1887

Abstract

Development of a safe and effective vaccine for induction of mucosal immunity to the human immunodeficiency virus (HIV) envelope glycoprotein (Env, gp160) represents the best hope for containing the spread of an HIV epidemic worldwide. The highly attenuated modified vaccinia virus Ankara (MVA) is a laboratory virus well suited as a safe vaccine vector. However, the presence of pre-existing immunity to in the adult population represents a hindrance that limits the application of the MVA vector for inducing immunity to HIV antigens. Here, cationic liposomes were covalently attached to the surface of recombinant MVA expressing the HIV-1 strain IIIB Env glycoprotein and -galactosidase (MVA) using tresylmonomethoxypolyethylene glycol (TMPEG) grafted into a lipid membrane without compromising viral infectivity and . The orally administered MVA–TMPEG/liposome complexes were capable of delivering the transgenes to mucosal tissues in mice with pre-existing poxvirus immunity based on -galactosidase gene expression in intestinal tissues measured 18 h after infection. Importantly, the MVA–TMPEG/liposome complexes enhanced Env-specific cellular and humoral immune responses in the mucosal and systemic tissues after repeated oral immunization of BALB/c mice. This approach may prove useful for induction of protective immunity against infectious diseases and cancer in populations with pre-existing immunity to vaccinia from smallpox vaccination.

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2007-01-01
2019-10-17
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References

  1. Abacioglu, Y. H., Fouts, T. R., Laman, J. D., Claassen, E., Pincus, S. H., Moore, J. P., Roby, C. A., Kamin-Lewis, R. & Lewis, G. K. ( 1994; ). Epitope mapping and topology of baculovirus-expressed HIV-1 gp160 determined with a panel of murine monoclonal antibodies. AIDS Res Hum Retroviruses 10, 371–381.[CrossRef]
    [Google Scholar]
  2. Bangham, A. D. ( 1963; ). Physical structure and behavior of lipids and lipid enzymes. Adv Lipid Res 64, 65–104.
    [Google Scholar]
  3. Belyakov, I. M., Wyatt, L. S., Ahlers, J. D., Earl, P., Pendleton, C. D., Kelsall, B. L., Strober, W., Moss, B. & Berzofsky, J. A. ( 1998; ). Induction of a mucosal cytotoxic T-lymphocyte response by intrarectal immunization with a replication-deficient recombinant vaccinia virus expressing human immunodeficiency virus 89.6 envelope protein. J Virol 72, 8264–8272.
    [Google Scholar]
  4. Belyakov, I. M., Moss, B., Strober, W. & Berzofsky, J. A. ( 1999; ). Mucosal vaccination overcomes the barrier to recombinant vaccinia immunization caused by preexisting poxvirus immunity. Proc Natl Acad Sci U S A 96, 4512–4517.[CrossRef]
    [Google Scholar]
  5. Belyakov, I. M., Earl, P., Dzutsev, A., Kuznetsov, V. A., Lemon, M., Wyatt, L. S., Snyder, J. T., Ahlers, J. D., Franchini, G. & other authors ( 2003; ). Shared modes of protection against poxvirus infection by attenuated and conventional smallpox vaccine viruses. Proc Natl Acad Sci U S A 100, 9458–9463.[CrossRef]
    [Google Scholar]
  6. Belyakov, I. M., Hammond, S. A., Ahlers, J. D., Glenn, G. M. & Berzofsky, J. A. ( 2004; ). Transcutaneous immunization induces mucosal CTLs and protective immunity by migration of primed skin dendritic cells. J Clin Invest 113, 998–1007.[CrossRef]
    [Google Scholar]
  7. Bender, B. S., Rowe, C. A., Taylor, S. F., Wyatt, L. S., Moss, B. & Small, P. A., Jr ( 1996; ). Oral immunization with a replication-deficient recombinant vaccinia virus protects mice against influenza. J Virol 70, 6418–6424.
    [Google Scholar]
  8. Chen, S. C., Jones, D. H., Fynan, E. F., Farrar, G. H., Clegg, J. C. S., Greenberg, H. B. & Herrmann, J. E. ( 1998; ). Protective immunity induced by oral immunization with a rotavirus DNA vaccine encapsulated in microparticles. J Virol 72, 5757–5761.
