1887

Abstract

As a prelude to primate studies, the immunogenicity of wild-type and codon-optimized versions of simian immunodeficiency virus (SIV)agm Gag DNA, with and without co-administered granulocyte–macrophage colony-stimulating factor (GM-CSF) DNA, was directly compared in two strains of mice. Gag-specific T cells in the splenocytes of BALB/c and C57BL/6 mice immunized by gene gun were quantified by ELISpot using panels of overlapping synthetic peptides (15mers) spanning the entire capsid proteins of SIVagm, SIVmac and human immunodeficiency virus type 1. Specific antibodies were measured by ELISA. Codon optimization was shown to significantly increase the immune response to the DNA immunogens, reducing the amount of DNA necessary to induce cellular and antibody responses by one and two orders of magnitude, respectively. Co-administration of murine GM-CSF DNA was necessary for the induction of high level T- and B-cell responses. Finally, it was possible to identify both known and novel T-cell epitopes in the Gag proteins of the three viruses.

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2009-10-01
2019-08-19
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References

  1. Allen, T. M., Mothé, B. R., Sidney, J., Jing, P., Dzuris, J. L., Liebl, M. E., Vogel, T. U., O'Connor, D. H., Wang, X. & other authors ( 2001; ). CD8+ lymphocytes from simian immunodeficiency virus-infected rhesus macaques recognize 14 different epitopes bound by the major histocompatibility complex class I molecule Mamu-A*01: implications for vaccine design and testing. J Virol 75, 738–749.[CrossRef]
    [Google Scholar]
  2. Barré-Sinoussi, F., Chermann, J. C., Rey, F., Nugeyre, M. T., Chamaret, S., Gruest, J., Dauguet, C., Axler-Blin, C., Vézinet-Brun, F. & other authors ( 1983; ). Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220, 868–871.[CrossRef]
    [Google Scholar]
  3. Beer, B. E., Bailes, E., Goeken, R., Dapolito, G., Coulibaly, C., Norley, S. G., Kurth, R., Gautier, J.-P., Gautier-Hion, A. & other authors ( 1999; ). Simian immunodeficiency virus (SIV) from sun-tailed monkeys (Cercopithecus solatus): evidence for host-dependent evolution of SIV within the C. lhoesti superspecies. J Virol 73, 7734–7744.
    [Google Scholar]
  4. Beer, B. E., Bailes, E., Dapolito, G., Campbell, B. J., Goeken, R. M., Axthelm, M. K., Markham, P. D., Bernard, J., Zagury, D. & other authors ( 2000; ). Patterns of genomic sequence diversity among their simian immunodeficiency viruses suggest that L'Hoest monkeys (Cercopithecus lhoesti) are a natural lentivirus reservoir. J Virol 74, 3892–3898.[CrossRef]
    [Google Scholar]
  5. Beer, B. E., Foley, B. T., Kuiken, C. L., Tooze, Z., Goeken, R. M., Brown, C. R., Hu, J., Claire, M. S., Korber, B. T. & Hirsch, V. M. ( 2001; ). Characterization of novel simian immunodeficiency viruses from Red-Capped Mangabeys from Nigeria (SIVrcmNG409 and -NG411). J Virol 75, 12014–12027.[CrossRef]
    [Google Scholar]
  6. Burshtyn, D. N. & Barber, B. H. ( 1993; ). High occupancy binding of antigenic peptides to purified, immunoadsorbed H-2Db β 2m molecules. J Immunol 151, 3070–3081.
    [Google Scholar]
  7. Chakrabarti, L. A., Lewin, S. R., Zhang, L., Gettie, A., Luckay, A., Martin, L. N., Skulsky, E., Ho, D. D., Cheng-Mayer, C. & Marx, P. A. ( 2000; ). Normal T-cell turnover in sooty mangabeys harboring active simian immunodeficiency virus infection. J Virol 74, 1209–1223.[CrossRef]
    [Google Scholar]
  8. Clavel, F., Guétard, D., Brun-Vézinet, F., Chamaret, S., Rey, M. A., Santos-Ferreira, M. O., Laurent, A. G., Dauguet, C., Katlama, C., Rouzioux, C. & other authors ( 1986; ). Isolation of a new human retrovirus from West African patients with AIDS. Science 233, 343–346.[CrossRef]
    [Google Scholar]
  9. Cumont, M. C., Diop, O., Vaslin, B., Elbim, C., Viollet, L., Monceaux, V., Lay, S., Silvestri, G., Le Grand, R. & other authors ( 2008; ). Early divergence in lymphoid tissue apoptosis between pathogenic and nonpathogenic simian immunodeficiency virus infections of nonhuman primates. J Virol 82, 1175–1184.[CrossRef]
    [Google Scholar]
  10. Deml, L., Bojak, A., Steck, S., Graf, M., Wild, J., Schirmbeck, R., Wolf, H. & Wagner, R. ( 2001; ). Multiple effects of codon usage optimization on expression and immunogenicity of DNA candidate vaccines encoding the human immunodeficiency virus type 1 Gag protein. J Virol 75, 10991–11001.[CrossRef]
    [Google Scholar]
  11. Emau, P., McClure, H. M., Isahakia, M., Else, J. G. & Fultz, P. N. ( 1991; ). Isolation from African Sykes' monkeys (Cercopithecus mitis) of a lentivirus related to human and simian immunodeficiency viruses. J Virol 65, 2135–2140.
