Advanced search
Publication Cover
Expert Review of Vaccines Volume 6, 2007 - Issue 2
Submit an article Journal homepage
96
Views
56
CrossRef citations to date
0
Altmetric
Review

Enhancing DNA vaccine potency by modifying the properties of antigen-presenting cells

Shaw-Wei D Tsen Department of Pathology, John Hopkins School of Medicine, Cancer Research Building II Room 309, 1550 Orleans Street, Baltimore, MD 21231, USA. [email protected]
,
Augustine H Paik Department of Pathology, John Hopkins School of Medicine, Cancer Research Building II Room 309, 1550 Orleans Street, Baltimore, MD 21231, USA. [email protected]
,
Chien-Fu Hung Department of Oncology, John Hopkins School of Medicine, Cancer Research Building II Room 309, 1550 Orleans Street, Baltimore, MD 21231, USA. [email protected]
&
T-C Wu Department of Pathology, John Hopkins School of Medicine, Cancer Research Building II Room 309, 1550 Orleans Street, Baltimore, MD 21231, USA. [email protected]
Pages 227-239 | Published online: 09 Jan 2014

References

  • Donnelly JJ, Ulmer JB, Shiver JW, Liu MA. DNA vaccines. Annu. Rev. Immunol.15, 617–648 (1997).
  • Gurunathan S, Klinman DM, Seder RA. DNA vaccines: immunology application, and optimization. Annu. Rev. Immunol.18, 927–974 (2000).
  • Guermonprez P, Valladeau J, Zitvogel L, Thery C, Amigorena S. Antigen presentation and T cell stimulation by dendritic cells. Annu. Rev. Immunol.20, 621–667 (2002).
  • Steinman RM. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol.9, 271–296 (1991).
  • Banchereau J, Briere F, Caux C et al. Immunobiology of dendritic cells. Annu. Rev. Immunol.18, 767–811 (2000).
  • Condon C, Watkins SC, Celluzzi CM, Thompson K, Falo LD Jr. DNA-based immunization by in vivo transfection of dendritic cells. Nat. Med.2(10), 1122–1128 (1996).
  • Porgador A, Irvine KR, Iwasaki A et al. Predominant role for directly transfected dendritic cells in antigen presentation to CD8+ T cells after gene gun immunization. J. Exp. Med.188(6), 1075–1082 (1998).
  • Payne LG, Fuller DH, Haynes JR. Particle-mediated DNA vaccination of mice, monkeys and men: looking beyond the dogma. Curr. Opin. Mol. Ther.4(5), 459–466 (2002).
  • Maloy KJ, Erdmann I, Basch V et al. Intralymphatic immunization enhances DNA vaccination. Proc. Natl Acad. Sci. USA98(6), 3299–3303 (2001).
  • Tagawa ST, Lee P, Snively J et al. Phase I study of intranodal delivery of a plasmid DNA vaccine for patients with stage IV melanoma. Cancer98(1), 144–154 (2003).
  • Munoz-Montesino C, Andrews E, Rivers R et al. Intraspleen delivery of a DNA vaccine coding for superoxide dismutase (SOD) of Brucella abortus induces SOD-specific CD4+ and CD8+ T cells. Infect. Immun.72(4), 2081–2087 (2004).
  • 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).
  • Paster W, Zehetner M, Kalat M, Schuller S, Schweighoffer T. In vivo plasmid DNA electroporation generates exceptionally high levels of epitope-specific CD8+ T-cell responses. Gene Ther.10(9), 717–724 (2003).
  • Kalat M, Kupcu Z, Schuller S et al.In vivo plasmid electroporation induces tumor antigen-specific CD8+ T-cell responses and delays tumor growth in a syngeneic mouse melanoma model. Cancer Res.62(19), 5489–5494 (2002).
  • Otten G, Schaefer M, Doe B et al. Enhancement of DNA vaccine potency in rhesus macaques by electroporation. Vaccine22(19), 2489–2493 (2004).
  • Babiuk S, Baca-Estrada ME, Foldvari M et al. Electroporation improves the efficacy of DNA vaccines in large animals. Vaccine20(27–28), 3399–3408 (2002).
