA in autoimmune skin inflammation. Curr. Opin. Immunol. 20(4), 401-407 (2008)
58. Clark RA. Skin-resident T cells: the ups and downs of on site immunity. J. Invest. Dermatol. 130(2), 362-370 (2010)
59. Gebhardt T, Wakim LM, Eidsmo L, Reading PC, Heath WR, Carbone FR. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10(5), 524-530 (2009)
60. Wakim LM, Waithman J, van Rooijen N, Heath WR, Carbone FR. Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 319 (5860), 198-202 (2008)
61. Girardi M, Oppenheim DE, Steele CR, et al. Regulation of cutaneous malignancy by gd T cells. Science 294 (5542), 605-609 (2001)
62. Strid J, Tigelaar RE, Hayday AC. Skin immune surveillance by T cells - a new order? Semin. Immunol. 21(3), 110-120 (2009)
63. Girardi M. Immunosurveillance and immunoregulation by gd T cells. J. Invest. Dermatol. 126(1), 25-31 (2006)
64. Forg P, von Hoegen P, Dalemans W, Schirrmacher V. Superiority of the ear pinna over muscle tissue as site for DNA vaccination. Gene Ther. 5(6), 789-797 (1998)
65. Hovav AH, Panas MW, Rahman S, et al. Duration of antigen expression in vivo following DNA immunization modifies the magnitude, contraction, and secondary responses of CD8+ T lymphocytes. J. Immunol. 179(10), 6725-6733 (2007)
66. Akbari O, Panjwani N, Garcia S, Tascon R, Lowrie D, Stockinger B. DNA vaccination: transfection and activation of dendritic cells as key events for immunity. J. Exp. Med. 189(1), 169-178 (1999)
67. Roos AK, Eriksson F, Walters DC, Pisa P, King AD. Optimization of skin electroporation in mice to increase tolerability of DNA vaccine delivery to patients. Mol. Ther. 17(9), 1637-1642 (2009)
68. Geiben-Lynn R, Greenland JR, Frimpong-Boateng K, van Rooijen N, Hovav AH, Letvin NL. CD4+ T lymphocytes mediate in vivo clearance of plasmid DNA vaccine antigen expression and potentiate CD8+ T-cell immune responses. Blood 112(12), 4585-4590 (2008)
69. Greenland JR, Geiben R, Ghosh S, Pastor WA, Letvin NL. Plasmid DNA vaccine-elicited cellular immune responses limit in vivo vaccine antigen expression through Fas-mediated apoptosis. J. Immunol. 178(9), 5652-5658 (2007) (Pubitemid 46674361)
70. Payette PJ, Weeratna RD, McCluskie MJ, Davis HL. Immune-mediated destruction of transfected myocytes following DNA vaccination occurs via multiple mechanisms. Gene Ther. 8(18), 1395-1400 (2001) (Pubitemid 32895670)
71. Brooks AR, Harkins RN, Wang P, Qian HS, Liu P, Rubanyi GM. Transcriptional silencing is associated with extensive methylation of the CMV promoter following adenoviral gene delivery to muscle. J. Gene Med. 6(4), 395-404 (2004) (Pubitemid 40228056)
72. Vanniasinkam T, Ertl H, Tang Q. Trichostatin-A enhances adaptive immune responses to DNA vaccination. J. Clin. Virol. 36(4), 292-297 (2006) (Pubitemid 44066897)
73. Geiben-Lynn R, Greenland JR, Frimpong-Boateng K, Letvin NL. Non-classical natural killer T cells modulate plasmid DNA vaccine antigen expression and vaccine-elicited immune responses by MCP-1 secretion after interaction with a b2-microglobulin-independent CD1d. J. Biol. Chem. 284(49), 33800-33806 (2009)
74. Bot A, Stan AC, Inaba K, Steinman R, Bona C. Dendritic cells at a DNA vaccination site express the encoded influenza nucleoprotein and prime MHC class I-restricted cytolytic lymphocytes upon adoptive transfer. Int. Immunol. 12(6), 825-832 (2000) (Pubitemid 30410455)