    [Google Scholar]
  9. Childers, N. K., Zhang, S. S. & Michalek, S. M. ( 1994; ). Oral immunization of humans with dehydrated liposomes containing Streptococcus mutans glucosyltransferase induces salivary immunoglobulin A2 antibody responses. Oral Microbiol Immunol 9, 146–153.[CrossRef]
    [Google Scholar]
  10. Cooney, E. L., Collier, A. C., Greenberg, P. D., Coombs, R. W., Zarling, J., Arditti, D. E., Hoffman, M. C., Hu, S.-L. & Corey, L. ( 1991; ). Safety of and immunological response to a recombinant vaccinia virus vaccine expressing HIV envelope glycoprotein. Lancet 337, 567–572.[CrossRef]
    [Google Scholar]
  11. Czerkinsky, C., Anjuere, F., McGhee, J. R., George-Chandy, A., Holmgren, J., Kieny, M. P., Fujiyashi, K., Mestecky, J. F., Pierrefite-Carle, V. & other authors ( 1999; ). Mucosal immunity and tolerance: relevance to vaccine development. Immunol Rev 170, 197–222.[CrossRef]
    [Google Scholar]
  12. Delgado, C., Patel, J. N., Francis, G. E. & Fisher, D. ( 1990; ). Coupling of poly(ethylene glycol) to albumin under very mild conditions by activation with tresyl chloride: characterization of the conjugate by partitioning in aqueous two-phase systems. Biotechnol Appl Biochem 12, 119–128.
    [Google Scholar]
  13. Fenner, F. ( 1989; ). Risks and benefits of vaccinia vaccine use in the worldwide smallpox eradication campaign. Res Virol 140, 465–466.[CrossRef]
    [Google Scholar]
  14. Francis, G. E., Fisher, D., Delgado, C., Malik, F., Gardiner, A. & Neale, D. ( 1998; ). PEGylation of cytokines and other therapeutic proteins and peptides: the importance of biological optimisation of coupling techniques. Int J Hematol 68, 1–18.[CrossRef]
    [Google Scholar]
  15. Fuertges, F. & Abuchowski, A. ( 1990; ). The clinical efficacy of poly(ethylene glycol)-modified proteins. J Control Release 11, 139–148.[CrossRef]
    [Google Scholar]
  16. Fuller, D. H., Rajakumar, P. A., Wilson, L. A., Trichel, A. M., Fuller, J. T., Shipley, T., Wu, M. S., Weis, K., Rinaldo, C. R. & other authors ( 2002; ). Induction of mucosal protection against primary, heterologous simian immunodeficiency virus by a DNA vaccine. J Virol 76, 3309–3317.[CrossRef]
    [Google Scholar]
  17. Gaidarov, I., Santini, F., Warren, R. A. & Keen, J. H. ( 1999; ). Spatial control of coated-pit dynamics in living cells. Nat Cell Biol 1, 1–7.[CrossRef]
    [Google Scholar]
  18. Gherardi, M. M. & Esteban, M. ( 1999; ). Mucosal and systemic immune responses induced after oral delivery of vaccinia virus recombinants. Vaccine 17, 1074–1083.[CrossRef]
    [Google Scholar]
  19. Gregoriadis, G. & Ryman, B. E. ( 1972; ). Fate of protein-containing liposomes injected into rats. An approach to the treatment of storage diseases. Eur J Biochem 24, 485–491.[CrossRef]
    [Google Scholar]
  20. Gurunathan, S., Wu, C.-Y., Freidag, B. L. & Seder, R. A. ( 2000; ). DNA vaccines: a key for inducing long-term cellular immunity. Curr Opin Immunol 12, 442–447.[CrossRef]
    [Google Scholar]
  21. Hanke, T., Blanchard, T. J., Schneider, J., Hannan, C. M., Becker, M., Gilbert, S. C., Hill, A. V. S., Smith, G. L. & McMichael, A. ( 1998; ). Enhancement of MHC class I-restricted peptide-specific T cell induction by a DNA prime/MVA boost vaccination regime. Vaccine 16, 439–445.[CrossRef]