  • Scheerlinck JP, Karlis J, Tjelle TE et al.In vivo electroporation improves immune responses to DNA vaccination in sheep. Vaccine22(13–14), 1820–1825 (2004).
  • Zhang X, Divangahi M, Ngai P et al. Intramuscular immunization with a monogenic plasmid DNA tuberculosis vaccine: enhanced immunogenicity by electroporation and co-expression of GM-CSF transgene. Vaccine25(7), 1342–1352 (2007).
  • Dilber MS, Phelan A, Aints A et al. Intercellular delivery of thymidine kinase prodrug activating enzyme by the herpes simplex virus protein, VP22. Gene Ther.6(1), 12–21 (1999).
  • Wybranietz WA, Gross CD, Phelan A et al. Enhanced suicide gene effect by adenoviral transduction of a VP22–cytosine deaminase (CD) fusion gene. Gene Ther.8(21), 1654–1664 (2001).
  • Phelan A, Elliott G, O’Hare P. Intercellular delivery of functional p53 by the herpesvirus protein VP22. Nat. Biotechnol.16(5), 440–443 (1998).
  • Elliott G, O’Hare P. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell88(2), 223–233 (1997).
  • Kim TW, Hung CF, Kim JW et al. Vaccination with a DNA vaccine encoding herpes simplex virus type 1 VP22 linked to antigen generates long-term antigen-specific CD8-positive memory T cells and protective immunity. Hum. Gene Ther.15(2), 167–177 (2004).
  • Hung CF, Cheng WF, Chai CY et al. Improving vaccine potency through intercellular spreading and enhanced MHC class I presentation of antigen. J. Immunol.166(9), 5733–5740 (2001).
  • Peng S, Trimble C, Ji H et al. Characterization of HPV-16 E6 DNA vaccines employing intracellular targeting and intercellular spreading strategies. J. Biomed. Sci.12(5), 689–700 (2005).
  • Saha S, Yoshida S, Ohba K et al. A fused gene of nucleoprotein (NP) and herpes simplex virus genes (VP22) induces highly protective immunity against different subtypes of influenza virus. Virology354(1), 48–57 (2006).
  • Harms JS, Ren X, Oliveira SC, Splitter GA. Distinctions between bovine herpesvirus 1 and herpes simplex virus type 1 VP22 tegument protein subcellular associations. J. Virol.74(7), 3301–3312 (2000).
  • Koptidesova D, Kopacek J, Zelnik V et al. Identification and characterization of a cDNA clone derived from the Marek’s disease tumour cell line RPL1 encoding a homologue of α-transinducing factor (VP16) of HSV-1. Arch. Virol.140(2), 355–362 (1995).
  • Dorange F, El Mehdaoui S, Pichon C, Coursaget P, Vautherot JF. Marek’s disease virus (MDV) homologues of herpes simplex virus type 1 UL49 (VP22) and UL48 (VP16) genes: high-level expression and characterization of MDV-1 VP22 and VP16. J. Gen. Virol.81(Pt 9), 2219–2230 (2000).
  • Mwangi W, Brown WC, Splitter GA et al. Enhancement of antigen acquisition by dendritic cells and MHC class II-restricted epitope presentation to CD4+ T cells using VP22 DNA vaccine vectors that promote intercellular spreading following initial transfection. J. Leukoc. Biol.78(2), 401–411 (2005).
  • Oliveira SC, Harms JS, Afonso RR, Splitter GA. A genetic immunization adjuvant system based on BVP22-antigen fusion. Hum. Gene Ther.12(10), 1353–1359 (2001).
  • Zheng CF, Brownlie R, Huang DY, Babiuk LA, van Drunen Littel-van den Hurk S. Intercellular trafficking of the major tegument protein VP22 of bovine herpesvirus-1 and its application to improve a DNA vaccine. Arch. Virol.151(5), 985–993 (2006).
  • Zheng C, Babiuk LA, van Drunen Littel-van den Hurk S. Bovine herpesvirus 1 VP22 enhances the efficacy of a DNA vaccine in cattle. J. Virol.79(3), 1948–1953 (2005).
