Route of adenovirus-based HIV-1 vaccine delivery impacts the phenotype and trafficking of vaccine-elicited CD8+ T lymphocytes

Journal of Virology

Volumn 84, Issue 12, 2010, Pages 5986-5996

  Kaufman, David R ^a   Bivas Benita, Maytal ^a   Simmons, Nathaniel L ^a   Miller, Darby ^a   Barouch, Dan H ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; HUMAN IMMUNODEFICIENCY VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELLULAR IMMUNITY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRUS RECOMBINANT;

ADENOVIRIDAE; ADMINISTRATION, INTRANASAL; AIDS VACCINES; ANIMALS; ANTIBODIES, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DRUG DELIVERY SYSTEMS; GENETIC VECTORS; HIV INFECTIONS; HUMANS; INJECTIONS, INTRAMUSCULAR; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PHENOTYPE;

ADENOVIRIDAE; HUMAN IMMUNODEFICIENCY VIRUS 1; MUS;

EID: 77952682160     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02563-09     Document Type: Article

References (46)

1. Abbink, P., A. A. Lemckert, B. A. Ewald, D. M. Lynch, M. Denholtz, S. Smits, L. Holterman, I. Damen, R. Vogels, A. R. Thorner, K. L. O'Brien, A. Carville, K. G. Mansfield, J. Goudsmit, M. J. Havenga, and D. H. Barouch. 2007. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J. Virol. 81:4654-4663. (Pubitemid 46668663)
2. Baig, J., D. B. Levy, P. F. McKay, J. E. Schmitz, S. Santra, R. A. Subbramanian, M. J. Kuroda, M. A. Lifton, D. A. Gorgone, L. S. Wyatt, B. Moss, Y. Huang, B. K. Chakrabarti, L. Xu, W. P. Kong, Z. Y. Yang, J. R. Mascola, G. J. Nabel, A. Carville, A. A. Lackner, R. S. Veazey, and N. L. Letvin. 2002. Elicitation of simian immunodeficiency virus-specific cytotoxic T lymphocytes in mucosal compartments of rhesus monkeys by systemic vaccination. J. Virol. 76:11484-11490. (Pubitemid 35231305)
3. Barouch, D. H., M. G. Pau, J. H. Custers, W. Koudstaal, S. Kostense, M. J. Havenga, D. M. Truitt, S. M. Sumida, M. G. Kishko, J. C. Arthur, B. Korioth-Schmitz, M. H. Newberg, D. A. Gorgone, M. A. Lifton, D. L. Panicali, G. J. Nabel, N. L. Letvin, and J. Goudsmit. 2004. Immunogenicity of recombinant adenovirus serotype 35 vaccine in the presence of pre-existing anti-Ad5 immunity. J. Immunol. 172:6290-6297.
4. Belyakov, I. M., J. D. Ahlers, G. J. Nabel, B. Moss, and J. A. Berzofsky. 2008. Generation of functionally active HIV-1 specific CD8+ CTL in intestinal mucosa following mucosal, systemic or mixed prime-boost immunization. Virology 381:106-115.
5. Belyakov, I. M., M. A. Derby, J. D. Ahlers, B. L. Kelsall, P. Earl, B. Moss, W. Strober, and J. A. Berzofsky. 1998. Mucosal immunization with HIV-1 peptide vaccine induces mucosal and systemic cytotoxic T lymphocytes and protective immunity in mice against intrarectal recombinant HIV-vaccinia challenge. Proc. Natl. Acad. Sci. U. S. A. 95:1709-1714.
6. Belyakov, I. M., Z. Hel, B. Kelsall, V. A. Kuznetsov, J. D. Ahlers, J. Nacsa, D. I. Watkins, T. M. Allen, A. Sette, J. Altman, R. Woodward, P. D. Markham, J. D. Clements, G. Franchini, W. Strober, and J. A. Berzofsky. 2001. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat. Med. 7:1320-1326.
7. Belyakov, I. M., D. Isakov, Q. Zhu, A. Dzutsev, and J. A. Berzofsky. 2007. A novel functional CTL avidity/activity compartmentalization to the site of mucosal immunization contributes to protection of macaques against simian/human immunodeficiency viral depletion of mucosal CD4+ T cells. J. Immunol. 178:7211-7221.
