Recent advances towards the clinical application of DNA vaccines

Netherlands Journal of Medicine

Volumn 71, Issue 3, 2013, Pages 109-117

  Bins, A D ^a   van den Berg, J H ^a   Oosterhuis, K ^b   Haanen, J B A G ^a  

^a ANTONI VAN LEEUWENHOEK HOSPITAL   (Netherlands)

^b CRUCELL HOLLAND BV   (Netherlands)

Author keywords

Cancer vaccination; DNA vaccination; Infection diseases

Indexed keywords

B7 ANTIGEN; CALRETICULIN; CD40 ANTIGEN; CD86 ANTIGEN; CHAPERONIN 60; DNA VACCINE; FLT3 LIGAND; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HEAT SHOCK PROTEIN 70; HEPATITIS B VACCINE; INTERLEUKIN 8; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; N (4 METHOXYPHENYLACETYL) DEHYDROALANINE; N (4 METHOXYPHENYLACETYL)DEHYDROALANINE; PATTERN RECOGNITION RECEPTOR; PLASMID DNA; PROTEIN E6; PROTEIN E7; PROTEIN VP22; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; WEST NILE VACCINE;

ADENOVIRUS INFECTION; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELLULAR IMMUNITY; CLINICAL TRIAL (TOPIC); DNA IMMUNIZATION; DNA SEQUENCE; DRUG EFFICACY; DRUG SAFETY; ELECTROPORATION; ENDOCYTOSIS; GENETIC IMMUNIZATION; HUMAN; IMMUNE RESPONSE; MELANOMA; NEOPLASM; NONHUMAN; REVIEW; T LYMPHOCYTE ACTIVATION; TUMOR SUPPRESSOR GENE; VACCINATION;

HUMANS; NEOPLASMS; VACCINATION; VACCINES, DNA;

EID: 84878326123     PISSN: 03002977     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (75)