  • Hung CF, He L, Juang J et al. Improving DNA vaccine potency by linking Marek’s disease virus type 1 VP22 to an antigen. J. Virol.76(6), 2676–2682 (2002).
  • Lundberg M, Johansson M. Is VP22 nuclear homing an artifact? Nat. Biotechnol.19(8), 713–714 (2001).
  • Perkins SD, Hartley MG, Lukaszewski RA et al. VP22 enhances antibody responses from DNA vaccines but not by intercellular spread. Vaccine23(16), 1931–1940 (2005).
  • Sciortino MT, Taddeo B, Poon AP, Mastino A, Roizman B. Of the three tegument proteins that package mRNA in herpes simplex virions, one (VP22) transports the mRNA to uninfected cells for expression prior to viral infection. Proc. Natl Acad. Sci. USA99(12), 8318–8323 (2002).
  • Trimble C, Lin CT, Hung CF et al. Comparison of the CD8+ T cell responses and antitumor effects generated by DNA vaccine administered through gene gun, biojector, and syringe. Vaccine21(25–26), 4036–4042 (2003).
  • Hauser H, Chen SY. Augmentation of DNA vaccine potency through secretory heat shock protein-mediated antigen targeting. Methods31(3), 225–231 (2003).
  • Hauser H, Shen L, Gu QL, Krueger S, Chen SY. Secretory heat-shock protein as a dendritic cell-targeting molecule: a new strategy to enhance the potency of genetic vaccines. Gene Ther.11(11), 924–932 (2004).
  • Hung CF, Hsu KF, Cheng WF et al. Enhancement of DNA vaccine potency by linkage of antigen gene to a gene encoding the extracellular domain of Fms-like tyrosine kinase 3-ligand. Cancer Res.61(3), 1080–1088 (2001).
  • Boyle JS, Brady JL, Lew AM. Enhanced responses to a DNA vaccine encoding a fusion antigen that is directed to sites of immune induction. Nature392(6674), 408–411 (1998).
  • You Z, Huang X, Hester J, Toh HC, Chen SY. Targeting dendritic cells to enhance DNA vaccine potency. Cancer Res.61(9), 3704–3711 (2001).
  • Kang TH, Lee JH, Song CK et al. Epigallocatechin-3-gallate enhances CD8+ T cell-mediated antitumor immunity induced by DNA vaccination. Cancer Res.67(2), 802–811 (2007).
  • Lin CT, Tsai YC, He L et al. A DNA vaccine encoding a codon-optimized human papillomavirus type 16 E6 gene enhances CTL response and anti-tumor activity. J. Biomed. Sci.13(4), 481–488 (2006).
  • Liu WJ, Gao F, Zhao KN et al. Codon modified human papillomavirus type 16 E7 DNA vaccine enhances cytotoxic T-lymphocyte induction and anti-tumour activity. Virology301(1), 43–52 (2002).
  • Chen CH, Wang TL, Hung CF et al. Enhancement of DNA vaccine potency by linkage of antigen gene to an HSP70 gene. Cancer Res.60(4), 1035–1042 (2000).
  • Hung CF, Cheng WF, He L et al. Enhancing major histocompatibility complex class I antigen presentation by targeting antigen to centrosomes. Cancer Res.63(10), 2393–2398 (2003).
  • Cheng WF, Hung CF, Chai CY et al. Tumor-specific immunity and antiangiogenesis generated by a DNA vaccine encoding calreticulin linked to a tumor antigen. J. Clin. Invest.108(5), 669–678 (2001).
  • Ciernik IF, Berzofsky JA, Carbone DP. Induction of cytotoxic T lymphocytes and antitumor immunity with DNA vaccines expressing single T cell epitopes. J. Immunol.156(7), 2369–2375 (1996).
  • Tobery TW, Siliciano RF. Targeting of HIV-1 antigens for rapid intracellular degradation enhances cytotoxic T lymphocyte (CTL) recognition and the induction of de novo CTL responses in vivo after immunization. J. Exp. Med.185(5), 909–920 (1997).