8. Betts, M. R., and R. A. Koup. 2004. Detection of T-cell degranulation: CD107a and b. Methods Cell Biol. 75:497-512.
9. Bivas-Benita, M., R. Zwier, H. E. Junginger, and G. Borchard. 2005. Non-invasive pulmonary aerosol delivery in mice by the endotracheal route. Eur. J. Pharm. Biopharm. 61:214-218.
10. Brenchley, J. M., D. A. Price, T. W. Schacker, T. E. Asher, G. Silvestri, S. Rao, Z. Kazzaz, E. Bornstein, O. Lambotte, D. Altmann, B. R. Blazar, B. Rodriguez, L. Teixeira-Johnson, A. Landay, J. N. Martin, F. M. Hecht, L. J. Picker, M. M. Lederman, S. G. Deeks, and D. C. Douek. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12:1365-1371.
11. Brenchley, J. M., T. W. Schacker, L. E. Ruff, D. A. Price, J. H. Taylor, G. J. Beilman, P. L. Nguyen, A. Khoruts, M. Larson, A. T. Haase, and D. C. Douek. 2004. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 200:749-759.
12. Casimiro, D. R., L. Chen, T. M. Fu, R. K. Evans, M. J. Caulfield, M. E. Davies, A. Tang, M. Chen, L. Huang, V. Harris, D. C. Freed, K. A. Wilson, S. Dubey, D. M. Zhu, D. Nawrocki, H. Mach, R. Troutman, L. Isopi, D. Williams, W. Hurni, Z. Xu, J. G. Smith, S. Wang, X. Liu, L. Guan, R. Long, W. Trigona, G. J. Heidecker, H. C. Perry, N. Persaud, T. J. Toner, Q. Su, X. Liang, R. Youil, M. Chastain, A. J. Bett, D. B. Volkin, E. A. Emini, and J. W. Shiver. 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. (Pubitemid 36588400)
13. Contag, C. H., P. R. Contag, J. I. Mullins, S. D. Spilman, D. K. Stevenson, and D. A. Benaron. 1995. Photonic detection of bacterial pathogens in living hosts. Mol. Microbiol. 18:593-603.
14. Croyle, M. A., A. Patel, K. N. Tran, M. Gray, Y. Zhang, J. E. Strong, H. Feldmann, and G. P. Kobinger. 2008. Nasal delivery of an adenovirus-based vaccine bypasses pre-existing immunity to the vaccine carrier and improves the immune response in mice. PLoS One 3:e3548.
15. Darrah, P. A., D. T. Patel, P. M. De Luca, R. W. Lindsay, D. F. Davey, B. J. Flynn, S. T. Hoff, P. Andersen, S. G. Reed, S. L. Morris, M. Roederer, and R. A. Seder. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13:843-850.
16. Gallichan, W. S., and K. L. Rosenthal. 1996. Long-lived cytotoxic T lymphocyte memory in mucosal tissues after mucosal but not systemic immunization. J. Exp. Med. 184:1879-1890.
17. Harari, A., S. Petitpierre, F. Vallelian, and G. Pantaleo. 2004. Skewed representation of functionally distinct populations of virus-specific CD4 T cells in HIV-1-infected subjects with progressive disease: changes after antiretroviral therapy. Blood 103:966-972. (Pubitemid 38129558)
18. Heritage, P. L., B. J. Underdown, A. L. Arsenault, D. P. Snider, and M. R. McDermott. 1997. Comparison of murine nasal-associated lymphoid tissue and Peyer's patches. Am. J. Respir. Crit. Care Med. 156:1256-1262.
19. Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76:17-27. (Pubitemid 24035278)
20. Huster, K. M., V. Busch, M. Schiemann, K. Linkemann, K. M. Kerksiek, H. Wagner, and D. H. Busch. 2004. Selective expression of IL-7 receptor on memory T cells identifies early CD40L-dependent generation of distinct CD8+ memory T cell subsets. Proc. Natl. Acad. Sci. U. S. A. 101:5610-5615.