    [Google Scholar]
  22. Harasym, T. O., Tardi, P., Longman, S. A., Ansell, S. M., Bally, M. B., Cullis, P. R. & Choi, L. S. L. ( 1995; ). Poly(ethylene glycol)-modified phospholipids prevent aggregation during covalent conjugation of proteins to liposomes. Bioconjug Chem 6, 187–194.[CrossRef]
    [Google Scholar]
  23. Hedley, M. L., Curley, J. & Urban, R. ( 1998; ). Microspheres containing plasmid-encoded antigens elicit cytotoxic T-cell responses. Nat Med 4, 365–368.[CrossRef]
    [Google Scholar]
  24. Ishii, N., Fukushima, J., Kaneko, T., Okada, E., Tani, K., Tanaka, S. I., Hamajima, K., Xin, K.-Q., Kawamoto, S. & other authors ( 1997; ). Cationic liposomes are a strong adjuvant for a DNA vaccine of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 13, 1421–1428.[CrossRef]
    [Google Scholar]
  25. Jones, D. H., Corris, S., McDonald, S., Clegg, J. C. S. & Farrar, G. H. ( 1997; ). Poly(dl-lactide-co-glycolide)-encapsulated plasmid DNA elicits systemic and mucosal antibody responses to encoded protein after oral administration. Vaccine 15, 814–817.[CrossRef]
    [Google Scholar]
  26. Kaneko, H., Bednarek, I., Wierzbicki, A., Kiszka, I., Dmochowski, M., Wasik, T. J., Kaneko, Y. & Kozbor, D. ( 2000; ). Oral DNA vaccination promotes mucosal and systemic immune responses to HIV envelope glycoprotein. Virology 267, 8–16.[CrossRef]
    [Google Scholar]
  27. Kiszka, I., Kmieciak, D., Gzyl, J., Naito, T., Bolesta, E., Sieron, A., Singh, S. P., Srinivasan, A., Trinchieri, G. & other authors ( 2002; ). Effect of the V3 loop deletion of envelope glycoprotein on cellular responses and protection against challenge with recombinant vaccinia virus expressing gp160 of primary human immunodeficiency virus type 1 isolates. J Virol 76, 4222–4232.[CrossRef]
    [Google Scholar]
  28. Konishi, E., Kurane, I., Mason, P. W., Shope, R. E. & Ennis, F. A. ( 1997; ). Poxvirus-based Japanese encephalitis vaccine candidates induce JE virus-specific CD8+ cytotoxic T lymphocytes in mice. Virology 227, 353–360.[CrossRef]
    [Google Scholar]
  29. Kresina, T. F. & Mathieson, B. ( 1999; ). Human immunodeficiency virus type 1 infection, mucosal immunity, and pathogenesis and extramural research programs at the National Institutes of Health. J Infect Dis 179 (Suppl. 3), S392–S396.[CrossRef]
    [Google Scholar]
  30. Lasic, D. D. ( 1998; ). Novel applications of liposomes. Trends Biotechnol 16, 307–321.[CrossRef]
    [Google Scholar]
  31. Malik, F., Delgado, C., Knusli, C., Irvine, A. E., Fisher, D. & Francis, G. E. ( 1992; ). Polyethylene glycol (PEG)-modified granulocyte-macrophage colony-stimulating factor (GM-CSF) with conserved biological activity. Exp Hematol 20, 1028–1035.
    [Google Scholar]
  32. Mayr, A., Stickl, H., Muller, H. K., Danner, K. & Singer, H. ( 1978; ). The smallpox vaccination strain MVA: marker, genetic structure, experience gained with the parenteral vaccination and behaviour in organisms with a debilitated defence mechanism. Zentralbl Bakteriol 167, 375–390 (in German).
    [Google Scholar]
  33. McGhee, J. R. & Mestecky, J. ( 1990; ). In defense of mucosal surfaces. Development of novel vaccines for IgA responses protective at the portals of entry of microbial pathogens. Infect Dis Clin North Am 4, 315–341.