75. Casares S, Inaba K, Brumeanu TD, Steinman RM, Bona CA. Antigen presentation by dendritic cells after immunization with DNA encoding a major histocompatibility complex class II-restricted viral epitope. J. Exp. Med. 186(9), 1481-1486 (1997) (Pubitemid 27479807)
76. Bouloc A, Walker P, Grivel JC, Vogel JC, Katz SI. Immunization through dermal delivery of protein-encoding DNA: a role for migratory dendritic cells. Eur. J. Immunol. 29(2), 446-454 (1999) (Pubitemid 29078505)
77. Tuomela M, Malm M, Wallen M, Stanescu I, Krohn K, Peterson P. Biodistribution and general safety of a naked DNA plasmid, GTU-MultiHIV, in a rat, using a quantitative PCR method. Vaccine 23(7), 890-896 (2005) (Pubitemid 39643176)
78. Bedoui S, Davey GM, Lew AM, Heath WR. Equivalent stimulation of naive and memory CD8 T cells by DNA vaccination: a dendritic cell-dependent process. Immunol. Cell Biol. 87(3), 255-259 (2009)
79. Hon H, Oran A, Brocker T, Jacob J. B lymphocytes participate in cross-presentation of antigen following gene gun vaccination. J. Immunol. 174(9), 5233-5242 (2005) (Pubitemid 40593161)
80. Corr M, von Damm A, Lee DJ, Tighe H. In vivo priming by DNA injection occurs predominantly by antigen transfer. J. Immunol. 163(9), 4721-4727 (1999) (Pubitemid 29501233)
81. Vandermeulen G, Richiardi H, Escriou V, et al. Skin-specific promoters for genetic immunisation by DNA electroporation. Vaccine 27(32), 4272-4277 (2009)
82. Cho JH, Youn JW, Sung YC. Cross-priming as a predominant mechanism for inducing CD8(+) T cell responses in gene gun DNA immunization. J. Immunol. 167(10), 5549-5557 (2001)
83. Lauterbach H, Gruber A, Ried C, Cheminay C, Brocker T. Insufficient APC capacities of dendritic cells in gene gun-mediated DNA vaccination. J. Immunol. 176(8), 4600-4607 (2006)
84. Furmanov K, Elnekave M, Lehmann D, Clausen BE, Kotton DN, Hovav AH. The role of skin-derived dendritic cells in CD8+ T cell priming following immunization with lentivectors. J. Immunol. 184(9), 4889-4897 (2010)
85. Brewig N, Kissenpfennig A, Malissen B, et al. Priming of CD8+ and CD4+ T cells in experimental leishmaniasis is initiated by different dendritic cell subtypes. J. Immunol. 182(2), 774-783 (2009)
86. Noordegraaf M, Flacher V, Stoitzner P, Clausen BE. Functional redundancy of Langerhans cells and langerin(+) dermal dendritic cells in contact hypersensitivity. J. Invest. Dermatol. 130(12), 2752-2759 (2010)
87. Stoecklinger A, Grieshuber I, Scheiblhofer S, et al. Epidermal Langerhans cells are dispensable for humoral and cell-mediated immunity elicited by gene gun immunization. J. Immunol. 179(2), 886-893 (2007)
88. Stoecklinger A, Eticha TD, Mesdaghi M, et al. Langerin+ dermal dendritic cells are critical for CD8+ T cell activation and IgH g-1 class switching in response to gene gun vaccines. J. Immunol. 186(3), 1377-1383 (2011)
89. Clausen BE, Kel JM. Langerhans cells: critical regulators of skin immunity? Immunol. Cell Biol. 88(4), 351-360 (2010)
90. Nudel I, Elnekave M, Furmanov K, et al. Dendritic cells in distinct oral mucosal tissues engage different mechanisms to prime CD8+ T cells. J. Immunol. 186(2), 891-900 (2011)
91. Henri S, Poulin LF, Tamoutounour S, et al. CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J. Exp. Med. 207(1), 189-206 (2010)
92. Sugita K, Kabashima K, Atarashi K, Shimauchi T, Kobayashi M, Tokura Y. Innate immunity mediated by epidermal keratinocytes promotes acquired immunity involving Langerhans cells and T cells in the skin. Clin. Exp. Immunol. 147(1), 176-183 (2007) (Pubitemid 44915569)