21. Kaufman, D. R., J. Goudsmit, L. Holterman, B. A. Ewald, M. Denholtz, C. Devoy, A. Giri, L. E. Grandpre, J. M. Heraud, G. Franchini, M. S. Seaman, M. J. Havenga, and D. H. Barouch. 2008. Differential antigen requirements for protection against systemic and intranasal vaccinia virus challenges in mice. J. Virol. 82:6829-6837.
22. Kaufman, D. R., J. Liu, A. Carville, K. G. Mansfield, M. J. Havenga, J. Goudsmit, and D. H. Barouch. 2008. Trafficking of antigen-specific CD8+ T lymphocytes to mucosal surfaces following intramuscular vaccination. J. Immunol. 181:4188-4198.
23. Ko, S. Y., C. Cheng, W. P. Kong, L. Wang, M. Kanekiyo, D. Einfeld, C. R. King, J. G. Gall, and G. J. Nabel. 2009. Enhanced induction of intestinal cellular immunity by oral priming with enteric adenovirus 41 vectors. J. Virol. 83:748-756.
24. Lackner, A. A., M. Mohan, and R. S. Veazey. 2009. The gastrointestinal tract and AIDS pathogenesis. Gastroenterology 136:1965-1978.
25. Lemckert, A. A., S. M. Sumida, L. Holterman, R. Vogels, D. M. Truitt, D. M. Lynch, A. Nanda, B. A. Ewald, D. A. Gorgone, M. A. Lifton, J. Goudsmit, M. J. Havenga, and D. H. Barouch. 2005. Immunogenicity of heterologous prime-boost regimens involving recombinant adenovirus serotype 11 (Ad11) and Ad35 vaccine vectors in the presence of anti-ad5 immunity. J. Virol. 79:9694-9701.
26. Li, Q., L. Duan, J. D. Estes, Z. M. Ma, T. Rourke, Y. Wang, C. Reilly, J. Carlis, C. J. Miller, and A. T. Haase. 2005. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434:1148-1152. (Pubitemid 40663495)
27. Li, Z., M. Zhang, C. Zhou, X. Zhao, N. Iijima, and F. R. Frankel. 2008. Novel vaccination protocol with two live mucosal vectors elicits strong cell-mediated immunity in the vagina and protects against vaginal virus challenge. J. Immunol. 180:2504-2513.
28. Lin, S. W., A. S. Cun, K. Harris-McCoy, and H. C. Ertl. 2007. Intramuscular rather than oral administration of replication-defective adenoviral vaccine vector induces specific CD8+ T cell responses in the gut. Vaccine 25:2187-2193.
29. Liu, J., K. L. O'Brien, D. M. Lynch, N. L. Simmons, A. La Porte, A. M. Riggs, P. Abbink, R. T. Coffey, L. E. Grandpre, M. S. Seaman, G. Landucci, D. N. Forthal, D. C. Montefiori, A. Carville, K. G. Mansfield, M. J. Havenga, M. G. Pau, J. Goudsmit, and D. H. Barouch. 2009. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 457:87-91.
30. Mattapallil, J. J., D. C. Douek, B. Hill, Y. Nishimura, M. Martin, and M. Roederer. 2005. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434:1093-1097.
31. Pantaleo, G., and R. A. Koup. 2004. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat. Med. 10:806-810.
32. Patel, A., Y. Zhang, M. Croyle, K. Tran, M. Gray, J. Strong, H. Feldmann, J. M. Wilson, and G. P. Kobinger. 2007. Mucosal delivery of adenovirus-based vaccine protects against Ebola virus infection in mice. J. Infect. Dis. 196(Suppl. 2):S413-S420.
33. Ranasinghe, C., S. J. Turner, C. McArthur, D. B. Sutherland, J. H. Kim, P. C. Doherty, and I. A. Ramshaw. 2007. Mucosal HIV-1 pox virus primeboost immunization induces high-avidity CD8+ T cells with regime-dependent cytokine/granzyme B profiles. J. Immunol. 178:2370-2379. (Pubitemid 46233436)
