1887

Abstract

Envelopes of primary R5-tropic human immunodeficiency virus type 1 (HIV-1) isolates may be particularly relevant for vaccine purposes and should be evaluated for immunogenicity in animals including macaques before carrying out human vaccine trials. In the present study, the immunogenicities of synthetic HIV-1 DNA vaccines, which had been derived from the early primary isolate Bx08 and contain humanized codons, were evaluated in mice, guinea pigs and rhesus macaques. Neutralization sensitivity of the HIV-1 isolate was found to resemble that of other primary isolate prototypes. Immunogenicity of gp120 delivered as codon-optimized DNA vaccine was comparable to that of recombinant gp120 protein plus adjuvant in mice. Similarly, DNA vaccination of guinea pigs with synthetic gp140 and gp150 DNA induced a strong antibody response independent of the gene construct and DNA immunization route. Mamu-A*01 rhesus macaques were DNA vaccinated with synthetic gp150 or gp140 DNA and boosted with a replication-deficient recombinant human adenovirus type 5 expressing a synthetic gp120 gene. DNA-vaccinated rhesus macaques developed specific CD8 T lymphocyte responses and anti-rgp120 antibody responses. Both the humoral and cellular responses were significantly improved following intramuscular boosting with the recombinant adenovirus. The demonstrated humoral and cellular immunogenicities of these HIV Bx08 Env vaccines in non-human primates encourages their further development as one component in candidate HIV vaccines for humans.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18589-0
2003-01-01
2019-12-07
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/1/vir840203.html?itemId=/content/journal/jgv/10.1099/vir.0.18589-0&mimeType=html&fmt=ahah

References

  1. Allen, T. M., Vogel, T. U., Fuller, D. H. & 11 other authors ( 2000; ). Induction of AIDS virus-specific CTL activity in fresh, unstimulated peripheral blood lymphocytes from rhesus macaques vaccinated with a DNA prime/modified vaccinia virus Ankara boost regimen. J Immunol 164, 4968–4978.[CrossRef]
    [Google Scholar]
  2. André., S., Seed, B., Eberle, J., Schraut, W., Bültmann, A. & Haas, J. ( 1998; ). Increased immune response elicited by DNA vaccination with a synthetic gp120 sequence with optimized codon usage. J Virol 72, 1497–1503.
    [Google Scholar]
  3. Anon. ( 1998; ). Looking forward to the back of HIV (Editorial). Nat Med 4, 867–868.[CrossRef]
    [Google Scholar]
  4. Barnett, S., Klinger, J. M., Doe, B., Walker, C. M., Hansen, L., Duliége, A. & Sinangil, F. M. ( 1998; ). Prime-boost immunization strategies against HIV. AIDS Res Hum Retroviruses 14, s299–310.[CrossRef]
    [Google Scholar]
  5. Barouch, D. H., Santra, S., Schmitz, J. E. & 23 other authors ( 2000; ). Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290, 486–492.[CrossRef]
    [Google Scholar]
  6. Beddows, S., Louisirirotchanakul, S., Cheingsong-Popov, R., Easterbrook, P. J., Simmonds, P. & Weber, J. ( 1998; ). Neutralization of primary and T-cell line adapted isolates of human immunodeficiency virus type 1: role of V3-specific antibodies. J Gen Virol 79, 77–82.
    [Google Scholar]
  7. Berlioz, T. C., Shacklett, B. L., Erdtmann, L., Delamarre, L., Bouchaert, I., Sonigo, P., Dokhelar, M. C. & Benarous, R. ( 1999; ). Interactions of the cytoplasmic domains of human and simian retroviral transmembrane proteins with components of the clathrinadaptor complexes modulate intracellular and cell surface expression of envelope glycoproteins. J Virol 73, 1350–1361.
    [Google Scholar]
  8. Bruce, C. B., Akrigg, A., Sharpe, S. A., Hanke, T., Wilkinson, G. W. & Cranage, M. P. ( 1999; ). Replication-deficient recombinant adenoviruses expressing the human immunodeficiency virus Env antigen can induce both humoral and CTL immune responses in mice. J Gen Virol 80, 2621–2628.
    [Google Scholar]
  9. Buge, S. L., Murty, L., Arora, K. & 8 other authors( 1999; ). Factors associated with slow disease progression in macaques immunized with an adenovirus-simian immunodeficiency virus (SIV) envelope priming-gp120 boosting regimen and challenged vaginally with SIVmac251. J Virol 73, 7430–7440.