93. Stoitzner P, Tripp CH, Eberhart A, et al. Langerhans cells cross-present antigen derived from skin. Proc. Natl Acad. Sci. USA 103(20), 7783-7788 (2006)
94. Jelley-Gibbs DM, Brown DM, Dibble JP, Haynes L, Eaton SM, Swain SL. Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J. Exp. Med. 202(5), 697-706 (2005) (Pubitemid 41248420)
95. Turner DL, Cauley LS, Khanna KM, Lefrancois L. Persistent antigen presentation after acute vesicular stomatitis virus infection. J. Virol. 81(4), 2039-2046 (2007) (Pubitemid 46214475)
96. Zammit DJ, Turner DL, Klonowski KD, Lefrancois L, Cauley LS. Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity 24(4), 439-449 (2006)
97. Barber DL, Wherry EJ, Masopust D, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439(7077), 682-687 (2006) (Pubitemid 43237609)
98. Halwani R, Boyer JD, Yassine-Diab B, et al. Therapeutic vaccination with simian immunodeficiency virus (SIV)-DNA + IL-12 or IL-15 induces distinct CD8 memory subsets in SIV-infected macaques. J. Immunol. 180(12), 7969-7979 (2008)
99. Velu V, Kannanganat S, Ibegbu C, et al. Elevated expression levels of inhibitory receptor programmed death 1 on simian immunodeficiency virus-specific CD8 T cells during chronic infection but not after vaccination. J. Virol. 81(11), 5819-5828 (2007) (Pubitemid 46847019)
100. Smith KA, Tam VL, Wong RM, et al. Enhancing DNA vaccination by sequential injection of lymph nodes with plasmid vectors and peptides. Vaccine 27(19), 2603-2615 (2009)
101. Bot A, Qiu Z, Wong R, Obrocea M, Smith KA. Programmed cell death-1 (PD-1) at the heart of heterologous prime-boost vaccines and regulation of CD8+ T cell immunity. J. Transl. Med. 8, 132 (2010)
102. Mueller SN, Jones CM, Smith CM, Heath WR, Carbone FR. Rapid cytotoxic T lymphocyte activation occurs in the draining lymph nodes after cutaneous herpes simplex virus infection as a result of early antigen presentation and not the presence of virus. J. Exp. Med. 195(5), 651-656 (2002) (Pubitemid 34461510)
103. Norbury CC, Malide D, Gibbs JS, Bennink JR, Yewdell JW. Visualizing priming of virus-specific CD8+ T cells by infected dendritic cells in vivo. Nat. Immunol. 3(3), 265-271 (2002) (Pubitemid 34213428)
104. Liu L, Fuhlbrigge RC, Karibian K, Tian T, Kupper TS. Dynamic programming of CD8+ T cell trafficking after live viral immunization. Immunity 25(3), 511-520 (2006) (Pubitemid 44354216)
105. Klinman DM, Sechler JM, Conover J, Gu M, Rosenberg AS. Contribution of cells at the site of DNA vaccination to the generation of antigen-specific immunity and memory. J. Immunol. 160(5), 2388-2392 (1998) (Pubitemid 28119922)
106. Torres CA, Iwasaki A, Barber BH, Robinson HL. Differential dependence on target site tissue for gene gun and intramuscular DNA immunizations. J. Immunol. 158(10), 4529-4532 (1997) (Pubitemid 127483769)
107. van den Berg JH, Nujien B, Beijnen JH, et al. Optimization of intradermal vaccination by DNA tattooing in human skin. Hum. Gene Ther. 20(3), 181-189 (2009)
108. Yoshida A, Nagata T, Uchijima M, Koide Y. Protective CTL response is induced in the absence of CD4+ T cells and IFN-g by gene gun DNA vaccination with a minigene encoding a CTL epitope of Listeria monocytogenes. Vaccine 19(30), 4297-4306 (2001) (Pubitemid 32703652)