34. Roberts, D. M., A. Nanda, M. J. Havenga, P. Abbink, D. M. Lynch, B. A. Ewald, J. Liu, A. R. Thorner, P. E. Swanson, D. A. Gorgone, M. A. Lifton, A. A. Lemckert, L. Holterman, B. Chen, A. Dilraj, A. Carville, K. G. Mansfield, J. Goudsmit, and D. H. Barouch. 2006. Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nature 441:239-243.
35. Rubio, V., T. B. Stuge, N. Singh, M. R. Betts, J. S. Weber, M. Roederer, and P. P. Lee. 2003. Ex vivo identification, isolation and analysis of tumor-cytolytic T cells. Nat. Med. 9:1377-1382.
36. Santosuosso, M., X. Zhang, S. McCormick, J. Wang, M. Hitt, and Z. Xing. 2005. Mechanisms of mucosal and parenteral tuberculosis vaccinations: adenoviral-based mucosal immunization preferentially elicits sustained accumulation of immune protective CD4 and CD8 T cells within the airway lumen. J. Immunol. 174:7986-7994. (Pubitemid 40806309)
37. Sené, C., A. Bout, J. L. Imler, H. Schultz, J. M. Willemot, V. Hennebel, C. Zurcher, D. Valerio, D. Lamy, and A. Pavirani. 1995. Aerosol-mediated delivery of recombinant adenovirus to the airways of nonhuman primates. Hum. Gene Ther. 6:1587-1593.
38. Smith, D. J., S. Bot, L. Dellamary, and A. Bot. 2003. Evaluation of novel aerosol formulations designed for mucosal vaccination against influenza virus. Vaccine 21:2805-2812.
39. Southam, D. S., M. Dolovich, P. M. O'Byrne, and M. D. Inman. 2002. Distribution of intranasal instillations in mice: effects of volume, time, body position, and anesthesia. Am. J. Physiol. Lung Cell. Mol. Physiol. 282:L833-L839.
40. Stevceva, L., X. Alvarez, A. A. Lackner, E. Tryniszewska, B. Kelsall, J. Nacsa, J. Tartaglia, W. Strober, and G. Franchini. 2002. Both mucosal and systemic routes of immunization with the live, attenuated NYVAC/simian immunodeficiency virus SIV(gpe) recombinant vaccine result in gag-specific CD8(+) T-cell responses in mucosal tissues of macaques. J. Virol. 76:11659-11676. (Pubitemid 35231321)
41. Tatsis, N., S. W. Lin, K. Harris-McCoy, D. A. Garber, M. B. Feinberg, and H. C. Ertl. 2007. Multiple immunizations with adenovirus and MVA vectors improve CD8+ T cell functionality and mucosal homing. Virology 367:156-167. (Pubitemid 47432788)
42. Veazey, R. S., M. DeMaria, L. V. Chalifoux, D. E. Shvetz, D. R. Pauley, H. L. Knight, M. Rosenzweig, R. P. Johnson, R. C. Desrosiers, and A. A. Lackner. 1998. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280:427-431.
43. Wang, J., L. Thorson, R. W. Stokes, M. Santosuosso, K. Huygen, A. Zganiacz, M. Hitt, and Z. Xing. 2004. Single mucosal, but not parenteral, immunization with recombinant adenoviral-based vaccine provides potent protection from pulmonary tuberculosis. J. Immunol. 173:6357-6365. (Pubitemid 39487795)
44. Wang, L., C. Cheng, S. Y. Ko, W. P. Kong, M. Kanekiyo, D. Einfeld, R. M. Schwartz, C. R. King, J. G. Gall, and G. J. Nabel. 2009. Delivery of human immunodeficiency virus vaccine vectors to the intestine induces enhanced mucosal cellular immunity. J. Virol. 83:7166-7175.
45. Williams, M. A., and M. J. Bevan. 2007. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25:171-192.
46. Zhu, Q., C. W. Thomson, K. L. Rosenthal, M. R. McDermott, S. M. Collins, and J. Gauldie. 2008. Immunization with adenovirus at the large intestinal mucosa as an effective vaccination strategy against sexually transmitted viral infection. Mucosal Immunol. 1:78-88.