    [Google Scholar]
  12. Fensterle, J., Grode, L., Hess, J. & Kaufmann, S. H. E. ( 1999; ). Effective DNA vaccination against listeriosis by prime/boost inoculation with the gene gun. J Immunol 163, 4510–4518.
    [Google Scholar]
  13. Gao, F., Bailes, E., Robertson, D. L., Chen, Y., Rodenburg, C. M., Michael, S. F., Cummins, L. B., Arthur, L. O., Peeters, M. & other authors ( 1999; ). Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397, 436–441.[CrossRef]
    [Google Scholar]
  14. Hanke, T., Schneider, J., Gilbert, S. C., Hill, A. V. & McMichael, A. ( 1998; ). DNA multi-CTL epitope vaccines for HIV and Plasmodium falciparum: immunogenicity in mice. Vaccine 16, 426–435.[CrossRef]
    [Google Scholar]
  15. Hartung, S., Boller, K., Cichutek, K., Norley, S. G. & Kurth, R. ( 1992; ). Quantitation of a lentivirus in its natural host: simian immunodeficiency virus in African green monkeys. J Virol 66, 2143–2149.
    [Google Scholar]
  16. Hazenberg, M. D., Otto, S. A., van Benthem, B. H., Roos, M. T., Coutinho, R. A., Lange, J. M., Hamann, D., Prins, M. & Miedema, F. ( 2003; ). Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 17, 1881–1888.[CrossRef]
    [Google Scholar]
  17. Hirsch, V. M., Olmsted, R. A., Murphey-Corb, M., Purcell, R. H. & Johnson, P. R. ( 1989; ). An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339, 389–392.[CrossRef]
    [Google Scholar]
  18. Hu, J., Switzer, W. M., Foley, B. T., Robertson, D. L., Goeken, R. M., Korber, B. T., Hirsch, V. M. & Beer, B. E. ( 2003; ). Characterization and comparison of recombinant simian imunodeficiency virus from drill (Mandrillus leucophaeus) and mandrill (Mandrillus sphinx) isolates. J Virol 77, 4867–4880.[CrossRef]
    [Google Scholar]
  19. Huang, J., Edwards, L. J., Evavold, B. D. & Zhu, C. ( 2007; ). Kinetics of MHC–CD8 interaction at the T cell membrane. J Immunol 179, 7653–7662.[CrossRef]
    [Google Scholar]
  20. Huet, T., Cheynier, R., Meyerhans, A., Roelants, G. & Wain-Hobson, S. ( 1990; ). Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature 345, 356–359.[CrossRef]
    [Google Scholar]
  21. Jaffray, A., Shephard, E., van Harmelen, J., Williamson, C., Williamson, A.-L. & Rybicki, E. P. ( 2004; ). Human immunodeficiency virus type 1 subtype C Gag virus-like particle boost substantially improves the immune response to a subtype C gag DNA vaccine in mice. J Gen Virol 85, 409–413.[CrossRef]
    [Google Scholar]
  22. Johnson, P. R., Fomsgaard, A., Allan, J., Gravell, M., London, W. T., Olmsted, R. A. & Hirsch, V. M. ( 1990; ). Simian immunodeficiency viruses from African green monkeys display unusual genetic diversity. J Virol 64, 1086–1092.
    [Google Scholar]
  23. Keele, B. F., Van Heuverswyn, F., Li, Y., Bailes, E., Takehisa, J., Santiago, M. L., Bibollet-Ruche, F., Chen, Y., Wain, L. V. & other authors ( 2006; ). Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 313, 523–526.[CrossRef]
    [Google Scholar]
  24. Kofman, A., Graf, M., Bojak, A., Deml, L., Bieler, K., Kharazova, A., Wolf, H. & Wagner, R. ( 2003; ). HIV-1 gag expression is quantitatively dependent on the ratio of native and optimized codons. Tsitologiia 45, 86–93.
