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The Korean Association of Immunobiologists (대한면역학회)
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Codelivery of IL-7 Augments Multigenic HCV DNA Vaccine-induced Antibody as well as Broad T Cell Responses in Cynomolgus Monkeys

  • Park, Su-Hyung (Division of Molecular and Life Science, Integrative Bioscience and Biotechnology, WCU, Pohang University of Science and Technology(POSTECH)) ;
  • Song, Mi-Young (Division of Molecular and Life Science, Integrative Bioscience and Biotechnology, WCU, Pohang University of Science and Technology(POSTECH)) ;
  • Nam, Hyo-Jung (Division of Molecular and Life Science, Integrative Bioscience and Biotechnology, WCU, Pohang University of Science and Technology(POSTECH)) ;
  • Im, Se-Jin (Division of Molecular and Life Science, Integrative Bioscience and Biotechnology, WCU, Pohang University of Science and Technology(POSTECH)) ;
  • Sung, Young-Chul (Division of Molecular and Life Science, Integrative Bioscience and Biotechnology, WCU, Pohang University of Science and Technology(POSTECH))
  • Received : 2010.10.29
  • Accepted : 2010.11.12
  • Published : 2010.12.31
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Abstract

Background: A crucial limitation of DNA vaccines is its weak immunogenicity, especially in terms of eliciting antibody responses in non-human primates or humans; therefore, it is essential to enhance immune responses to vaccination for the development of successful DNA vaccines for humans. Methods: Here, we approached this issue by evaluating interleukin-7 (IL-7) as a genetic adjuvant in cynomolgus monkeys immunized with multigenic HCV DNA vaccine. Results: Codelivery of human IL-7 (hIL-7)-encoding DNA appeared to increase DNA vaccine-induced antibody responses specific for HCV E2 protein, which plays a critical role in protecting from HCV infection. HCV-specific T cell responses were also significantly enhanced by codelivery of hIL-7 DNA. Interestingly, the augmentation of T cell responses by codelivery of hIL-7 DNA was shown to be due to the enhancement of both the breadth and magnitude of immune responses against dominant and subdominant epitopes. Conclusion: Taken together, these findings suggest that the hIL-7-expressing plasmid serves as a promising vaccine adjuvant capable of eliciting enhanced vaccine-induced antibody and broad T cell responses.