    [Google Scholar]
  10. Bures, R., Gaitan, A., Zhu, T. & 13 other authors ( 2000; ). Immunization with recombinant canarypox vectors expressing membrane-anchored glycoprotein 120 followed by glycoprotein 160 boosting fails to generate antibodies that neutralize R5 primary isolates of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 16, 2019–2035.[CrossRef]
    [Google Scholar]
  11. Bures, R., Morris, L., Williamson, C., Ramjee, G., Deers, M., Fiscus, S. A., Abdool-Karim, S. & Montefiori, D. C. ( 2002; ). Regional clustering of shared neutralization determinants on primary isolates of clade C human immunodeficiency virus type 1 from South Africa. J Virol 76, 2233–2244.[CrossRef]
    [Google Scholar]
  12. Burton, D. R., Pyati, J., Koduri, R. & 7 other authors ( 1994; ). Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266, 1024–1027.[CrossRef]
    [Google Scholar]
  13. Chan, D. C., Fass, D., Berger, J. M. & Kim, P. S. ( 1997; ). Core structure of gp41 from the HIV envelope glycoprotein. Cell 89, 263–273.[CrossRef]
    [Google Scholar]
  14. Conley, A. J., Kessler, J. A., II, Boots, L. J. & 9 other authors ( 1996; ). The consequence of passive administration of an anti-human immunodeficiency virus type 1 neutralizing monoclonal antibody before challenge of chimpanzees with a primary virus isolate. J Virol 70, 6751–6758.
    [Google Scholar]
  15. Connor, R. I., Korber, B. T. M., Graham, B. S. & 17 authors ( 1998; ). Immunological and virological analyses of persons infected by human immunodeficiency virus type 1 while participating in trials of recombinant gp120 subunit vaccines. J Virol 72, 1552–1576.
    [Google Scholar]
  16. Corbet, S., Vinner, L., Hougaard, D. M., Bryder, K., Nielsen, H. V., Nielsen, C. & Fomsgaard, A. ( 2000; ). Construction, biological activity, and immunogenicity of synthetic envelope DNA vaccines based on a primary, CCR5-tropic, early HIV type 1 isolate (BX08) with human codons. AIDS Res Hum Retroviruses 16, 1997–2008.[CrossRef]
    [Google Scholar]
  17. Egan, M. A., Kuroda, M. J., Voss, G., Schmitz, J. E., Charini, W. A., Lord, C. I., Forman, M. A. & Letvin, N. L. ( 1999; ). Use of major histocompatibility complex class I/peptide/β2M tetramers to quantitate CD8+ cytotoxic T lymphocytes specific for dominant and nondominant viral epitopes in simian-human immunodeficiency virus-infected rhesus monkeys. J Virol 73, 5466–5472.
    [Google Scholar]
  18. Egan, M. A., Charini, W. A., Kuroda, M. J. & 10 other authors ( 2000; ). Simian immunodeficiency virus (SIV) gag DNA-vaccinated rhesus monkeys develop secondary cytotoxic T-lymphocyte responses and control viral replication after pathogenic SIV infection. J Virol 74, 7485–7495.[CrossRef]
    [Google Scholar]
  19. Farina, S. F., Gao, G. P., Xiang, Z. Q., Rux, J. J., Burnett, R. M., Alvira, M. R., Marsh, J., Ertl, H. C. & Wilson, J. M. ( 2001; ). Replication-defective vector based on a chimpanzee adenovirus. J Virol 75, 11603–11613.[CrossRef]
    [Google Scholar]
  20. Follis, K. E., Trahey, M., LaCasse, R. A. & Nunberg, J. H. ( 1998; ). Continued utilization of CCR5 coreceptor by a newly derived T-cell line-adapted isolate of human immunodeficiency virus type 1. J Virol 72, 7603–7608.
    [Google Scholar]
  21. Francis, D. P., Gregory, T., McElrath, M. J. & 8 other authors ( 1998; ). Advancing AIDSVAX to phase 3. Safety, immunogenicity, and plans for phase 3. AIDS Res Hum Retroviruses 14, S325–332.