    [Google Scholar]
  25. Kotsopoulou, E., Kim, V. N., Kingsman, A. J., Kingsman, S. M. & Mitrophanous, K. A. ( 2000; ). A rev-independent human immunodeficiency virus type 1 (HIV-1)-based vector that exploits a codon-optimized HIV-1 gagpol gene. J Virol 74, 4839–4852.[CrossRef]
    [Google Scholar]
  26. Kraus, G., Werner, A., Baier, M., Binniger, D., Ferdinand, F. J., Norley, S. & Kurth, R. ( 1989; ). Isolation of human immunodeficiency virus-related simian immunodeficiency viruses from African green monkeys. Proc Natl Acad Sci U S A 86, 2892–2896.[CrossRef]
    [Google Scholar]
  27. Letvin, N. L., Daniel, M. D., Sehgal, P. K., Desrosiers, R. C., Hunt, R. D., Waldron, L. M., MacKey, J. J., Schmidt, D. K., Chalifoux, L. V. & King, N. W. ( 1985; ). Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III. Science 230, 71–73.[CrossRef]
    [Google Scholar]
  28. Mata, M., Travers, P. J., Liu, Q., Frankel, F. R. & Paterson, Y. ( 1998; ). The MHC class I-restricted immune response to HIV-gag in BALB/c mice selects a single epitope that does not have a predictable MHC-binding motif and binds to Kd through interactions between a glutamine at P3 and pocket D. J Immunol 161, 2985–2993.
    [Google Scholar]
  29. Murphey-Corb, M., Martin, L. N., Rangan, S. R., Baskin, G. B., Gormus, B. J., Wolf, R. H., Andes, W. A., West, M. & Montelaro, R. C. ( 1986; ). Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature 321, 435–437.[CrossRef]
    [Google Scholar]
  30. Norley, S. & Kurth, R. ( 2004; ). The role of the immune response during SIVagm infection of the African green monkey natural host. Front Biosci 9, 550–564.[CrossRef]
    [Google Scholar]
  31. Norley, S. G., Kraus, G., Ennen, J., Bonilla, J., Konig, H. & Kurth, R. ( 1990; ). Immunological studies of the basis for the apathogenicity of simian immunodeficiency virus from African green monkeys. Proc Natl Acad Sci U S A 87, 9067–9071.[CrossRef]
    [Google Scholar]
  32. Norley, S., Beer, B., Holzammer, S., zur Megede, J. & Kurth, R. ( 1999; ). Why are the natural hosts of SIV resistant to AIDS? Immunol Lett 66, 47–52.[CrossRef]
    [Google Scholar]
  33. Peeters, M., Courgnaud, V., Abela, B., Auzel, P., Pourrut, X., Bibollet-Ruche, F., Loul, S., Liegeois, F., Butel, C. & other authors ( 2002; ). Risk to human health from a plethora of simian immunodeficiency viruses in primate bushmeat. Emerg Infect Dis 8, 451–457.[CrossRef]
    [Google Scholar]
  34. Rey-Cuillé, M.-A., Berthier, J.-L., Bomsel-Demontoy, M.-C., Chaduc, Y., Montagnier, L., Hovanessian, A. G. & Chakrabarti, L. A. ( 1998; ). Simian immunodeficiency virus replicates to high levels in sooty mangabeys without inducing disease. J Virol 72, 3872–3886.
    [Google Scholar]
  35. Sharp, P. M., Shaw, G. M. & Hahn, B. H. ( 2005; ). Simian immunodeficiency virus infection of chimpanzees. J Virol 79, 3891–3902.[CrossRef]
    [Google Scholar]
  36. Silvestri, G., Sodora, D. L., Koup, R. A., Paiardini, M., O'Neil, S. P., McClure, H. M., Staprans, S. I. & Feinberg, M. B. ( 2003; ). Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18, 441–452.[CrossRef]
    [Google Scholar]
  37. Smith, H. O., Hutchison, C. A., III, Pfannkoch, C. & Venter, J. C. ( 2003; ). Generating a synthetic genome by whole genome assembly: φX174 bacteriophage from synthetic oligonucleotides. Proc Natl Acad Sci U S A 100, 15440–15445.[CrossRef]
    [Google Scholar]
  38. Takehisa, J., Kraus, M. H., Decker, J. M., Li, Y., Keele, B. F., Bibollet-Ruche, F., Zammit, K. P., Weng, Z., Santiago, M. L. & other authors ( 2007; ). Generation of infectious molecular clones of simian immunodeficiency virus from fecal consensus sequences of wild chimpanzees. J Virol 81, 7463–7475.[CrossRef]
    [Google Scholar]
  39. Tsujimoto, H., Cooper, R. W., Kodama, T., Fukasawa, M., Miura, T., Ohta, Y., Ishikawa, K., Nakai, M., Frost, E. & Roelants, G. E. ( 1988; ). Isolation and characterization of simian immunodeficiency virus from mandrills in Africa and its relationship to other human and simian immunodeficiency viruses. J Virol 62, 4044–4050.
    [Google Scholar]
  40. Van Heuverswyn, F., Li, Y., Neel, C., Bailes, E., Keele, B. F., Liu, W., Loul, S., Butel, C., Liegeois, F. & other authors ( 2006; ). Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 444, 164 [CrossRef]
    [Google Scholar]
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