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References

  1. Kiyosawa K, Tanaka E, Sodeyama T, Furuta K, Usuda S, Yousuf M, Furuta S: Transition of antibody to hepatitis C virus from chronic hepatitis to hepatocellular carcinoma. Jpn J Cancer Res 81;1089-1091, 1990 https://doi.org/10.1111/j.1349-7006.1990.tb02517.x
  2. Alter MJ, Kruszon-Moran D, Nainan OV, McQuillan GM, Gao F, Moyer LA, Kaslow RA, Margolis HS: The prevalence of hepatitis C virus infection in the United States, 1988 through 1994. N Engl J Med 341;556-562, 1999 https://doi.org/10.1056/NEJM199908193410802
  3. Nascimbeni M, Mizukoshi E, Bosmann M, Major ME, Mihalik K, Rice CM, Feinstone SM, Rehermann B: Kinetics of CD4+ and CD8+ memory T-cell responses during hepatitis C virus rechallenge of previously recovered chimpanzees. J Virol 77;4781-4793, 2003 https://doi.org/10.1128/JVI.77.8.4781-4793.2003
  4. Lanford RE, Guerra B, Chavez D, Bigger C, Brasky KM, Wang XH, Ray SC, Thomas DL: Cross-genotype immunity to hepatitis C virus. J Virol 78;1575-1581, 2004 https://doi.org/10.1128/JVI.78.3.1575-1581.2004
  5. Folgori A, Capone S, Ruggeri L, Meola A, Sporeno E, Ercole BB, Pezzanera M, Tafi R, Arcuri M, Fattori E, Lahm A, Luzzago A, Vitelli A, Colloca S, Cortese R, Nicosia A: A T-cell HCV vaccine eliciting effective immunity against heterologous virus challenge in chimpanzees. Nat Med 12;190- 197, 2006 https://doi.org/10.1038/nm1353
  6. Youn JW, Park SH, Lavillette D, Cosset FL, Yang SH, Lee CG, Jin HT, Kim CM, Shata MT, Lee DH, Pfahler W, Prince AM, Sung YC: Sustained E2 antibody response correlates with reduced peak viremia after hepatitis C virus infection in the chimpanzee. Hepatology 42;1429-1436, 2005 https://doi.org/10.1002/hep.20934
  7. Forns X, Payette PJ, Ma X, Satterfield W, Eder G, Mushahwar IK, Govindarajan S, Davis HL, Emerson SU, Purcell RH, Bukh J: Vaccination of chimpanzees with plasmid DNA encoding the hepatitis C virus (HCV) envelope E2 protein modified the infection after challenge with homologous monoclonal HCV. Hepatology 32;618-625, 2000
  8. Pertmer TM, Roberts TR, Haynes JR: Influenza virus nucleoprotein- specific immunoglobulin G subclass and cytokine responses elicited by DNA vaccination are dependent on the route of vector DNA delivery. J Virol 70;6119-6125, 1996
  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 U S A 90;11478-11482, 1993 https://doi.org/10.1073/pnas.90.24.11478
  10. Choi SY, Suh YS, Cho JH, Jin HT, Chang J, Sung YC: Enhancement of DNA vaccine-induced immune responses by influenza virus NP gene. Immune Netw 9;169-178, 2009 https://doi.org/10.4110/in.2009.9.5.169
  11. Barouch DH, Letvin NL, Seder RA: The role of cytokine DNAs as vaccine adjuvants for optimizing cellular immune responses. Immunol Rev 202;266-274, 2004 https://doi.org/10.1111/j.0105-2896.2004.00200.x
  12. Appasamy PM: Biological and clinical implications of interleukin- 7 and lymphopoiesis. Cytokines Cell Mol Ther 5;25- 39, 1999
  13. Faltynek CR, Wang S, Miller D, Young E, Tiberio L, Kross K, Kelley M, Kloszewski E: Administration of human recombinant IL-7 to normal and irradiated mice increases the numbers of lymphocytes and some immature cells of the myeloid lineage. J Immunol 149;1276-1282, 1992
  14. Komschlies KL, Gregorio TA, Gruys ME, Back TC, Faltynek CR, Wiltrout RH: Administration of recombinant human IL-7 to mice alters the composition of B-lineage cells and T cell subsets, enhances T cell function, and induces regression of established metastases. J Immunol 152;5776-5784, 1994
  15. Morrissey PJ, Goodwin RG, Nordan RP, Anderson D, Grabstein KH, Cosman D, Sims J, Lupton S, Acres B, Reed SG: Recombinant interleukin 7, pre-B cell growth factor, has costimulatory activity on purified mature T cells. J Exp Med 169;707-716, 1989 https://doi.org/10.1084/jem.169.3.707