1. Davis BS, Chang GJ, Cropp B, et al. West Nile virus recombinant DNA vaccine protects mouse and horse from virus challenge and expresses in vitro a noninfectious recombinant antigen that can be used in enzyme-linked immunosorbent assays. J Virol. 2001;75:4040-7.
2. Kilpatrick AM, Dupuis AP, Chang G-JJ, Kramer LD. DNA vaccination of American robins (Turdus migratorius) against West Nile virus. Vector Borne Zoonotic Dis. 2010;10:377-80.
3. Bergman PJ, McKnight J, Novosad A, et al. Long-term survival of dogs with advanced malignant melanoma after DNA vaccination with xenogeneic human tyrosinase: a phase I trial. Clin Cancer Res. 2003;9:1284-90.
4. Liao JCF, Gregor P, Wolchok JD, et al. Vaccination with human tyrosinase DNA induces antibody responses in dogs with advanced melanoma. Cancer Immun. 2006;6:8.
5. Naked Plasmid DNA Formulation: Effect of Different Disaccharides on Stability after Lyophilisation. AAPS Pharm Sci Tech. 2010;11:344-50.
6. Dudley ME, Wunderlich JR, Robbins PF, et al. Cancer Regression and Autoimmunity in Patients After Clonal Repopulation with Antitumor Lymphocytes. Science. 2002;298:850-4.
7. Ahmed R, Akondy RS. Insights into human CD8(+) T-cell memory using the yellow fever and smallpox vaccines. Immunol Cell Biol. 2011;89:340-5.
8. Gudmundsdotter L, Nilsson C, Brave A, et al. Recombinant Modified Vaccinia Ankara (MVA) effectively boosts DNA-primed HIV-specific immune responses in humans despite pre-existing vaccinia immunity. Vaccine. 2009;27:4468-74.
9. Frahm N, DeCamp AC, Friedrich DP, et al. Human adenovirus-specific T cells modulate HIV-specific T cell responses to an Ad5-vectored HIV-1 vaccine. J Clin Invest. 2012;122:359-67.
10. Walsh SR, Seaman MS, Grandpre LE, et al. Impact of anti-orthopoxvirus neutralizing antibodies induced by a heterologous prime-boost HIV-1 vaccine on insert-specific immune responses. Vaccine. 2012;31:114-9.
11. Buchbinder SP, Mehrotra DV, Duerr A, et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet. 2008;372:1881-93.
12. Duerr A, Huang Y, Buchbinder S, et al. Extended follow-up confirms early vaccine-enhanced risk of HIV acquisition and demonstrates waning effect over time among participants in a randomized trial of recombinant adenovirus HIV vaccine (Step study). J Infect Dis. In press.
13. Blackman MA, Woodland DL. The narrowing of the CD8 T cell repertoire in old age. Curr. Opin Immunol. 2011;23:537-42.
14. 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. 2003;4:907-12.
15. Loirat D, Li Z, Mancini M, Tiollais P, Paulin D, Michel ML. Muscle-specific expression of hepatitis B surface antigen: no effect on DNA-raised immune responses. Virology. 1999;260:74-83.
16. Babiuk S, Mookherjee N, Pontarollo R, et al. TLR9-/-and TLR9+/+ mice display similar immune responses to a DNA vaccine. Immunology. 2004;113:114-20.
17. Tudor D, Dubuquoy C, Gaboriau V, Lefèvre F, Charley B, Riffault S. TLR9 pathway is involved in adjuvant effects of plasmid DNA-based vaccines. Vaccine. 2005;23:1258-64.
18. 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. 2003;171:5908-12.
19. Hornung V, Ablasser A, Charrel-Dennis M, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature. 2009;458:514-8.
20. Liu MA. DNA vaccines: an historical perspective and view to the future. Immunol Rev. 2011;239:62-84.
21. Liu MA, Ulmer JB. Human clinical trials of plasmid DNA vaccines. Adv Genet. 2005;55:25-40.
22. Wang R, Doolan DL, Le TP, et al. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science. 1998;282:476-80.
23. Rottinghaus ST, Poland GA, Jacobson RM, Barr LJ, Roy MJ. Hepatitis B DNA vaccine induces protective antibody responses in human non-responders to conventional vaccination. Vaccine. 2003;21:4604-8.
24. Low L, Mander A, McCann K, et al. DNA vaccination with electroporation induces increased antibody responses in patients with prostate cancer. Hum Gene Ther. 2009;20:1269-78.
25. Roy MJ, Wu MS, Barr LJ, et al. Induction of antigen-specific CD8+ T cells, T helper cells, and protective levels of antibody in humans by particlemediated administration of a hepatitis B virus DNA vaccine. Vaccine. 2000;19:764-78.
26. Chudley L, McCann K, Mander A, et al. DNA fusion-gene vaccination in patients with prostate cancer induces high-frequency CD8(+) T-cell responses and increases PSA doubling time. Cancer Immunol Immunother. 2012;61:2161-70.
27. Calarota SA, Leandersson AC, Bratt G, et al. Immune responses in asymptomatic HIV-1-infected patients after HIV-DNA immunization followed by highly active antiretroviral treatment. J Immunol. 1999;163:2330-8.
28. Asmuth DM, Brown EL, DiNubile MJ, et al. Comparative cell-mediated immunogenicity of DNA/DNA, DNA/adenovirus type 5 (Ad5), or Ad5/ Ad5 HIV-1 clade B gag vaccine prime-boost regimens. J Infect Dis. 2010;201:132-41.