  • Hung CF, Cheng WF, Hsu KF et al. Cancer immunotherapy using a DNA vaccine encoding the translocation domain of a bacterial toxin linked to a tumor antigen. Cancer Res.61(9), 3698–3703 (2001).
  • Kim JW, Hung CF, Juang J et al. Comparison of HPV DNA vaccines employing intracellular targeting strategies. Gene Ther.11(12), 1011–1018 (2004).
  • Castellino F, Germain RN. Cooperation between CD4+ and CD8+ T cells: when, where, and how. Annu. Rev. Immunol.24, 519–540 (2006).
  • Wu T-C, Guarnieri FG, Staveley-O’Carroll KF et al. Engineering an intracellular pathway for MHC class II presentation of HPV-16 E7. Proc. Natl Acad. Sci. USA92, 11671–11675 (1995).
  • Ji H, Wang T-L, Chen C-H et al. Targeting HPV-16 E7 to the endosomal/lysosomal compartment enhances the antitumor immunity of DNA vaccines against murine HPV-16 E7-expressing tumors. Hum. Gene Ther.10(17), 2727–2740 (1999).
  • de Arruda LB, Chikhlikar PR, August JT, Marques ET. DNA vaccine encoding human immunodeficiency virus-1 Gag, targeted to the major histocompatibility complex II compartment by lysosomal-associated membrane protein, elicits enhanced long-term memory response. Immunology112(1), 126–133 (2004).
  • Wang S, Bartido S, Yang G et al. A role for a melanosome transport signal in accessing the MHC class II presentation pathway and in eliciting CD4+ T cell responses. J. Immunol.163(11), 5820–5826 (1999).
  • Diebold SS, Cotten M, Koch N, Zenke M. MHC class II presentation of endogenously expressed antigens by transfected dendritic cells. Gene Ther.8(6), 487–493 (2001).
  • Cresswell P. Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol.12, 259–293 (1994).
  • Trombetta ES, Mellman I. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol.23, 975–1028 (2005).
  • Fujii S, Senju S, Chen YZ et al. The CLIP-substituted invariant chain efficiently targets an antigenic peptide to HLA class II pathway in L cells. Hum. Immunol.59(10), 607–614 (1998).
  • Malcherek G, Wirblich C, Willcox N et al. MHC class II-associated invariant chain peptide replacement by T cell epitopes: engineered invariant chain as a vehicle for directed and enhanced MHC class II antigen processing and presentation. Eur. J. Immunol.28(5), 1524–1533 (1998).
  • Nagata T, Higashi T, Aoshi T et al. Immunization with plasmid DNA encoding MHC class II binding peptide/CLIP-replaced invariant chain (Ii) induces specific helper T cells in vivo: the assessment of Ii p31 and p41 isoforms as vehicles for immunization. Vaccine20(1–2), 105–114 (2001).
  • Hung C-F, Tsai Y-C, He L, Wu T-C. DNA vaccines encoding Ii-PADRE generates potent PADRE-specific CD4(+) T-cell immune responses and enhances vaccine potency. Mol. Ther. DOI:10.1038/mt.sj.6300121 (2007) (Epub ahead of print).
  • Primeau T, Myers NB, Yu YY et al. Applications of major histocompatibility complex class I molecules expressed as single chains. Immunol. Res.32(1–3), 109–121 (2005).
  • Huang CH, Peng S, He L et al. Cancer immunotherapy using a DNA vaccine encoding a single-chain trimer of MHC class I linked to an HPV-16 E6 immunodominant CTL epitope. Gene Ther.12(15), 1180–1186 (2005).
  • Hung CF, Calizo R, Tsai YC, He L, Wu TC. A DNA vaccine encoding a single-chain trimer of HLA-A2 linked to human mesothelin peptide generates anti-tumor effects against human mesothelin-expressing tumors. Vaccine25, 127–135 (2007).
  • Hemmi H, Takeuchi O, Kawai T et al. A Toll-like receptor recognizes bacterial DNA. Nature408(6813), 740–745 (2000).