  16. Alderson MR, Sassenfeld HM, Widmer MB: Interleukin 7 enhances cytolytic T lymphocyte generation and induces lymphokine- activated killer cells from human peripheral blood.J Exp Med 172;577-587, 1990 https://doi.org/10.1084/jem.172.2.577
  17. Schluns KS, Kieper WC, Jameson SC, Lefrancois L: Interleukin-7 mediates the homeostasis of naïve and memory CD8 T cells in vivo. Nat Immunol 1;426-432, 2000 https://doi.org/10.1038/80868
  18. Tan JT, Dudl E, LeRoy E, Murray R, Sprent J, Weinberg KI, Surh CD: IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci U S A 98;8732-8737, 2001 https://doi.org/10.1073/pnas.161126098
  19. Boise LH, Minn AJ, June CH, Lindsten T, Thompson CB: Growth factors can enhance lymphocyte survival without committing the cell to undergo cell division. Proc Natl Acad Sci U S A 92;5491-5495, 1995 https://doi.org/10.1073/pnas.92.12.5491
  20. Maeurer MJ, Trinder P, Hommel G, Walter W, Freitag K, Atkins D, Störkel S: Interleukin-7 or interleukin-15 enhances survival of Mycobacterium tuberculosis-infected mice. Infect Immun 68;2962-2970, 2000 https://doi.org/10.1128/IAI.68.5.2962-2970.2000
  21. Sin JI, Kim J, Pachuk C, Weiner DB: Interleukin 7 can enhance antigen-specific cytotoxic-T-lymphocyte and/or Th2- type immune responses in vivo. Clin Diagn Lab Immunol 7;751-758, 2000
  22. Calarota SA, Dai A, Trocio JN, Weiner DB, Lori F, Lisziewicz J: IL-15 as memory T-cell adjuvant for topical HIV-1 DermaVir vaccine. Vaccine 26;5188-5195, 2008 https://doi.org/10.1016/j.vaccine.2008.03.067
  23. Melchionda F, Fry TJ, Milliron MJ, McKirdy MA, Tagaya Y, Mackall CL: Adjuvant IL-7 or IL-15 overcomes immunodominance and improves survival of the CD8+ memory cell pool. J Clin Invest 115;1177-1187, 2005 https://doi.org/10.1172/JCI200523134
  24. Geiselhart LA, Humphries CA, Gregorio TA, Mou S, Subleski J, Komschlies KL: IL-7 administration alters the CD4:CD8 ratio, increases T cell numbers, and increases T cell function in the absence of activation. J Immunol 166;3019-3027, 2001 https://doi.org/10.4049/jimmunol.166.5.3019
  25. Lee KJ, Suh YA, Cho YG, Cho YS, Ha GW, Chung KH, Hwang JH, Yun YD, Lee DS, Kim CM, Sung YC: Hepatitis C virus E2 protein purified from mammalian cells is frequently recognized by E2-specific antibodies in patient sera. J Biol Chem 272;30040-30046, 1997 https://doi.org/10.1074/jbc.272.48.30040
  26. Sheehan JJ, Tsirka SE: Fibrin-modifying serine proteases thrombin, tPA, and plasmin in ischemic stroke: a review. Glia 50;340-350, 2005 https://doi.org/10.1002/glia.20150
  27. Youn JW, Park SH, Cho JH, Sung YC: Optimal induction of T-cell responses against hepatitis C virus E2 by antigen engineering in DNA immunization. J Virol 77;11596-11602, 2003 https://doi.org/10.1128/JVI.77.21.11596-11602.2003
  28. Park SH, Yang SH, Lee CG, Youn JW, Chang J, Sung YC: Efficient induction of T helper 1 CD4+ T-cell responses to hepatitis C virus core and E2 by a DNA prime-adenovirus boost. Vaccine 21;4555-4564, 2003 https://doi.org/10.1016/S0264-410X(03)00499-7
  29. Park SH, Lee SR, Hyun BH, Kim BM, Sung YC: Codelivery of PEG-IFN-alpha inhibits HCV DNA vaccine-induced T cell responses but not humoral responses in African green monkeys. Vaccine 26;3978-3983, 2008 https://doi.org/10.1016/j.vaccine.2008.05.017
  30. Ma A, Koka R, Burkett P: Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 24;657-679, 2006 https://doi.org/10.1146/annurev.immunol.24.021605.090727
  31. Sinha ML, Fry TJ, Fowler DH, Miller G, Mackall CL: Interleukin 7 worsens graft-versus-host disease. Blood 100;2642-2649, 2002 https://doi.org/10.1182/blood-2002-04-1082
  32. Milne CD, Paige CJ: IL-7: a key regulator of B lymphopoiesis. Semin Immunol 18;20-30, 2006 https://doi.org/10.1016/j.smim.2005.10.003
  33. Morrissey PJ, Conlon P, Charrier K, Braddy S, Alpert A, Williams D, Namen AE, Mochizuki D: Administration of IL-7 to normal mice stimulates B-lymphopoiesis and peripheral lymphadenopathy. J Immunol 147;561-568, 1991

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