    [Google Scholar]
  34. Mestecky, J. & Eldridge, J. H. ( 1991; ). Targeting and controlled release of antigens for the effective induction of secretory antibody responses. Curr Opin Immunol 3, 492–495.[CrossRef]
    [Google Scholar]
  35. Meyer, H., Sutter, G. & Mayr, A. ( 1991; ). Mapping of deletions in the genome of the highly attenuated vaccinia virus MVA and their influence on virulence. J Gen Virol 72, 1031–1038.[CrossRef]
    [Google Scholar]
  36. O'Riordan, C. R., Lachapelle, A., Delgado, C., Parkes, V., Wadsworth, S. C., Smith, A. E. & Francis, G. E. ( 1999; ). PEGylation of adenovirus with retention of infectivity and protection from neutralizing antibody in vitro and in vivo. Hum Gene Ther 10, 1349–1358.[CrossRef]
    [Google Scholar]
  37. Pal, R., Venzon, D., Santra, S., Kalyanaraman, V. S., Montefiori, D. C., Hocker, L., Hudacik, L., Rose, N., Nacsa, J. & other authors ( 2006; ). Systemic immunization with an ALVAC-HIV-1/protein boost vaccine strategy protects rhesus macaques from CD4+ T-cell loss and reduces both systemic and mucosal simian-human immunodeficiency virus SHIVKU2 RNA levels. J Virol 80, 3732–3742.[CrossRef]
    [Google Scholar]
  38. Schneider, J., Gilbert, S. C., Blanchard, T. J., Hanke, T., Robson, K. J., Hannan, C. M., Becker, M., Sinden, R., Smith, G. L. & Hill, A. V. ( 1998; ). Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nat Med 4, 397–402.[CrossRef]
    [Google Scholar]
  39. Senior, J., Delgado, C., Fisher, D., Tilcock, C. & Gregoriadis, G. ( 1991; ). Influence of surface hydrophilicity of liposomes on their interaction with plasma protein and clearance from the circulation: studies with poly(ethylene glycol)-coated vesicles. Biochim Biophys Acta 1062, 77–82.[CrossRef]
    [Google Scholar]
  40. Snyder, J. T., Belyakov, I. M., Dzutsev, A., Lemonnier, F. & Berzofsky, J. A. ( 2004; ). Protection against lethal vaccinia virus challenge in HLA-A2 transgenic mice by immunization with a single CD8+ T-cell peptide epitope of vaccinia and variola viruses. J Virol 78, 7052–7060.[CrossRef]
    [Google Scholar]
  41. Sutter, G. & Moss, B. ( 1992; ). Nonreplicating vaccinia vector efficiently expresses recombinant genes. Proc Natl Acad Sci U S A 89, 10847–10851.[CrossRef]
    [Google Scholar]
  42. Sutter, G. & Moss, B. ( 1995; ). Novel vaccinia vector derived from the host range restricted and highly attenuated MVA strain of vaccinia virus. Dev Biol Stand 84, 195–200.
    [Google Scholar]
  43. Takahashi, H., Nakagawa, Y., Leggatt, G. R., Ishida, Y., Saito, T., Yokomuro, K. & Berzofsky, J. A. ( 1996; ). Inactivation of human immunodeficiency virus (HIV)-1 envelope-specific CD8+ cytotoxic T lymphocytes by free antigenic peptide: a self-veto mechanism? J Exp Med 183, 879–889.[CrossRef]
    [Google Scholar]
  44. Tartaglia, J., Perkus, M. E., Taylor, J., Norton, E. K., Audonnet, J.-C., Cox, W. I., Davis, S. W., van der Hoeven, J., Meignier, B. & other authors ( 1992; ). NYVAC: a highly attenuated strain of vaccinia virus. Virology 188, 217–232.[CrossRef]
    [Google Scholar]
  45. Wierzbicki, A., Kiszka, I., Kaneko, H., Kmieciak, D., Wasik, T. J., Gzyl, J., Kaneko, Y. & Kozbor, D. ( 2002; ). Immunization strategies to augment oral vaccination with DNA and viral vectors expressing HIV envelope glycoprotein. Vaccine 20, 1295–1307.[CrossRef]
    [Google Scholar]
  46. Wyatt, L. S., Moss, B. & Rozenblatt, S. ( 1995; ). Replication-deficient vaccinia virus encoding bacteriophage T7 RNA polymerase for transient gene expression in mammalian cells. Virology 210, 202–205.[CrossRef]
    [Google Scholar]
  47. Wyatt, L. S., Shors, S. T., Murphy, B. R. & Moss, B. ( 1996; ). Development of a replication-deficient recombinant vaccinia virus vaccine effective against parainfluenza virus 3 infection in an animal model. Vaccine 14, 1451–1458.[CrossRef]
    [Google Scholar]
  48. Zalipsky, S. ( 1993; ). Synthesis of an end-group functionalized polyethylene glycol-lipid conjugate for preparation of polymer-grafted liposomes. Bioconjug Chem 4, 296–299.[CrossRef]
    [Google Scholar]
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