109. Hawkins WG, Gold JS, Dyall R, et al. Immunization with DNA coding for gp100 results in CD4 T-cell independent antitumor immunity. Surgery 128(2), 273-280 (2000) (Pubitemid 30622495)
110. Maecker HT, Umetsu DT, DeKruyff RH, Levy S. Cytotoxic T cell responses to DNA vaccination: dependence on antigen presentation via class II MHC. J. Immunol. 161(12), 6532-6536 (1998) (Pubitemid 28562191)
111. Wild J, Grusby MJ, Schirmbeck R, Reimann J. Priming MHC-I-restricted cytotoxic T lymphocyte responses to exogenous hepatitis B surface antigen is CD4+ T cell dependent. J. Immunol. 163(4), 1880-1887 (1999) (Pubitemid 29382188)
112. Chan K, Lee DJ, Schubert A, et al. The roles of MHC class II, CD40, and B7 costimulation in CTL induction by plasmid DNA. J. Immunol. 166(5), 3061-3066 (2001) (Pubitemid 33117301)
113. Corr M, Tighe H, Lee D, et al. Costimulation provided by DNA immunization enhances antitumor immunity. J. Immunol. 159(10), 4999-5004 (1997) (Pubitemid 127471038)
114. Obst R, van Santen HM, Mathis D, Benoist C. Antigen persistence is required throughout the expansion phase of a CD4(+) T cell response. J. Exp. Med. 201(10), 1555-1565 (2005) (Pubitemid 40721001)
115. Badovinac VP, Porter BB, Harty JT. Programmed contraction of CD8(+) T cells after infection. Nat. Immunol. 3(7), 619-626 (2002) (Pubitemid 34752470)
116. Koup RA, Roederer M, Lamoreaux L, et al. Priming immunization with DNA augments immunogenicity of recombinant adenoviral vectors for both HIV-1 specific antibody and T-cell responses. PLoS ONE 5(2), e9015 (2010)
117. Jaoko W, Karita E, Kayitenkore K, et al. Safety and immunogenicity study of Multiclade HIV-1 adenoviral vector vaccine alone or as boost following a multiclade HIV-1 DNA vaccine in Africa. PLoS ONE 5(9), e12873 (2010)
118. Santra S, Liao HX, Zhang R, et al. Mosaic vaccines elicit CD8+ T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat. Med. 16(3), 324-328 (2010)
119. Gilbert SC, Moorthy VS, Andrews L, et al. Synergistic DNA-MVA prime-boost vaccination regimes for malaria and tuberculosis. Vaccine 24(21), 4554-4561 (2006) (Pubitemid 43776762)
120. Hovav AH, Panas MW, Osuna CE, Cayabyab MJ, Autissier P, Letvin NL. The impact of a boosting immunogen on the differentiation of secondary memory CD8+ T cells. J. Virol. 81(23), 12793-12802 (2007) (Pubitemid 350156917)
121. Santra S, Barouch DH, Korioth-Schmitz B, et al. Recombinant poxvirus boosting of DNA-primed rhesus monkeys augments peak but not memory T lymphocyte responses. Proc. Natl Acad. Sci. USA 101(30), 11088-11093 (2004) (Pubitemid 38989588)
122. Richmond JF, Lu S, Santoro JC, et al. Studies of the neutralizing activity and avidity of anti-human immunodeficiency virus type 1 Env antibody elicited by DNA priming and protein boosting. J. Virol. 72(11), 9092-9100 (1998) (Pubitemid 28471853)
123. Richmond JF, Mustafa F, Lu S, et al. Screening of HIV-1 Env glycoproteins for the ability to raise neutralizing antibody using DNA immunization and recombinant vaccinia virus boosting. Virology 230(2), 265-274 (1997) (Pubitemid 27211857)
124. Fuller DH, Simpson L, Cole KS, et al. Gene gun-based nucleic acid immunization alone or in combination with recombinant vaccinia vectors suppresses virus burden in rhesus macaques challenged with a heterologous SIV. Immunol. Cell Biol. 75(4), 389-396 (1997) (Pubitemid 27408047)
