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Enhancement of DNA Vaccine-induced Immune Responses by Influenza Virus NP Gene

  • Choi, So-Young (Research Institute, Genexine Co. Ltd.) ;
  • Suh, You-Suk (Research Institute, Genexine Co. Ltd.) ;
  • Cho, Jae-Ho (Garvan Institute of Medical Research) ;
  • Jin, Hyun-Tak (Research Institute, Genexine Co. Ltd.) ;
  • Chang, Jun (Division of Life and Pharmaceutical Sciences, and Center for Cell signaling & Drug Discovery Research, Ewha Womans University) ;
  • Sung, Young-Chul (Research Institute, Genexine Co. Ltd.)
  • Received : 2009.08.05
  • Accepted : 2009.09.02
  • Published : 2009.10.31
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Abstract

DNA immunization induces B and T cell responses to various pathogens and tumors. However, these responses are known to be relatively weak and often transient. Thus, novel strategies are necessary for enhancing immune responses induced by DNA immunization. Here, we demonstrated that co-immunization of influenza virus nucleoprotein (NP) gene significantly enhances humoral and cell-mediated responses to codelivered antigens in mice. We also found that NP DNA coimmunization augments in vivo proliferation of adoptively transferred antigen-specific CD4 and CD8 T cells, which enhanced protective immunity against tumor challenge. Our results suggest that NP DNA can serve as a novel genetic adjuvant in cocktail DNA vaccination.