    [Google Scholar]
  22. Fuller, D. H., Corb, M. M., Barnett, S., Steimer, K. & Haynes, J. R. ( 1997; ). Enhancement of immunodeficiency virus-specific immune responses in DNA-immunized rhesus macaques. Vaccine 15, 924–926.[CrossRef]
    [Google Scholar]
  23. Gao, G. P., Yang, Y. & Wilson, J. M. ( 1996; ). Biology of adenovirus vectors with E1 and E4 deletions for liver-directed gene therapy. J Virol 70, 8934–8943.
    [Google Scholar]
  24. Gartner, S., Markovits, P., Markovitz, D. M., Kaplan, M. H., Gallo, R. C. & Popovic, M. ( 1986; ). The role of mononuclear phagocytes in HTLV-III/LAV infection. Science 233, 215–219.[CrossRef]
    [Google Scholar]
  25. Graham, B. S., McElrath, M. J., Connor, R. I. & 16 other authors ( 1998; ). Analysis of intercurrent human immunodeficiency virus type 1 infections in phase I and II trials of candidate AIDS vaccines. AIDS Vaccine Evaluation Group, and the Correlates of HIV Immune Protection Group. J Infect Dis 177, 310–319.[CrossRef]
    [Google Scholar]
  26. Gurunathan, S., Klinman, D. M. & Seder, R. A. ( 2000; ). DNA vaccines: immunology, application, and optimization. Annu Rev Immunol 18, 927–974.[CrossRef]
    [Google Scholar]
  27. Haas, J., Park, E. C. & Seed, B. ( 1996; ). Codon usage limitation in the expression of HIV-1 envelope glycoprotein. Curr Biol 6, 315–324.[CrossRef]
    [Google Scholar]
  28. Hanke, T., Samuel, R. V., Blanchard, T. J. & 9 other authors ( 1999; ). Effective induction of simian immunodeficiency virus-specific cytotoxic T lymphocytes in macaques by using a multiepitope gene and DNA prime-modified vaccinia virus Ankara boost vaccination regimen. J Virol 73, 7524–7532.
    [Google Scholar]
  29. Kamstrup, S., San Martin, R., Doberti, A., Grande, H. & Dalsgaard, K. ( 2000; ). Preparation and characterisation of quillaja saponin with less heterogeneity than Quil-A. Vaccine 18, 2244–2249.[CrossRef]
    [Google Scholar]
  30. Kent, S. J., Zhao, A., Best, S. J., Chandler, J. D., Boyle, D. B. & Ramshaw, I. A. ( 1998; ). Enhanced T-cell immunogenicity and protective efficacy of a human immunodeficiency virus type 1 vaccine regimen consisting of consecutive priming with DNA and boosting with recombinant fowlpox virus. J Virol 72, 10180–10188.
    [Google Scholar]
  31. LaBranche, C. C., Sauter, M. M., Haggarty, B. S., Vance, P. J., Romano, J., Hart, T. K., Bugelski, P. J., Marsh, M. & Hoxie, J. A. ( 1995; ). A single amino acid change in the cytoplasmic domain of the simian immunodeficiency virus transmembrane molecule increases envelope glycoprotein expression on infected cells. J Virol 69, 5217–5227.
    [Google Scholar]
  32. Lu, S., Arthos, J., Montefiori, D. C., Yasutomi, Y. & 11 other authors ( 1996; ). Simian immunodeficiency virus DNA vaccine trial in macaques. J Virol 70, 3978–3991.
    [Google Scholar]
  33. Lu, S., Wyatt, R., Richmond, J. F., Mustafa, F., Wang, S., Weng, J., Montefiori, D. C., Sodroski, J. & Robinson, H. L. ( 1998; ). Immunogenicity of DNA vaccines expressing human immunodeficiency virus type 1 envelope glycoprotein with and without deletions in the V1/2 and V3 regions. AIDS Res Hum Retroviruses 14, 151–155.[CrossRef]
    [Google Scholar]
  34. Mascola, J. R., Snyder, S. W., Weislow, O. S. & 17 other authors ( 1996; ). Immunization with envelope subunit vaccine products elicits neutralizing antibodies against laboratory-adapted but not primary isolates of human immunodeficiency virus type 1. The National Institute of Allergy and Infectious Diseases AIDS Vaccine Evaluation Group. J Infect Dis 173, 340–348.[CrossRef]
    [Google Scholar]
  35. Mascola, J. R., Stiegler, G., VanCott, T. C. & 11 other authors ( 2000; ). Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat Med 6, 207–210.[CrossRef]
    [Google Scholar]
  36. McCluskie, M. J., Millan, C. L. B., Gramzinski, R. A. & 7 other authors ( 1999; ). Route and method of delivery of DNA vaccine influences immune responses in mice and non-human primates. Mol Med 5, 287–300.[CrossRef]
    [Google Scholar]
  37. Montefiori, D. C., Safrit, J. T., Lydy, S. L. & 7 other authors ( 2001; ). Induction of neutralizing antibodies and gag-specific cellular immune responses to an R5 primary isolate of human immunodeficiency virus type 1 in rhesus macaques. J Virol 75, 5879–5890.[CrossRef]
    [Google Scholar]
  38. Moog, C., Fleury, H. J., Pellegrin, I., Kirn, A. & Aubertin, A. M. ( 1997a; ). Autologous and heterologous neutralizing antibody responses following initial seroconversion in human immunodeficiency virus type 1-infected individuals. J Virol 71, 3734–3741.