125. Degano P, Schneider J, Hannan CM, Gilbert SC, Hill AV. Gene gun intradermal DNA immunization followed by boosting with modified vaccinia virus Ankara: enhanced CD8+ T cell immunogenicity and protective efficacy in the influenza and malaria models. Vaccine 18 (7-8), 623-632 (1999) (Pubitemid 29509846)
126. Radcliffe JN, Roddick JS, Friedmann PS, Stevenson FK, Thirdborough SM. Prime-boost with alternating DNA vaccines designed to engage different antigen presentation pathways generates high frequencies of peptide-specific CD8+ T cells. J. Immunol. 177(10), 6626-6633 (2006) (Pubitemid 44715025)
127. Kim TW, Lee JH, He L, Boyd DA, Hung CF, Wu TC. DNA vaccines employing intracellular targeting strategies and a strategy to prolong dendritic cell life generate a higher number of CD8+ memory T cells and better long-term antitumor effects compared with a DNA prime- vaccinia boost regimen. Hum. Gene Ther. 16(1), 26-34 (2005) (Pubitemid 40250329)
128. Brice GT, Dobano C, Sedegah M, et al. Extended immunization intervals enhance the immunogenicity and protective efficacy of plasmid DNA vaccines. Microbes Infect. 9 (12-13), 1439-1446 (2007) (Pubitemid 350016978)
129. Belz GT, Bedoui S, Kupresanin F, Carbone FR, Heath WR. Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat. Immunol. 8(10), 1060-1066 (2007) (Pubitemid 47423753)
130. Radcliffe JN, Roddick JS, Stevenson FK, Thirdborough SM. Prolonged antigen expression following DNA vaccination impairs effector CD8+ T cell function and memory development. J. Immunol. 179(12), 8313-8321 (2007)
131. Wherry EJ, Barber DL, Kaech SM, Blattman JN, Ahmed R. Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc. Natl Acad. Sci. USA 101(45), 16004-16009 (2004) (Pubitemid 39507917)
132. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401(6754), 708-712 (1999)
133. Elnekave M, Bivas-Benita M, Gillard GO, Sircar P, Hovav AH. A matter of timing: unsynchronized antigen expression and antigen presentation diminish secondary T cell responses. J. Immunol. 183(2), 1013-1021 (2009)
134. Endmann A, Baden M, Weisermann E, et al. Immune response induced by a linear DNA vector: influence of dose, formulation and route of injection. Vaccine 28(21), 3642-3649 (2010)
135. Kurupati P, Ramachandran NP, Poh CL. Protective efficacy of DNA vaccines encoding outer membrane protein A and OmpK36 of Klebsiella pneumoniae in mice. Clin. Vaccine Immunol. 18(1), 82-88 (2011)
136. Osinubi MO, Wu X, Franka R, et al. Enhancing comparative rabies DNA vaccine effectiveness through glycoprotein gene modifications. Vaccine 27(51), 7214-7218 (2009)
137. Lodmell DL, Ewalt LC, Parnell MJ, Rupprecht CE, Hanlon CA. One-time intradermal DNA vaccination in ear pinnae one year prior to infection protects dogs against rabies virus. Vaccine 24(4), 412-416 (2006) (Pubitemid 41832543)
138. Gaffal E, Schweichel D, Tormo D, et al. Comparative evaluation of CD8+CTL responses following gene gun immunization targeting the skin with intracutaneous injection of antigen-transduced dendritic cells. Eur. J. Cell Biol. 86(11-12), 817-826 (2007) (Pubitemid 350082192)
139. Garg S, Oran A, Wajchman J, et al. Genetic tagging shows increased frequency and longevity of antigen-presenting, skin-derived dendritic cells in vivo. Nat. Immunol. 4(9), 907-912 (2003) (Pubitemid 37098662)
140. Dondji B, Deak E, Goldsmith-Pestana K, et al. Intradermal NKT cell activation during DNA priming in heterologous prime-boost vaccination enhances T cell responses and protection against Leishmania. Eur. J. Immunol. 38(3), 706-719 (2008)