Keywords

References

  1. Kutzler MA, Weiner DB: DNA vaccines: ready for prime time? Nat Rev Genet 9;776-788, 2008 https://doi.org/10.1038/nrg2432
  2. Liu MA: DNA vaccines: a review. J Intern Med 253;402-410, 2003 https://doi.org/10.1046/j.1365-2796.2003.01140.x
  3. Belakova J, Horynova M, Krupka M, Weigl E, Raska M: DNA vaccines: are they still just a powerful tool for the future? Arch Immunol Ther Exp (Warsz) 55;387-398, 2007 https://doi.org/10.1007/s00005-007-0044-4
  4. Abdulhaqq SA, Weiner DB: DNA vaccines: developing new strategies to enhance immune responses. Immunol Res 42;219-232, 2008 https://doi.org/10.1007/s12026-008-8076-3
  5. Liu MA, Wahren B, Karlsson Hedestam GB: DNA vaccines: recent developments and future possibilities. Hum Gene Ther 17;1051-1061, 2006 https://doi.org/10.1089/hum.2006.17.1051
  6. Lee AH, Suh YS, Sung YC: DNA inoculations with HIV-1 recombinant genomes that express cytokine genes enhance HIV-1 specific immune responses. Vaccine 17;473-479, 1999 https://doi.org/10.1016/S0264-410X(98)00221-7
  7. Suh YS, Ha SJ, Lee CH, Sin JI, Sung YC: Enhancement of VP1-specific immune responses and protection against EMCV-K challenge by co-delivery of IL-12 DNA with VP1 DNA vaccine. Vaccine 19;1891-1898, 2001 https://doi.org/10.1016/S0264-410X(00)00443-6
  8. Yu DH, Li M, Hu XD, Cai H: A combined DNA vaccine enhances protective immunity against Mycobacterium tuberculosis and Brucella abortus in the presence of an IL-12 expression vector. Vaccine 25;6744-6754, 2007 https://doi.org/10.1016/j.vaccine.2007.06.061
  9. Lee SW, Cho JH, Sung YC: Optimal induction of hepatitis C virus envelope-specific immunity by bicistronic plasmid DNA inoculation with the granulocyte-macrophage colony-stimulating factor gene. J Virol 72;8430-8436, 1998
  10. Maksaereekul S, Dubie RA, Shen X, Kieu H, Dean GA, Sparger EE: Vaccination with vif-deleted feline immuno-deficiency virus provirus, GM-CSF, and TNF-alpha plasmids preserves global CD4 T lymphocyte function after challenge with FIV. Vaccine 27;3754-3765, 2009 https://doi.org/10.1016/j.vaccine.2009.03.081
  11. Gomez CE, Najera JL, Sanchez R, Jimenez V, Esteban M: Multimeric soluble CD40 ligand (sCD40L) efficiently enhances HIV specific cellular immune responses during DNA prime and boost with attenuated poxvirus vectors MVA and NYVAC expressing HIV antigens. Vaccine 27;3165-3174, 2009 https://doi.org/10.1016/j.vaccine.2009.03.049
  12. Maue AC, Waters WR, Palmer MV, Whipple DL, Minion FC, Brown WC, Estes DM: CD80 and CD86, but not CD154, augment DNA vaccine-induced protection in experimental bovine tuberculosis. Vaccine 23;769-779, 2004 https://doi.org/10.1016/j.vaccine.2004.07.019
  13. Stone GW, Barzee S, Snarsky V, Kee K, Spina CA, Yu XF, Kornbluth RS: Multimeric soluble CD40 ligand and GITR ligand as adjuvants for human immunodeficiency virus DNA vaccines. J Virol 80;1762-1772, 2006 https://doi.org/10.1128/JVI.80.4.1762-1772.2006
  14. Salgaller ML, Lodge PA: Use of cellular and cytokine adjuvants in the immunotherapy of cancer. J Surg Oncol 68;122-138, 1998 https://doi.org/10.1002/(SICI)1096-9098(199806)68:2<122::AID-JSO10>3.0.CO;2-4
  15. Shiver JW, Fu TM, Chen L, Casimiro DR, Davies ME, Evans RK, Zhang ZQ, Simon AJ, Trigona WL, Dubey SA, Huang L, Harris VA, Long RS, Liang X, Handt L, Schleif WA, Zhu L, Freed DC, Persaud NV, Guan L, Punt KS, Tang A, Chen M, Wilson KA, Collins KB, Heidecker GJ, Fernandez VR, Perry HC, Joyce JG, Grimm KM, Cook JC, Keller PM, Kresock DS, Mach H, Troutman RD, Isopi LA, Williams DM, Xu Z, Bohannon KE, Volkin DB, Montefiori DC, Miura A, Krivulka GR, Lifton MA, Kuroda MJ, Schmitz JE, Letvin NL, Caulfield MJ, Bett AJ, Youil R, Kaslow DC, Emini EA: Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 415;331-335, 2002 https://doi.org/10.1038/415331a
  16. Chaudhry UI, Kingham TP, Plitas G, Katz SC, Raab JR, DeMatteo RP: Combined stimulation with interleukin-18 and CpG induces murine natural killer dendritic cells to produce IFN-gamma and inhibit tumor growth. Cancer Res 66;10497-10504, 2006 https://doi.org/10.1158/0008-5472.CAN-06-1908
  17. Paget C, Bialecki E, Fontaine J, Vendeville C, Mallevaey T, Faveeuw C, Trottein F: Role of invariant NK T lymphocytes in immune responses to CpG oligodeoxynucleotides. J Immunol 182;1846-1853, 2009 https://doi.org/10.4049/jimmunol.0802492
  18. Kojima Y, Xin KQ, Ooki T, Hamajima K, Oikawa T, Shinoda K, Ozaki T, Hoshino Y, Jounai N, Nakazawa M, Klinman D, Okuda K: Adjuvant effect of multi-CpG motifs on an HIV-1 DNA vaccine. Vaccine 20;2857-2865, 2002 https://doi.org/10.1016/S0264-410X(02)00238-4
  19. Sato Y, Roman M, Tighe H, Lee D, Corr M, Nguyen MD, Silverman GJ, Lotz M, Carson DA, Raz E: Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science 273;352-354, 1996 https://doi.org/10.1126/science.273.5273.352
  20. Seaman MS, Xu L, Beaudry K, Martin KL, Beddall MH, Miura A, Sambor A, Chakrabarti BK, Huang Y, Bailer R, Koup RA, Mascola JR, Nabel GJ, Letvin NL: Multiclade human immunodeficiency virus type 1 envelope immunogens elicit broad cellular and humoral immunity in rhesus monkeys. J Virol 79;2956-2963, 2005 https://doi.org/10.1128/JVI.79.5.2956-2963.2005