29. 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 2010;5:e12873.
30. Kibuuka H, Kimutai R, Maboko L, et al. A phase 1/2 study of a multiclade HIV-1 DNA plasmid prime and recombinant adenovirus serotype 5 boost vaccine in HIV-Uninfected East Africans (RV 172). J Infect Dis. 2010;201:600-7.
31. Cebere I, Dorrell L, McShane H, et al. Phase I clinical trial safety of DNAand modified virus Ankara-vectored human immunodeficiency virus type 1 (HIV-1) vaccines administered alone and in a prime-boost regime to healthy HIV-1-uninfected volunteers. Vaccine. 2006;24:417-25.
32. Goonetilleke N, Moore S, Dally L, et al. Induction of multifunctional human immunodeficiency virus type 1 (HIV-1)-specific T cells capable of proliferation in healthy subjects by using a prime-boost regimen of DNAand modified vaccinia virus Ankara-vectored vaccines expressing HIV-1 Gag coupled to CD8+ T-cell epitopes. J Virol. 2006;80:4717-28.
33. Guimarães-Walker A, Mackie N, et al. Lessons from IAVI-006, a phase I clinical trial to evaluate the safety and immunogenicity of the pTHr. HIVA DNA and MVA. HIVA vaccines in a prime-boost strategy to induce HIV-1 specific T-cell responses in healthy volunteers. Vaccine. 2008;26:6671-7.
34. Jaoko W, Nakwagala FN, Anzala O, et al. Safety and immunogenicity of recombinant low-dosage HIV-1 A vaccine candidates vectored by plasmid pTHr DNA or modified vaccinia virus Ankara (MVA) in humans in East Africa. Vaccine. 2008;26:2788-95.
35. Peters BS, Jaoko W, Vardas E, et al. Studies of a prophylactic HIV-1 vaccine candidate based on modified vaccinia virus Ankara (MVA) with and without DNA priming: effects of dosage and route on safety and immunogenicity. Vaccine. 2007;25:2120-7.
36. Sandström E, Nilsson C, Hejdeman B, et al. Broad immunogenicity of a multigene, multiclade HIV-1 DNA vaccine boosted with heterologous HIV-1 recombinant modified vaccinia virus Ankara. J Infect Dis. 2008;198:1482-90.
37. Dunachie SJ, Walther M, Epstein JE, et al. A DNA prime-modified vaccinia virus ankara boost vaccine encoding thrombospondin-related adhesion protein but not circumsporozoite protein partially protects healthy malaria-naive adults against Plasmodium falciparum sporozoite challenge. Infect Immun. 2006;74:5933-42.
38. Moorthy VS, Imoukhuede EB, Milligan P, et al. A randomised, double-blind, controlled vaccine efficacy trial of DNA/MVA ME-TRAP against malaria infection in Gambian adults. PLoS Med. 2004;1:e33.
39. Vuola JM, Keating S, Webster DP, et al. Differential immunogenicity of various heterologous prime-boost vaccine regimens using DNA and viral vectors in healthy volunteers. J Immunol. 2005;174:449-55.
40. Vardas E, Stanescu I, Leinonen M, et al. Indicators of therapeutic effect in FIT-06, a Phase II trial of a DNA vaccine, GTU(®)-Multi-HIVB, in untreated HIV-1 infected subjects. Vaccine. 2012;30:4046-54.
41. Kalams SA, Parker S, Jin X, et al. Safety and immunogenicity of an HIV-1 gag DNA vaccine with or without IL-12 and/or IL-15 plasmid cytokine adjuvant in healthy, HIV-1 uninfected adults. PLoS ONE. 2012;7:e29231.
42. Bagarazzi ML, Yan J, Morrow MP, et al. Immunotherapy Against HPV16/18 Generates Potent TH1 and Cytotoxic Cellular Immune Responses. Sci Transl Med. 2012;4:155-138.
43. Cole J, Skopek TR. International Commission for Protection Against Environmental Mutagens and Carcinogens. Working paper no. 3. Somatic mutant frequency, mutation rates and mutational spectra in the human population in vivo. Mutat Res. 1994;304:33-105.
44. Pal R, Yu Q, Wang S, et al. Definitive toxicology and biodistribution study of a polyvalent DNA prime/protein boost human immunodeficiency virus type 1 (HIV-1) vaccine in rabbits. Vaccine. 2006;24:1225-34.
45. Manam S, Ledwith BJ, Barnum AB, et al. Plasmid DNA vaccines: tissue distribution and effects of DNA sequence, adjuvants and delivery method on integration into host DNA. Intervirology. 2000;43:273-81.
46. Martin T, Parker SE, Hedstrom R, et al. Plasmid DNA malaria vaccine: the potential for genomic integration after intramuscular injection. Hum Gene Ther. 1999;10:759-68.
47. Nichols WW, Ledwith BJ, Manam SV, Troilo PJ. Potential DNA vaccine integration into host cell genome. Ann N Y Acad Sci. 1995;772:30-9.
48. Wang Z, Troilo PJ, Wang X, et al. Detection of integration of plasmid DNA into host genomic DNA following intramuscular injection and electroporation. Gene Ther. 2004;11:711-21.
49. Sheets RL, Stein J, Manetz TS, et al. Biodistribution of DNA plasmid vaccines against HIV-1, Ebola, Severe Acute Respiratory Syndrome, or West Nile virus is similar, without integration, despite differing plasmid backbones or gene inserts. Toxicol Sci. 2006;91:610-9.