141. Minigo G, Scholzen A, Tang CK, et al. Poly-l-lysine-coated nanoparticles: a potent delivery system to enhance DNA vaccine efficacy. Vaccine 25(7), 1316-1327 (2007) (Pubitemid 46027334)
142. Kawase A, Isaji K, Yamaoka A, Kobayashi N, Nishikawa M, Takakura Y. Enhanced antigen-specific antibody production following polyplex-based DNA vaccination via the intradermal route in mice. Vaccine 24(27-28), 5535-5545 (2006) (Pubitemid 43867106)
143. Schwendener RA, Ludewig B, Cerny A, Engler O. Liposome-based vaccines. Methods Mol. Biol. 605, 163-175 (2010)
144. Manoj S, Griebel PJ, Babiuk LA, van Drunen Littel-van den Hurk S. Modulation of immune responses to bovine herpesvirus-1 in cattle by immunization with a DNA vaccine encoding glycoprotein D as a fusion protein with bovine CD154. Immunology 112(2), 328-338 (2004) (Pubitemid 38703579)
145. Melkebeek V, Verdonck F, Stuyven E, Goddeeris B, Cox E. Plasmid-encoded GM-CSF induces priming of the F4(K88)- specific serum IgA response by FaeG DNA vaccination in pigs. Vaccine 24(21), 4592-4594 (2006) (Pubitemid 43792481)
146. Gartner T, Romano M, Suin V, et al. Immunogenicity and protective efficacy of a tuberculosis DNA vaccine co-expressing pro-apoptotic caspase-3. Vaccine 26(11), 1458-1470 (2008)
147. Geiben-Lynn R, Frimpong-Boateng K, Letvin NL. Modulation of plasmid DNA vaccine antigen clearance by caspase 12 RNA interference (RNAi) potentiates vaccination. Clin. Vaccine Immunol. 18(4), 533-538 (2011)
148. Parsania M, Bamdad T, Hassan ZM, et al. Evaluation of apoptotic and anti-apoptotic genes on efficacy of DNA vaccine encoding glycoprotein B of herpes simplex virus type 1. Immunol. Lett. 128(2), 137-142 (2010)
149. Kim JH, Chen J, Majumder N, Lin H, Falo LD Jr, You Z. 'Survival gene' Bcl-xl potentiates DNA-raised antitumor immunity. Gene Ther. 12(20), 1517-1525 (2005) (Pubitemid 41508677)
150. Kim TW, Hung CF, Ling M, et al. Enhancing DNA vaccine potency by coadministration of DNA encoding antiapoptotic proteins. J. Clin. Invest. 112(1), 109-117 (2003) (Pubitemid 38056382)
151. Hon H, Rucker EB 3rd, Hennighausen L, Jacob J. bcl-xl is critical for dendritic cell survival in vivo. J. Immunol. 173(7), 4425-4432 (2004) (Pubitemid 39280672)
152. Holst PJ, Bassi MR, Thomsen AR, Christensen JP. DNA fusion gene vaccines. Curr. Opin. Mol. Ther. 12(1), 47-54 (2010)
153. Huang Y, Babiuk LA, van Drunen Littel-van den Hurk S. The cell-mediated immune response induced by plasmid encoding bovine herpesvirus 1 glycoprotein B is enhanced by plasmid encoding IL-12 when delivered intramuscularly or by gene gun, but not after intradermal injection. Vaccine 24(25), 5349-5359 (2006) (Pubitemid 43818204)
154. Kutzler MA, Weiner DB. DNA vaccines: ready for prime time? Nat. Rev. Genet. 9(10), 776-788 (2008)
155. Nchinda G, Kuroiwa J, Oks M, et al. The efficacy of DNA vaccination is enhanced in mice by targeting the encoded protein to dendritic cells. J. Clin. Invest. 118(4), 1427-1436 (2008) (Pubitemid 351500436)
156. Demangel C, Zhou J, Choo AB, Shoebridge G, Halliday GM, Britton WJ. Single chain antibody fragments for the selective targeting of antigens to dendritic cells. Mol. Immunol. 42(8), 979-985 (2005) (Pubitemid 40489023)
157. Grossmann C, Tenbusch M, Nchinda G, et al. Enhancement of the priming efficacy of DNA vaccines encoding dendritic cell-targeted antigens by synergistic Toll-like receptor ligands. BMC Immunol. 10, 43 (2009)