    [Google Scholar]
  39. Moog, C., Spenlehauer, C., Fleury, H. J., Heshmati, F., Saragosti, S., Letourneur, F., Kirn, A. & Aubertin, A. M. ( 1997b; ). Neutralization of primary human immunodeficiency virus type 1 isolates: a study of parameters implicated in neutralization in vitro. AIDS Res Hum Retroviruses 13, 19–27.[CrossRef]
    [Google Scholar]
  40. Moore, J. P., Burkly, L. C., Connor, R. I., Cao, Y., Tizard, R., Ho, D. D. & Fisher, R. A. ( 1993; ). Adaptation of two primary human immunodeficiency virus type 1 isolates to growth in transformed T cell lines correlates with alterations in the responses of their envelope glycoproteins to soluble CD4. AIDS Res Hum Retroviruses 9, 529–539.[CrossRef]
    [Google Scholar]
  41. Moore, J. P., Cao, Y., Qing, L., Sattentau, Q. J. & 7 other authors ( 1995; ). Primary isolates of human immunodeficiency virus type 1 are relatively resistant to neutralization by monoclonal antibodies to gp120, and their neutralization is not predicted by studies with monomeric gp120. J Virol 69, 101–109.
    [Google Scholar]
  42. Muster, T., Steindl, F., Purtscher, M., Trkola, A., Klima, A., Himmler, G., Rüker, F. & Katinger, H. ( 1993; ). A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J Virol 67, 6642–6647.
    [Google Scholar]
  43. Natuk, R. J., Chanda, P. K., Lubeck, M. D. & 7 other authors ( 1992; ). Adenovirus-human immunodeficiency virus (HIV) envelope recombinant vaccines elicit high-titered HIV-neutralizing antibodies in the dog model. Proc Natl Acad Sci U S A 89, 7777–7781.[CrossRef]
    [Google Scholar]
  44. Nielsen, C. M., Bygbjerg, I. C. & Vestergaard, B. F. ( 1987; ). Detection of HIV antigens in eluates from whole blood collected on filterpaper [letter]. Lancet i, 566–567.
    [Google Scholar]
  45. Nyambi, P. N., Nadas, A., Mbah, H. A., Burda, S., Williams, C., Gorny, M. K. & Zolla-Pazner, S. ( 2000; ). Immunoreactivity of intact virions of human immunodeficiency virus type 1 (HIV-1) reveals the existence of fewer HIV-1 immunotypes than genotypes. J Virol 74, 10670–10680.[CrossRef]
    [Google Scholar]
  46. Parren, P. W., Gauduin, M. C., Koup, R. A., Poignard, P., Fisicaro, P., Burton, D. R. & Sattentau, Q. J. ( 1997; ). Relevance of the antibody response against human immunodeficiency virus type 1 envelope to vaccine design. Immunol Lett 57, 105–112.[CrossRef]
    [Google Scholar]
  47. Parren, P. W., Marx, P. A., Hessell, A. J., Luckay, A., Harouse, J., Cheng-Mayer, C., Moore, J. P. & Burton, D. R. ( 2001; ). Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralisation in vitro. J Virol 75, 8340–8347.[CrossRef]
    [Google Scholar]
  48. Prevec, L., Christie, B. S., Laurie, K. E., Bailey, M. M., Graham, F. L. & Rosenthal, K. L. ( 1991; ). Immune response to HIV-1 gag antigens induced by recombinant adenovirus vectors in mice and rhesus macaque monkeys. J Acquir Immune Defic Syndr 4, 568–576.