  • Hartmann G, Weiner GJ, Krieg AM. CpG DNA: a potent signal for growth, activation, and maturation of human dendritic cells. Proc. Natl Acad. Sci. USA96(16), 9305–9310 (1999).
  • Klinman DM, Yamshchikov G, Ishigatsubo Y. Contribution of CpG motifs to the immunogenicity of DNA vaccines. J. Immunol.158(8), 3635–3639 (1997).
  • Coban C, Ishii KJ, Gursel M, Klinman DM, Kumar N. Effect of plasmid backbone modification by different human CpG motifs on the immunogenicity of DNA vaccine vectors. J. Leukoc. Biol.78(3), 647–655 (2005).
  • Zhang A, Jin H, Zhang F et al. Effects of multiple copies of CpG on DNA vaccination. DNA Cell Biol.24(5), 292–298 (2005).
  • Kojima Y, Xin KQ, Ooki T et al. Adjuvant effect of multi-CpG motifs on an HIV-1 DNA vaccine. Vaccine20(23–24), 2857–2865 (2002).
  • Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat. Immunol.5(10), 987–995 (2004).
  • Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature406(6797), 782–787 (2000).
  • Akira S, Takeda K. Toll-like receptor signalling. Nat. Rev. Immunol.4(7), 499–511 (2004).
  • Hemmi H, Kaisho T, Takeuchi O et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol.3(2), 196–200 (2002).
  • Schon MP, Schon M. Immune modulation and apoptosis induction: two sides of the antitumoral activity of imiquimod. Apoptosis9(3), 291–298 (2004).
  • Thomsen LL, Topley P, Daly MG, Brett SJ, Tite JP. Imiquimod and resiquimod in a mouse model: adjuvants for DNA vaccination by particle-mediated immunotherapeutic delivery. Vaccine22(13–14), 1799–1809 (2004).
  • Smorlesi A, Papalini F, Orlando F et al. Imiquimod and S-27609 as adjuvants of DNA vaccination in a transgenic murine model of HER2/neu-positive mammary carcinoma. Gene Ther.12(17), 1324–1332 (2005).
  • Zuber AK, Brave A, Engstrom G et al. Topical delivery of imiquimod to a mouse model as a novel adjuvant for human immunodeficiency virus (HIV) DNA. Vaccine22(13–14), 1791–1798 (2004).
  • Otero M, Calarota SA, Felber B et al. Resiquimod is a modest adjuvant for HIV-1 gag-based genetic immunization in a mouse model. Vaccine22(13–14), 1782–1790 (2004).
  • Ulrich JT, Myers KR. Monophosphoryl lipid A as an adjuvant. Past experiences and new directions. Pharm. Biotechnol.6, 495–524 (1995).
  • Baldridge JR, McGowan P, Evans JT et al. Taking a Toll on human disease: Toll-like receptor 4 agonists as vaccine adjuvants and monotherapeutic agents. Expert Opin. Biol. Ther.4(7), 1129–1138 (2004).
  • Sasaki S, Tsuji T, Hamajima K et al. Monophosphoryl lipid A enhances both humoral and cell-mediated immune responses to DNA vaccination against human immunodeficiency virus type 1. Infect. Immun.65(9), 3520–3528 (1997).
  • Takeshita F, Tanaka T, Matsuda T et al. Toll-like receptor adaptor molecules enhance DNA-raised adaptive immune responses against influenza and tumors through activation of innate immunity. J. Virol.80(13), 6218–6224 (2006).
  • Dow SW, Fradkin LG, Liggitt DH et al. Lipid-DNA complexes induce potent activation of innate immune responses and antitumor activity when administered intravenously. J. Immunol.163(3), 1552–1561 (1999).
  • U’Ren L, Kedl R, Dow S. Vaccination with liposome–DNA complexes elicits enhanced antitumor immunity. Cancer Gene Ther.13(11), 1033–1044 (2006).
  • Gagliardi MC, Sallusto F, Marinaro M et al. Cholera toxin induces maturation of human dendritic cells and licences them for Th2 priming. Eur. J. Immunol.30(8), 2394–2403 (2000).
