Broad cellular immunity with robust memory responses to simian immunodeficiency virus following serial vaccination with adenovirus 5- and 35-based vectors Free

Abstract

Adenovirus serotype 35 (Ad35) is a promising vaccine platform for human immunodeficiency virus (HIV) infection and emerging infectious diseases as it is uncommon in humans worldwide and is distinct from Ad5, the major vaccine serotype for which many individuals have pre-existing immunity. The immunogenicity of a first-generation, replication-competent Ad35-based vaccine was tested in the simian immunodeficiency virus (SIV) rhesus macaque model by evaluating its capacity to boost immunity generated by Ad5-based vectors. A series of four immunizations with replication-defective Ad5 vectors expressing SIVmac239 induced high-frequency responses mediated by both CD8 and CD4 T cells directed against several epitopes. Ad5-specific neutralizing antibody responses that did not neutralize Ad35 were rapidly induced but waned over time. Subsequent immunization with Ad5-based vectors was minimally effective, whereas immunization with Ad35-based vectors generated a strong increase in the frequency of Gag-specific T cells with specificities that were unchanged. While this boosting response was relatively transient, challenge with the distinct pathogenic isolate SIV/DeltaB670 generated robust and selective recall responses to Gag with similar specificities as induced by vaccination that were elevated for 25 weeks relative to controls. Vaccination had measurable albeit minor effects on virus load. Unexpectedly, regional hypervariability within the Gag sequence of SIV/DeltaB670 was associated with mutation of the conserved CD8 T-cell epitope CM9 without concurrent flanking mutations and in the absence of immune pressure. These findings support the further development of Ad35 as a vaccine vector, and promote vaccine regimens that utilize serial administration of heterologous adenoviruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81445-0
2006-01-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/1/139.html?itemId=/content/journal/jgv/10.1099/vir.0.81445-0&mimeType=html&fmt=ahah

References

  1. Amara R. R., Villinger F., Altman J. D. & 19 other authors 2001; Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292:69–74 [CrossRef]
    [Google Scholar]
  2. Amedee A. M., Lacour N., Gierman J. L., Martin L. N., Clements J. E., Bohm R. Jr, Harrison R. M., Murphey-Corb M. 1995; Genotypic selection of simian immunodeficiency virus in macaque infants infected transplacentally. J Virol 69:7982–7990
    [Google Scholar]
  3. Barouch D. H., Nabel G. J. 2005; Adenovirus vector-based vaccines for human immunodeficiency virus type 1. Hum Gene Ther 16:149–156 [CrossRef]
    [Google Scholar]
  4. Barouch D. H., Santra S., Kuroda M. J. & 13 other authors 2001; Reduction of simian-human immunodeficiency virus 89.6P viremia in rhesus monkeys by recombinant modified vaccinia virus Ankara vaccination. J Virol 75:5151–5158 [CrossRef]
    [Google Scholar]
  5. Barouch D. H., Kunstman J., Kuroda M. J. & 11 other authors 2002; Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415:335–339 [CrossRef]
    [Google Scholar]
  6. Barouch D. H., Kunstman J., Glowczwskie J. & 12 other authors 2003; Viral escape from dominant simian immunodeficiency virus epitope-specific cytotoxic T lymphocytes in DNA-vaccinated rhesus monkeys. J Virol 77:7367–7375 [CrossRef]
    [Google Scholar]
  7. Barouch D. H., Pau M. G., Custers J. H. & 15 other authors 2004; Immunogenicity of recombinant adenovirus serotype 35 vaccine in the presence of pre-existing anti-Ad5 immunity. J Immunol 172:6290–6297 [CrossRef]
    [Google Scholar]
  8. Brown K., Gao W., Alber S., Trichel A., Murphey-Corb M., Watkins S. C., Gambotto A., Barratt-Boyes S. M. 2003; Adenovirus-transduced dendritic cells injected into skin or lymph node prime potent simian immunodeficiency virus-specific T cell immunity in monkeys. J Immunol 171:6875–6882 [CrossRef]
    [Google Scholar]
  9. Casimiro D. R., Chen L., Fu T. M. & 36 other authors 2003; Comparative immunogenicity in rhesus monkeys of DNA plasmid, recombinant vaccinia virus, and replication-defective adenovirus vectors expressing a human immunodeficiency virus type 1 gag gene. J Virol 77:6305–6313 [CrossRef]
    [Google Scholar]
  10. Davis N. L., Caley I. J., Brown K. W. & 9 other authors 2000; Vaccination of macaques against pathogenic simian immunodeficiency virus with Venezuelan equine encephalitis virus replicon particles. J Virol 74:371–378 [CrossRef]