50. Ulmer JB, Mason PW, Geall A, Mandl CW. RNA-based vaccines. Vaccine. 2012;30:4414-8.
51. Gao Y-S, Huang T-H, Wang D, Xie Q-D, Kang X-J. In vivo study on vertical transmission of the HIV-1 gag gene via mouse oocytes. Curr HIV Res. 2009;7:562-8.
52. Jones S, Evans K, McElwaine-Johnn H, et al. DNA vaccination protects against an influenza challenge in a double-blind randomised placebocontrolled phase 1b clinical trial. Vaccine. 2009;27:2506-12.
53. Bahloul C, Taieb D, Diouani MF, et al. Field trials of a very potent rabies DNA vaccine which induced long lasting virus neutralizing antibodies and protection in dogs in experimental conditions. Vaccine. 2006;24:1063-72.
54. Taniyama Y, Tachibana K, Hiraoka K, et al. Development of safe and efficient novel nonviral gene transfer using ultrasound: enhancement of transfection efficiency of naked plasmid DNA in skeletal muscle. Gene Ther. 2002;9:372-80.
55. Prow TW, Chen X, Prow NA, et al. Nanopatch-targeted skin vaccination against West Nile Virus and Chikungunya virus in mice. Small. 2010;6:1776-84.
56. 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. 2005;11:899-904.
57. Verstrepen BE, Bins AD, Rollier CS, et al. Improved HIV-1 specific T-cell responses by short-interval DNA tattooing as compared to intramuscular immunization in non-human primates. Vaccine. 2008;26:3346-51.
58. Van den Berg JH, Nuijen B, Schumacher TN, et al. Synthetic vehicles for DNA vaccination. J Drug Target. 2010;18:1-14.
59. Loudon PT, Yager EJ, Lynch DT, et al. GM-CSF increases mucosal and systemic immunogenicity of an H1N1 influenza DNA vaccine administered into the epidermis of non-human primates. PLoS ONE 2010;5:e11021.
60. Katae M, Miyahira Y, Takeda K, et al. Coadministration of an interleukin-12 gene and a Trypanosoma cruzi gene improves vaccine efficacy. Infect Immun. 2002;70:4833-40.
61. Eickhoff CS, Vasconcelos JR, Sullivan NL, et al. Co-administration of a plasmid DNA encoding IL-15 improves long-term protection of a genetic vaccine against Trypanosoma cruzi. PLoS Negl Trop Dis. 2011;5:e983.
62. Fagone P, Shedlock DJ, Bao H, et al. Molecular adjuvant HMGB1 enhances anti-influenza immunity during DNA vaccination. Gene Therapy. 2011;18:1070-7.
63. Ko H-J, Ko S-Y, Kim Y-J, Lee E-G, Cho S-N, Kang C-Y. Optimization of Codon Usage Enhances the Immunogenicity of a DNA Vaccine Encoding Mycobacterial Antigen Ag85B. Infect Immun. 2005;73:5666-74.
64. Brulet J-M, Maudoux F, Thomas S, et al. DNA vaccine encoding endosome-targeted human papillomavirus type 16 E7 protein generates CD4+ T cell-dependent protection. Eur J Immunol. 2007;37:376-84.
65. Ji H, Wang T-L, Chen C-H, et al. Targeting Human Papillomavirus Type 16 E7 to the Endosomal/Lysosomal Compartment Enhances the Antitumor Immunity of DNA Vaccines against Murine Human Papillomavirus Type 16 E7-Expressing Tumors. Hum Gene Ther. 1999;10:2727-40.
66. Uchijima M, Yoshida A, Nagata T, Koide Y. Optimization of codon usage of plasmid DNA vaccine is required for the effective MHC class I-restricted T cell responses against an intracellular bacterium. J Immunol. 1998;161:5594-9.
67. Loera-Arias MJ, Martínez-Pérez AG, Barrera-Hernández A, et al. Targeting and retention of HPV16 E7 to the endoplasmic reticulum enhances immune tumour protection. J Cell Mol Med. 2010;14:890-4.
68. Deliyannis G, Boyle JS, Brady JL, Brown LE, Lew AM. A fusion DNA vaccine that targets antigen-presenting cells increases protection from viral challenge. Proc Natl Acad Sci. U.S.A. 2000;97:6676-80.
69. Michel N, Osen W, Gissmann L, Schumacher TN., Zentgraf H, Müller M. Enhanced Immunogenicity of HPV 16 E7 Fusion Proteins in DNA Vaccination. Virology. 2002;294:47-59.
70. Šmahel M, Pokorná D, Macková J, Vlasák J. Enhancement of immunogenicity of HPV16 E7 oncogene by fusion with E. coli o-glucuronidase. J Gene Med. 2004;6:1092-101.
71. Oosterhuis K, Öhlschläger P, Van den Berg JH, et al. Preclinical development of highly effective and safe DNA vaccines directed against HPV 16 E6 and E7. Int J Cancer. 2011;129:397-406.
72. Bins AD, Wolkers MC, Van den Boom MD, Haanen JBAG, Schumacher TNM. In Vivo Antigen Stability Affects DNA Vaccine Immunogenicity. J Immunol. 2007;179:2126-33.
73. Wolkers MC, Brouwenstijn N, Bakker AH, Toebes M, Schumacher TNM. Antigen bias in T cell cross-priming. Science. 2004;304:1314-7.
74. Oosterhuis K, Aleyd E, Vrijland K, Schumacher TN, Haanen JB. Rational Design of DNA Vaccines for the Induction of Human Papillomavirus Type 16 E6-and E7-Specific Cytotoxic T-Cell Responses. Hum Gene Ther. 2012;23:1301-12.
75. Isaji K, Kawase A, Matono M, Guan X, Nishikawa M, Takakura Y. Enhanced CTL response by controlled intracellular trafficking of antigen in dendritic cells following DNA vaccination. J Control Release. 2009;135:227-33.