  • Martin M, Sharpe A, Clements JD, Michalek SM. Role of B7 costimulatory molecules in the adjuvant activity of the heat-labile enterotoxin of Escherichia coli. J. Immunol.169(4), 1744–1752 (2002).
  • Bagley KC, Abdelwahab SF, Tuskan RG, Fouts TR, Lewis GK. Cholera toxin and heat-labile enterotoxin activate human monocyte-derived dendritic cells and dominantly inhibit cytokine production through a cyclic AMP-dependent pathway. Infect. Immun.70(10), 5533–5539 (2002).
  • Rappuoli R, Pizza M, Douce G, Dougan G. Structure and mucosal adjuvanticity of cholera and Escherichia coli heat-labile enterotoxins. Immunol. Today20(11), 493–500 (1999).
  • Williams NA, Hirst TR, Nashar TO. Immune modulation by the cholera-like enterotoxins: from adjuvant to therapeutic. Immunol. Today20(2), 95–101 (1999).
  • Holmgren J, Adamsson J, Anjuere F et al. Mucosal adjuvants and anti-infection and anti-immunopathology vaccines based on cholera toxin, cholera toxin B subunit and CpG DNA. Immunol. Lett.97(2), 181–188 (2005).
  • Arrington J, Braun RP, Dong L et al. Plasmid vectors encoding cholera toxin or the heat-labile enterotoxin from Escherichia coli are strong adjuvants for DNA vaccines. J. Virol.76(9), 4536–4546 (2002).
  • Endo TA, Masuhara M, Yokouchi M et al. A new protein containing an SH2 domain that inhibits JAK kinases. Nature387(6636), 921–924 (1997).
  • Alexander WS. Suppressors of cytokine signalling (SOCS) in the immune system. Nat. Rev. Immunol.2(6), 410–416 (2002).
  • Song XT, Evel-Kabler K, Rollins L et al. An alternative and effective HIV vaccination approach based on inhibition of antigen presentation attenuators in dendritic cells. PLoS Med.3(1), e11 (2006).
  • Lori F, Weiner DB, Calarota SA, Kelly LM, Lisziewicz J. Cytokine-adjuvanted HIV-DNA vaccination strategies. Springer Semin. Immunopathol.28(3), 231–238 (2006).
  • Laddy DJ, Weiner DB. From plasmids to protection: a review of DNA vaccines against infectious diseases. Int. Rev. Immunol.25(3–4), 99–123 (2006).
  • Ferrone CR, Perales MA, Goldberg SM et al. Adjuvanticity of plasmid DNA encoding cytokines fused to immunoglobulin Fc domains. Clin. Cancer Res.12(18), 5511–5519 (2006).
  • Barouch DH, Letvin NL, Seder RA. The role of cytokine DNAs as vaccine adjuvants for optimizing cellular immune responses. Immunological Rev.202, 266–274 (2004).
  • Kim TW, Hung CF, Ling M et al. Enhancing DNA vaccine potency by co-administration of DNA encoding anti-apoptotic proteins. J. Clin. Invest.113(1), 109–117 (2002).
  • Kim TW, Lee JH, He L et al. Modification of professional antigen-presenting cells with small interfering RNA in vivo to enhance cancer vaccine potency. Cancer Res.65(1), 309–316 (2005).
  • Sasaki S, Amara RR, Oran AE, Smith JM, Robinson HL. Apoptosis-mediated enhancement of DNA-raised immune responses by mutant caspases. Nat. Biotechnol.19(6), 543–547 (2001).
  • Rice J, Elliott T, Buchan S, Stevenson FK. DNA fusion vaccine designed to induce cytotoxic T cell responses against defined peptide motifs: implications for cancer vaccines. J. Immunol.167(3), 1558–1565 (2001).
  • Rice J, Buchan S, Stevenson FK. Critical components of a DNA fusion vaccine able to induce protective cytotoxic T cells against a single epitope of a tumor antigen. J. Immunol.169(7), 3908–3913 (2002).
  • Rice J, Buchan S, Dewchand H, Simpson E, Stevenson FK. DNA fusion vaccines induce targeted epitope-specific CTLs against minor histocompatibility antigens from a normal or tolerized repertoire. J. Immunol.173(7), 4492–4499 (2004).