  21. Kjerrstrom A, Hinkula J, Engstrom G, Ovod V, Krohn K, Benthin R, Wahren B: Interactions of single and combined human immunodeficiency virus type 1 (HIV-1) DNA vaccines. Virology 284;46-61, 2001 https://doi.org/10.1006/viro.2001.0905
  22. Grifantini R, Finco O, Bartolini E, Draghi M, Del Giudice G, Kocken C, Thomas A, Abrignani S, Grandi G: Multi-plasmid DNA vaccination avoids antigenic competition and enhances immunogenicity of a poorly immunogenic plasmid. Eur J Immunol 28;1225-1232, 1998 https://doi.org/10.1002/(SICI)1521-4141(199804)28:04<1225::AID-IMMU1225>3.0.CO;2-6
  23. Sin JI, Sung JH, Suh YS, Lee AH, Chung JH, Sung YC: Protective immunity against heterologous challenge with encephalomyocarditis virus by VP1 DNA vaccination: effect of coinjection with a granulocyte-macrophage colony stimulating factor gene. Vaccine 15;1827-1833, 1997 https://doi.org/10.1016/S0264-410X(97)88856-1
  24. Song MK, Lee SW, Suh YS, Lee KJ, Sung YC: Enhancement of immunoglobulin G2a and cytotoxic T-lymphocyte responses by a booster immunization with recombinant hepatitis C virus E2 protein in E2 DNA-primed mice. J Virol 74;2920-2925, 2000 https://doi.org/10.1128/JVI.74.6.2920-2925.2000
  25. Power CA, Grand CL, Ismail N, Peters NC, Yurkowski DP, Bretscher PA: A valid ELISPOT assay for enumeration of ex vivo, antigen-specific, IFNgamma-producing T cells. J Immunol Methods 227;99-107, 1999 https://doi.org/10.1016/S0022-1759(99)00074-5
  26. Kurts C, Miller JF, Subramaniam RM, Carbone FR, Heath WR: Major histocompatibility complex class I-restricted cross-presentation is biased towards high dose antigens and those released during cellular destruction. J Exp Med 188;409-414, 1998 https://doi.org/10.1084/jem.188.2.409
  27. Bot A, Bot S, Bona C: Enhanced protection against influenza virus of mice immunized as newborns with a mixture of plasmids expressing hemagglutinin and nucleoprotein. Vaccine 16;1675-1682, 1998 https://doi.org/10.1016/S0264-410X(98)00054-1
  28. Murali-Krishna K, Altman JD, Suresh M, Sourdive DJ, Zajac AJ, Miller JD, Slansky J, Ahmed R: Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8;177-187, 1998 https://doi.org/10.1016/S1074-7613(00)80470-7
  29. Kaech SM, Wherry EJ, Ahmed R: Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2;251-262, 2002 https://doi.org/10.1038/nri778
  30. Li M, Davey GM, Sutherland RM, Kurts C, Lew AM, Hirst C, Carbone FR, Heath WR: Cell-associated ovalbumin is cross-presented much more efficiently than soluble ovalbumin in vivo. J Immunol 166;6099-6103, 2001 https://doi.org/10.4049/jimmunol.166.10.6099
  31. Fu TM, Guan L, Friedman A, Schofield TL, Ulmer JB, Liu MA, Donnelly JJ: Dose dependence of CTL precursor frequency induced by a DNA vaccine and correlation with protective immunity against influenza virus challenge. J Immunol 162;4163-4170, 1999
  32. Justewicz DM, Morin MJ, Robinson HL, Webster RG: Antibody-forming cell response to virus challenge in mice immunized with DNA encoding the influenza virus hemagglutinin. J Virol 69;7712-7717, 1995
  33. Fu TM, Friedman A, Ulmer JB, Liu MA, Donnelly JJ: Protective cellular immunity: cytotoxic T-lymphocyte responses against dominant and recessive epitopes of influenza virus nucleoprotein induced by DNA immunization. J Virol 71;2715-2721, 1997
  34. Lee SW, Youn JW, Seong BL, Sung YC: IL-6 induces long-term protective immunity against a lethal challenge of influenza virus. Vaccine 17;490-496, 1999 https://doi.org/10.1016/S0264-410X(98)00223-0
  35. Chen W, Anton LC, Bennink JR, Yewdell JW: Dissecting the multifactorial causes of immunodominance in class I-restricted T cell responses to viruses. Immunity 12;83-93, 2000 https://doi.org/10.1016/S1074-7613(00)80161-2
  36. Potter P, Tourdot S, Blanchard T, Smith GL, Gould KG: Differential processing and presentation of the H-2D(b)-restricted epitope from two different strains of influenza virus nucleoprotein. J Gen Virol 82;1069-1074, 2001 https://doi.org/10.1099/0022-1317-82-5-1069
  37. Yewdell JW, Bennink JR: Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 17;51-88, 1999 https://doi.org/10.1146/annurev.immunol.17.1.51
  38. Krieg AM: CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 20;709-760, 2002 https://doi.org/10.1146/annurev.immunol.20.100301.064842
  39. Fomsgaard A, Nielsen HV, Bryder K, Nielsen C, Machuca R, Bruun L, Hansen J, Buns S: Improved humoral and cellular immune responses against the gp120 V3 loop of HIV-1 following genetic immunization with a chimeric DNA vaccine encoding the V3 inserted into the hepatitis B surface antigen. Scand J Immunol 47(4);289-295, 1998 https://doi.org/10.1046/j.1365-3083.1998.00323.x
  40. Cella M, Scheidegger D, Palmer-Lehmann K, Lane P, Lanzavecchia A, Alber G: Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med 184(2);747-752, 1996 https://doi.org/10.1084/jem.184.2.747
  41. Ramanathan S, Gagnon J, Ilangumaran S: Antigen-nonspecific activation of CD8+ T lymphocytes by cytokines: relevance to immunity, autoimmunity, and cancer. Arch Immunol Ther Exp (Warsz) 56(5);311-323, 2008 https://doi.org/10.1007/s00005-008-0033-2

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