    [Google Scholar]
  11. Day R., Ganz P. A., Costantino J. P., Cronin W. M., Wickerham D. L., Fisher B. 1999; Health-related quality of life and tamoxifen in breast cancer prevention: a report from the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Clin Oncol 17:2659–2669
    [Google Scholar]
  12. 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]
  13. Fisher E. R., van Belle G. 1993 Biostatistics: a Methodology for the Health Sciences New York, NY: Wiley;
    [Google Scholar]
  14. Fitzgerald J. C., Gao G. P., Reyes-Sandoval A., Pavlakis G. N., Xiang Z. Q., Wlazlo A. P., Giles-Davis W., Wilson J. M., Ertl H. C. 2003; A simian replication-defective adenoviral recombinant vaccine to HIV-1 gag. J Immunol 170:1416–1422 [CrossRef]
    [Google Scholar]
  15. Friedrich T. C., Frye C. A., Yant L. J. & 10 other authors 2004a; Extraepitopic compensatory substitutions partially restore fitness to simian immunodeficiency virus variants that escape from an immunodominant cytotoxic-T-lymphocyte response. J Virol 78:2581–2585 [CrossRef]
    [Google Scholar]
  16. Friedrich T. C., McDermott A. B., Reynolds M. R. & 12 other authors 2004b; Consequences of cytotoxic T-lymphocyte escape: common escape mutations in simian immunodeficiency virus are poorly recognized in naive hosts. J Virol 78:10064–10073 [CrossRef]
    [Google Scholar]
  17. Fuller D. H., Rajakumar P. A., Wilson L. A. & 8 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]
  18. Gaggar A., Shayakhmetov D. M., Lieber A. 2003; CD46 is a cellular receptor for group B adenoviruses. Nat Med 9:1408–1412 [CrossRef]
    [Google Scholar]
  19. Gao W., Robbins P. D., Gambotto A. 2003a; Human adenovirus type 35: nucleotide sequence and vector development. Gene Ther 10:1941–1949 [CrossRef]
    [Google Scholar]
  20. Gao W., Tamin A., Soloff A., D'Aiuto L., Nwanegbo E., Robbins P. D., Bellini W. J., Barratt-Boyes S., Gambotto A. 2003b; Effects of a SARS-associated coronavirus vaccine in monkeys. Lancet 362:1895–1896 [CrossRef]
    [Google Scholar]
  21. Gao W., Rzewski A., Sun H., Robbins P. D., Gambotto A. 2004; UpGene: application of a web-based DNA codon optimization algorithm. Biotechnol Prog 20:443–448
    [Google Scholar]
  22. Hel Z., Nacsa J., Tryniszewska E. & 7 other authors 2002; Containment of simian immunodeficiency virus infection in vaccinated macaques: correlation with the magnitude of virus-specific pre- and postchallenge CD4+ and CD8+ T cell responses. J Immunol 169:4778–4787 [CrossRef]
    [Google Scholar]
  23. Juillard V., Villefroy P., Godfrin D., Pavirani A., Venet A., Guillet J. G. 1995; Long-term humoral and cellular immunity induced by a single immunization with replication-defective adenovirus recombinant vector. Eur J Immunol 25:3467–3473 [CrossRef]
    [Google Scholar]
  24. Kostense S., Koudstaal W., Sprangers M. & 8 other authors 2004; Adenovirus types 5 and 35 seroprevalence in AIDS risk groups supports type 35 as a vaccine vector. AIDS 18:1213–1216 [CrossRef]
    [Google Scholar]
  25. Letvin N. L., Huang Y., Chakrabarti B. K. & 15 other authors 2004; Heterologous envelope immunogens contribute to AIDS vaccine protection in rhesus monkeys. J Virol 78:7490–7497 [CrossRef]
    [Google Scholar]
  26. Mei Y. F., Skog J., Lindman K., Wadell G. 2003; Comparative analysis of the genome organization of human adenovirus 11, a member of the human adenovirus species B, and the commonly used human adenovirus 5 vector, a member of species C. J Gen Virol 84:2061–2071 [CrossRef]
    [Google Scholar]
  27. Miller M. D., Yamamoto H., Hughes A. L., Watkins D. I., Letvin N. L. 1991; Definition of an epitope and MHC class I molecule recognized by gag-specific cytotoxic T lymphocytes in SIVmac-infected rhesus monkeys. J Immunol 147:320–329
    [Google Scholar]
  28. Mothe B. R., Weinfurter J., Wang C., Rehrauer W., Wilson N., Allen T. M., Allison D. B., Watkins D. I. 2003; Expression of the major histocompatibility complex class I molecule Mamu-A*01 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 77:2736–2740 [CrossRef]
    [Google Scholar]
  29. Muhl T., Krawczak M., Ten Haaft P., Hunsmann G., Sauermann U. 2002; MHC class I alleles influence set-point viral load and survival time in simian immunodeficiency virus-infected rhesus monkeys. J Immunol 169:3438–3446 [CrossRef]
    [Google Scholar]