  • Panina-Bordignon P, Tan A, Termijtelen A et al. Universally immunogenic T cell epitopes: promiscuous binding to human MHC class II and promiscuous recognition by T cells. Eur. J. Immunol.19(12), 2237–2242 (1989).
  • Belkaid Y, Rouse BT. Natural regulatory T cells in infectious disease. Nat. Immunol.6(4), 353–360 (2005).
  • Beyer M, Schultze JL. Regulatory T cells in cancer. Blood108(3), 804–811 (2006).
  • Toka FN, Suvas S, Rouse BT. CD4+ CD25+ T cells regulate vaccine-generated primary and memory CD8+ T-cell responses against herpes simplex virus type 1. J. Virol.78(23), 13082–13089 (2004).
  • Cohen AD, Diab A, Perales MA et al. Agonist anti-GITR antibody enhances vaccine-induced CD8+ T-cell responses and tumor immunity. Cancer Res.66(9), 4904–4912 (2006).
  • Nair S, Boczkowski D, Fassnacht M, Pisetsky D, Gilboa E. Vaccination against the forkhead family transcription factor Foxp3 enhances tumor immunity. Cancer Res.67(1), 371–380 (2007).
  • Nayak BP, Sailaja G, Jabbar AM. Augmenting the immunogenicity of DNA vaccines: role of plasmid-encoded Flt-3 ligand, as a molecular adjuvant in genetic vaccination. Virology348(2), 277–288 (2006).
  • Fong CL, Mok CL, Hui KM. Intramuscular immunization with plasmid coexpressing tumour antigen and Flt-3L results in potent tumour regression. Gene Ther.13(3), 245–256 (2006).
  • Sumida SM, McKay PF, Truitt DM et al. Recruitment and expansion of dendritic cells in vivo potentiate the immunogenicity of plasmid DNA vaccines. J. Clin. Invest.114(9), 1334–1342 (2004).
  • Ulmer JB, Wahren B, Liu MA. Gene-based vaccines: recent technical and clinical advances. Trends Mol. Med.12(5), 216–222 (2006).
  • Hejdeman B, Bostrom AC, Matsuda R et al. DNA immunization with HIV early genes in HIV type 1-infected patients on highly active antiretroviral therapy. AIDS Res. Hum. Retroviruses20(8), 860–870 (2004).
  • MacGregor RR, Boyer JD, Ugen KE et al. Plasmid vaccination of stable HIV-positive subjects on antiviral treatment results in enhanced CD8 T-cell immunity and increased control of viral ‘blips’. Vaccine23(17–18), 2066–2073 (2005).
  • Wang R, Doolan DL, Le TP et al. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science282(5388), 476–480 (1998).
  • Le TP, Coonan KM, Hedstrom RC et al. Safety, tolerability and humoral immune responses after intramuscular administration of a malaria DNA vaccine to healthy adult volunteers. Vaccine18(18), 1893–1901 (2000).
  • Wang R, Richie TL, Baraceros MF et al. Boosting of DNA vaccine-elicited γ interferon responses in humans by exposure to malaria parasites. Infect. Immun.73(5), 2863–2872 (2005).
  • McConkey SJ, Reece WH, Moorthy VS et al. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat. Med.9(6), 729–735 (2003).
  • Sheets EE, Urban RG, Crum CP et al. Immunotherapy of human cervical high-grade cervical intraepithelial neoplasia with microparticle-delivered human papillomavirus 16 E7 plasmid DNA. Am. J. Obstet. Gynecol.188(4), 916–926 (2003).
  • Garcia F, Petry KU, Muderspach L et al. ZYC101a for treatment of high-grade cervical intraepithelial neoplasia: a randomized controlled trial. Obstet. Gynecol.103(2), 317–326 (2004).
  • Pavlenko M, Roos AK, Lundqvist A et al. A Phase I trial of DNA vaccination with a plasmid expressing prostate-specific antigen in patients with hormone-refractory prostate cancer. Br. J. Cancer91(4), 688–694 (2004).

Website

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.