    [Google Scholar]
  49. Richmond, J. F., Lu, S., Santoro, J. C., Weng, J., Hu, S. L., Montefiori, D. C. & Robinson, H. L. ( 1998; ). Studies of the neutralizing activity and avidity of anti-human immunodeficiency virus type 1 Env antibody elicited by DNA priming and protein boosting. J Virol 72, 9092–9100.
    [Google Scholar]
  50. Robinson, H. L., Montefiori, D. C., Johnson, R. P. & 14 other authors ( 1999; ). Neutralizing antibody-independent containment of immunodeficiency virus challenges by DNA priming and recombinant pox virus booster immunizations. Nat Med 5, 526–534.[CrossRef]
    [Google Scholar]
  51. Ruxrungtham, K. & Phanuphak, P. ( 2001; ). Update on HIV/AIDS in Thailand. J Med Assoc Thai 84, S1–17.
    [Google Scholar]
  52. Shibata, R., Igarashi, T., Haigwood, N., Buckler-White, A., Ogert, R., Ross, W., Willie, R., Cho, M. W. & Martin, M. A. ( 1999; ). Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat Med 2, 204–210.
    [Google Scholar]
  53. Shiver, J. W., Fu, T. M., Chen, L. & 49 other authors ( 2002; ). Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 415, 331–335.[CrossRef]
    [Google Scholar]
  54. Sorensen, N. S. ( 2001; ). On the effect of antibodies on the humoral response to protein antigens. PhD thesis, Faculty of Health Sciences, University of Copenhagen, Denmark.
  55. Stamatatos, L. & Cheng-Mayer, C. ( 1998; ). An envelope modification that renders a primary, neutralisation resistant clade B human immunodeficiency virus type 1 isolate highly susceptible to neutralization by sera from other clades. J Virol 72, 7840–7845.
    [Google Scholar]
  56. Trkola, A., Purtscher, M., Muster, T. & 7 other authors ( 1996; ). Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J Virol 70, 1100–1108.
    [Google Scholar]
  57. Trono, D. & Baltimore, D. ( 1990; ). A human cell factor is essential for HIV-1 Rev action. EMBO J 9, 4155–4160.
    [Google Scholar]
  58. Vinner, L., Nielsen, H. V., Bryder, K., Corbet, S., Nielsen, C. & Fomsgaard, A. ( 1999; ). Gene gun DNA vaccination with Rev-independent synthetic HIV-1 gp160 envelope gene using mammalian codons. Vaccine 17, 2166–2175.[CrossRef]
    [Google Scholar]
  59. Wee, E. G. T., Patel, S., McMichael, A. J. & Hanke, T. ( 2002; ). A DNA/MVA-based candidate human immunodeficiency virus vaccine for Kenya induces multi-specific T cell responses in rhesus macaques. J Gen Virol 83, 75–80.
    [Google Scholar]
  60. World Health Organization ( 2001; ). Global situation of HIV/AIDS pandemic, end 2001. Wkly Epidemiol Rec 76, 381–388.
    [Google Scholar]
  61. Wrin, T., Loh, T. P., Vennari, J. C., Schuitemaker, H. & Nunberg, J. H. ( 1995; ). Adaptation to persistent growth in the H9 cell line renders a primary isolate of human immunodeficiency virus type 1 sensitive to neutralization by vaccine sera. J Virol 69, 39–48.
    [Google Scholar]
  62. Zhang, L., Huang, Y., He, T., Cao, Y. & Ho, D. D. ( 1996; ). HIV-1 subtype and second-receptor use [letter]. Nature 383, 768.[CrossRef]
    [Google Scholar]
  63. Zhang, Y. J., Fredriksson, R., McKeating, J. A. & Fenyo, E. M. ( 1997; ). Passage of HIV-1 molecular clones into different cell lines confers differential sensitivity to neutralization. Virology 238, 254–264.[CrossRef]
    [Google Scholar]
  64. Zhou, J. Y. & Montefiori, D. C. ( 1997; ). Antibody-mediated neutralization of primary isolates of human immunodeficiency virus type 1 in peripheral blood mononuclear cells is not affected by the initial activation state of the cells. J Virol 71, 2512–2517.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.18589-0
Loading
/content/journal/jgv/10.1099/vir.0.18589-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error