  30. Nwanegbo E., Vardas E., Gao W., Whittle H., Sun H., Rowe D. T., Robbins P. D., Gambotto A. 2004; Prevalence of neutralizing antibodies to adenoviral serotypes 5 and 35 in the adult populations of The Gambia, South Africa, and the United States. Clin Diagn Lab Immunol 11:351–357
    [Google Scholar]
  31. Palmowski M. J., Choi E. M., Hermans I. F. & 10 other authors 2002; Competition between CTL narrows the immune response induced by prime-boost vaccination protocols. J Immunol 168:4391–4398 [CrossRef]
    [Google Scholar]
  32. Patterson L. J., Malkevitch N., Venzon D. & 7 other authors 2004; Protection against mucosal simian immunodeficiency virus SIV(mac251) challenge by using replicating adenovirus-SIV multigene vaccine priming and subunit boosting. J Virol 78:2212–2221 [CrossRef]
    [Google Scholar]
  33. Peyerl F. W., Barouch D. H., Yeh W. W., Bazick H. S., Kunstman J., Kunstman K. J., Wolinsky S. M., Letvin N. L. 2003; Simian-human immunodeficiency virus escape from cytotoxic T-lymphocyte recognition at a structurally constrained epitope. J Virol 77:12572–12578 [CrossRef]
    [Google Scholar]
  34. Peyerl F. W., Bazick H. S., Newberg M. H., Barouch D. H., Sodroski J., Letvin N. L. 2004; Fitness costs limit viral escape from cytotoxic T lymphocytes at a structurally constrained epitope. J Virol 78:13901–13910 [CrossRef]
    [Google Scholar]
  35. Pinto A. R., Fitzgerald J. C., Giles-Davis W., Gao G. P., Wilson J. M., Ertl H. C. 2003; Induction of CD8+ T cells to an HIV-1 antigen through a prime boost regimen with heterologous E1-deleted adenoviral vaccine carriers. J Immunol 171:6774–6779 [CrossRef]
    [Google Scholar]
  36. Reyes-Sandoval A., Fitzgerald J. C., Grant R., Roy S., Xiang Z. Q., Li Y., Gao G. P., Wilson J. M., Ertl H. C. 2004; Human immunodeficiency virus type 1-specific immune responses in primates upon sequential immunization with adenoviral vaccine carriers of human and simian serotypes. J Virol 78:7392–7399 [CrossRef]
    [Google Scholar]
  37. Rose N. F., Marx P. A., Luckay A. & 7 other authors 2001; An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell 106:539–549 [CrossRef]
    [Google Scholar]
  38. Sanchez M. P., Erdman D. D., Torok T. J., Freeman C. J., Matyas B. T. 1997; Outbreak of adenovirus 35 pneumonia among adult residents and staff of a chronic care psychiatric facility. J Infect Dis 176:760–763 [CrossRef]
    [Google Scholar]
  39. Santra S., Seaman M. S., Xu L. & 13 other authors 2005; Replication-defective adenovirus serotype 5 vectors elicit durable cellular and humoral immune responses in nonhuman primates. J Virol 79:6516–6522 [CrossRef]
    [Google Scholar]
  40. Seshidhar Reddy P., Ganesh S., Limbach M. P., Brann T., Pinkstaff A., Kaloss M., Kaleko M., Connelly S. 2003; Development of adenovirus serotype 35 as a gene transfer vector. Virology 311:384–393 [CrossRef]
    [Google Scholar]
  41. Shiver J. W., Emini E. A. 2004; Recent advances in the development of HIV-1 vaccines using replication-incompetent adenovirus vectors. Annu Rev Med 55:355–372 [CrossRef]
    [Google Scholar]
  42. 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]
  43. Sullivan N. J., Geisbert T. W., Geisbert J. B., Xu L., Yang Z. Y., Roederer M., Koup R. A., Jahrling P. B., Nabel G. J. 2003; Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates. Nature 424:681–684 [CrossRef]
    [Google Scholar]
  44. Trichel A. M., Roberts E. D., Wilson L. A., Martin L. N., Ruprecht R. M., Murphey-Corb M. 1997; SIV/DeltaB670 transmission across oral, colonic, and vaginal mucosae in the macaque. J Med Primatol 26:3–10 [CrossRef]
    [Google Scholar]
  45. Vanniasinkam T., Ertl H. C. 2005; Adenoviral gene delivery for HIV-1 vaccination. Curr Gene Ther 5:203–212 [CrossRef]
    [Google Scholar]
  46. Vogels R., Zuijdgeest D., van Rijnsoever R. & 20 other authors 2003; Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: efficient human cell infection and bypass of preexisting adenovirus immunity. J Virol 77:8263–8271 [CrossRef]
    [Google Scholar]
  47. Yang Y., Li Q., Ertl H. C., Wilson J. M. 1995; Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J Virol 69:2004–2015
    [Google Scholar]
  48. Zhang Z. Q., Fu T. M., Casimiro D. R. & 14 other authors 2002; Mamu-A*01 allele-mediated attenuation of disease progression in simian-human immunodeficiency virus infection. J Virol 76:12845–12854 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81445-0
Loading
/content/journal/jgv/10.1099/vir.0.81445-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed