Signature for long-term vaccine-mediated control of a simian and human immunodeficiency virus 89.6P challenge: Stable low-breadth and low-frequency T-cell response capable of coproducing gamma interferon and interleukin-2

Journal of Virology

Volumn 79, Issue 6, 2005, Pages 3243-3253

  Sadagopal, Shanmugalakshmi ^a   Amara, Rama Rao ^a   Montefiori, David C ^b   Wyatt, Linda S ^c   Staprans, Silvija I ^d   Kozyr, Natalia L ^d   McClure, Harold M ^a   Moss, Bernard ^c   Robinson, Harriet L ^a  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; EPITOPE; GAMMA INTERFERON; INTERLEUKIN 2; NEUTRALIZING ANTIBODY; VACCINE;

ARTICLE; CELL ACTIVITY; EUTHANASIA; HISTOCOMPATIBILITY; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE DEFICIENCY; MACACA; NONHUMAN; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE; VIREMIA; VIRUS INFECTION; VIRUS LOAD;

AIDS VACCINES; ANIMALS; CD4 LYMPHOCYTE COUNT; DISEASE MODELS, ANIMAL; EPITOPES; GENE PRODUCTS, ENV; GENE PRODUCTS, GAG; GENE PRODUCTS, POL; HIV; INTERFERON TYPE II; INTERLEUKIN-2; MACACA; RNA, VIRAL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES; VACCINES, DNA; VACCINIA VIRUS; VIRAL LOAD; VIREMIA;

EID: 14744278299     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.6.3243-3253.2005     Document Type: Article

References (48)

1. Addo, M. M., X. G. Yu, A. Rathod, D. Cohen, R. L. Eldridge, D. Strick, M. N. Johnston, C. Corcoran, A. G. Wurcel, C. A. Fitzpatrick, M. E. Feeney, W. R. Rodriguez, N. Basgoz, R. Draenert, D. R. Stone, C. Brander, P. J. Goulder, E. S. Rosenberg, M. Altfeld, and B. D. Walker. 2003. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J. Virol. 77:2081-2092.
2. Allen, T. M., M. Altfeld, X. G. Yu, K. M. O'Sullivan, M. Lichterfeld, S. Le Gall, M. John, B. R. Mothe, P. K. Lee, E. T. Kalife, D. E. Cohen, K. A. Freedberg, D. A. Strick, M. N. Johnston, A. Sette, E. S. Rosenberg, S. A. Mallal, P. J. Goulder, C. Brander, and B. D. Walker. 2004. Selection, transmission, and reversion of an antigen-processing cytotoxic T-lymphocyte escape mutation in human immunodeficiency virus type 1 infection. J. Virol. 78:7069-7078.
3. Altfeld, M., T. M. Allen, X. G. Yu, M. N. Johnston, D. Agrawal, B. Korber, D. Montefiori, D. H. O'Connor, B. T. Davis, P. K. Lee, E. L. Maier, J. Harlow, P. J. R. Goulder, C. Brander, E. Rosenberg, and B. Walker. 2002. HIV-1 superinfection despite broad CD8+ T cell responses containing replication of the primary virus. Nature 420:434-439.
4. Amara, R. R., J. M. Smith, S. I. Staprans, D. C. Montefiori, F. Villinger, J. D. Altman, S. P. O'Neil, N. L. Kozyr, Y. Xu, L. S. Wyatt, P. L. Earl, J. G. Herndon, J. M. McNicholl, H. M. McClure, B. Moss, and H. L. Robinson. 2002. Critical role for Env as well as Gag-Pol in control of a simian-human immunodeficiency virus 89.6P challenge by a DNA prime/recombinant modified vaccinia virus Ankara vaccine. J. Virol. 76:6138-6146.
5. Amara, R. R., F. Villinger, J. D. Altman, S. L. Lydy, S. P. O'Neil, S. Staprans, D. C. Montefiori, Y. Xu, J. G. Herndon, L. S. Wyatt, M. A. Candido, N. L. Kozyr, P. L. Earl, J. M. Smith, H.-L. Ma, B. D. Grimm, M. L. Hulsey, J. Miller, H. M. McClure, J. M. McNicholl, B. Moss, and H. L. Robinson. 2001. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292:69-74.
6. 5a. Anonymous. 1996. Guide for the care and use of laboratory animals. Institute of Laboratory Animal Resources, Commission of Life Sciences, National Research Council, National Academy Press, Washington, D.C.
7. Barouch, D. H., J. Kunstman, J. Glowczwskie, K. J. Kunstman, M. A. Egan, F. W. Peyerl, S. Santra, M. J. Kuroda, J. E. Schmitz, K. Beaudry, G. R. Krivulka, M. A. Lifton, D. A. Gorgone, S. M. Wolinsky, and N. L. Letvin. 2003. Viral escape from dominant simian immunodeficiency virus epitope-specific cytotoxic T lymphocytes in DNA-vaccinated rhesus monkeys. J. Virol. 77:7367-7375.
8. Barouch, D. H., J. Kuntsman, M. J. Kuroda, J. E. Schmitz, S. Santra, F. W. Peyerl, G. R. Krivulka, K. Beaudry, M. A. Lifton, D. A. Gorgone, D. Montefiori, M. G. Lewis, S. M. Wolinsky, and N. L. Letvin. 2002. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415:335-339.
9. Barouch, D. H., S. Santra, J. E. Schmitz, M. J. Kuroda, T. M. Fu, W. Wagner, M. Bilska, A. Craiu, X. X. Zheng, G. R. Krivulka, K. Beaudry, M. A. Lifton, C. E. Nickerson, W. L. Trigona, K. Punt, D. C. Freed, L. Guan, S. Dubey, D. Casimiro, A. Simon, M. E. Davies, M. Chastain, T. B. Strom, R. S. Gelman, D. C. Montefiori, and M. G. Lewis. 2000. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290:486-492.
10. Blattman, J. N., J. M. Grayson, E. J. Wherry, S. M. Kaech, K. A. Smith, and R. Ahmed. 2003. Therapeutic use of IL-2 to enhance antiviral T-cell responses in vivo. Nat. Med. 9:540-547.
11. Boaz, M. J., A. Waters, S. Murad, P. J. Easterbrook, E. D'Sousa, C. van Wheeley, and A. Vyakarnam. 2003. CD4 responses to conserved HIV-1 T helper epitopes show both negative and positive associations with virus load in chronically infected subjects. Clin. Exp. Immunol. 134:454-463.
12. Boaz, M. J., A. Waters, S. Murad, P. J. Easterbrook, and A. Vyakarnam. 2002. Presence of HIV-1 Gag-specific IFN-gamma+IL-2+ and CD28+IL-2+ CD4 T cell responses is associated with nonprogression in HIV-1 infection. J. Immunol. 169:6376-6385.
13. Buge, S. L., H. L. Ma, R. R. Amara, L. S. Wyatt, P. L. Earl, F. Villinger, D. C. Montefiori, S. I. Staprans, Y. Xu, E. Carter, S. P. O'Neil, J. G. Herndon, E. Hill, B. Moss, H. L. Robinson, and J. M. McNicholl. 2003. Gp120-alum boosting of a Gag-Pol-Env DNA/MVA AIDS vaccine: poorer control of a pathogenic viral challenge. AIDS Res. Hum. Retrovir. 19:891-900.
14. 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.
15. Casimiro, D. R., A. Tang, L. Chen, T. M. Fu, R. K. Evans, M. E. Davies, D. C. Freed, W. Hurni, J. M. Aste-Amezaga, L. Guan, R. Long, L. Huang, V. Harris, D. K. Nawrocki, H. Mach, R. D. Troutman, L. A. Isopi, K. K. Murthy, K. Rice, K. A. Wilson, D. B. Volkin, E. A. Emini, and J. W. Shiver. 2003. Vaccine-induced immunity in baboons by using DNA and replication-incompetent adenovirus type 5 vectors expressing a human immunodeficiency virus type 1 gag gene. J. Virol. 77:7663-7668.
16. +-T-cell depletion after simian-human immunodeficiency virus SHIV89.6P mucosal challenge. J. Virol. 77:11563-11577.
17. Douek, D. C., J. M. Brenchley, M. R. Betts, D. R. Ambrozak, B. J. Hill, Y. Okamoto, J. P. Casazza, J. Kuruppu, K. Kunstman, S. Wolinsky, Z. Grossman, M. Dybul, A. Oxenius, D. A. Price, M. Connors, and R. A. Koup. 2002. HIV preferentially infects HIV-specific CD4+ T cells. Nature 417:95-98.
18. Draenert, R., S. Le Gall, K. J. Pfafferott, A. J. Leslie, P. Chetty, C. Brander, E. C. Holmes, S. C. Chang, M. E. Feeney, M. M. Addo, L. Ruiz, D. Ramduth, P. Jeena, M. Altfeld, S. Thomas, Y. Tang, C. L. Verrill, C. Dixon, J. G. Prado, P. Kiepiela, J. Martinez-Picado, B. D. Walker, and P. J. Goulder. 2004. Immune selection for altered antigen processing leads to cytotoxic T lymphocyte escape in chronic HIV-1 infection. J. Exp. Med. 199:905-915.
19. Earl, P. L., L. S. Wyatt, D. C. Montefiori, M. Bilska, R. Woodward, P. D. Markham, J. D. Malley, T. U. Vogel, T. M. Allen, D. I. Watkins, N. Miller, and B. Moss. 2002. Comparison of vaccine strategies using recombinant env-gag-pol MVA with or without an oligomeric Env protein boost in the SHIV rhesus macaque model. Virology 294:270-281.
20. Friedrich, T. C., E. J. Dodds, L. J. Yant, L. Vojnov, R. Rudersdorf, C. Cullen, D. T. Evans, R. C. Desrosiers, B. R. Mothe, J. Sidney, A. Sette, K. Kunstman, S. Wolinsky, M. Piatak, J. Lifson, A. L. Hughes, N. Wilson, D. H. O'Connor, and D. I. Watkins. 2004. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat. Med. 10:275-281.
21. Goulder, P., D. Price, M. Nowak, S. Rowland-Jones, R. Phillips, and A. McMichael. 1997. Co-evolution of human immunodeficiency virus and cytotoxic T-lymphocyte responses. Immunol. Rev. 159:17-29.
22. Goulder, P. J., and D. I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4:630-640.
23. 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.
24. Horton, H., T. U. Vogel, D. K. Carter, K. Vielhuber, D. H. Fuller, T. Shipley, J. T. Fuller, K. J. Kunstman, G. Sutter, D. C. Montefiori, V. Erfle, R. C. Desrosiers, N. Wilson, L. J. Picker, S. M. Wolinsky, C. Wang, D. B. Allison, and D. I. Watkins. 2002. Immunization of rhesus macaques with a DNA prime/modified vaccinia virus Ankara boost regimen induces broad simian immunodeficiency virus (SIV)-specific T-cell responses and reduces initial viral replication but does not prevent disease progression following challenge with pathogenic SIVmac239. J. Virol. 76:7187-7202.
25. + T cells is associated with diminished interleukin-2 (IL-2) production and is recovered by exogenous IL-2. J. Virol. 77:10900-10909.
26. Kahn, P. 2003. AIDS vaccines, from monkeys to people: an interview with John Shriver, p. 10-12. In Press, Washington, D.C. P. Kahn (ed.), IAVI report, vol. 7, no. 2 West End Graphics, New York, N.Y.
27. Kantzanou, M., M. Lucas, E. Barnes, H. Komatsu, G. Dusheiko, S. Ward, G. Harcourt, and P. Klenerman. 2003. Viral escape and T cell exhaustion in hepatitis C virus infection analysed using class I peptide tetramers. Immunol. Lett. 85:165-171.
28. +-T-cell response to human cytomegalovirus: the 72-kilodalton major immediate-early protein revisited. J. Virol. 73:8179-8184.
29. Kostense, S., K. Vandenberghe, J. Joling, D. Van Baarle, N. Nanlohy, E. Manting, and F. Miedema. 2002. Persistent numbers of tetramer+ CD8(+) T cells, but loss of interferon-gamma+ HIV-specific T cells during progression to AIDS. Blood 99:2505-2511.
30. Letvin, N. L., Y. Huang, B. K. Chakrabarti, L. Xu, M. S. Seaman, K. Beaudry, B. Korioth-Schmitz, F. Yu, D. Rohne, K. L. Martin, A. Miura, W. P. Kong, Z. Y. Yang, R. S. Gelman, O. G. Golubeva, D. C. Montefiori, J. R. Mascola, and G. J. Nabel. 2004. Heterologous envelope immunogens contribute to AIDS vaccine protection in rhesus monkeys. J. Virol. 78:7490-7497.
31. McKay, P. F., J. E. Schmitz, D. H. Barouch, M. J. Kuroda, M. A. Lifton, C. E. Nickerson, D. A. Gorgone, and N. L. Letvin. 2002. Vaccine protection against functional CTL abnormalities in simian human immunodeficiency virus-infected rhesus monkeys. J. Immunol. 168:332-337.
32. Mellors, J. W., C. R. Rinaldo, Jr., P. Gupta, R. M. White, J. A. Todd, and L. A. Kingsley. 1996. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272:1167-1170.
33. Migueles, S. A., A. C. Laborico, W. L. Shupert, M. S. Sabbaghian, R. Rabin, C. W. Hallahan, D. Van Baarle, S. Kostense, F. Miedema, M. McLaughlin, L. Ehler, J. Metcalf, S. Liu, and M. Connors. 2002. HIV-specific CD8+ T cell proliferation is coupled to perform expression and is maintained in nonprogressors. Nat. Immunol. 3:1061-1068.
34. Montefiori, D. C., K. A. Reimann, M. S. Wyand, K. Manson, M. G. Lewis, R. G. Collman, J. G. Sodroski, D. P. Bolognesi, and N. L. Letvin. 1998. Neutralizing antibodies in sera from macaques infected with chimeric simian-human immunodeficiency virus containing the envelope glycoproteins of either a laboratory-adapted variant or a primary isolate of human immunodeficiency virus type 1. J. Virol. 72:3427-3431.
35. Moskophidis, D., F. Lechner, H. Pircher, and R. M. Zinkernagel. 1993. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362:758-761.
36. mac239 replication. J. Virol. 77:2736-2740.
37. mac-induced immunodeficiency. J. Virol. 76:292-302.
38. 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.
39. Parren, P. W., and D. R. Burton. 2001. The antiviral activity of antibodies in vitro and in vivo. Adv. Immunol. 77:195-262.
40. Quinn, T. C., M. J. Wawer, N. Sewankambo, D. Serwadda, C. Li, F. Wabwire-Mangen, M. O. Meehan, T. Lutalo, and R. H. Gray for the Rakai Project Study Group. 2000. Viral load and heterosexual transmission of human immunodeficiency virus type 1. N. Engl. J. Med. 342:921-929.
41. Robinson, H. L. 2002. New hope for an AIDS vaccine. Nat. Rev. Immunol. 2:239-250.
42. Shiver, J. W., T. Fu, L. Chen, D. Casimiro, M. E. Davies, R. K. Evans, Z.-Q. Zhang, A. Simon, W. L. Trigona, S. Dubey, L. Huang, V. A. Harris, R. S. Long, L. Xiaoping, L. Handt, W. A. Schleif, L. Zhu, D. C. Freed, N. V. Persaud, L. Guan, K. Punt, A. Tang, M. Chen, K. A. Wilson, K. B. Collins, G. J. Heidecker, H. C. Perry, J. G. Joyce, K. M. Grimm, J. C. Cook, P. M. Keller, D. S. Kresock, H. Mach, R. D. Troutman, L. A. Iospi, D. M. Williams, Z. Xu, K. E. Bohannon, D. B. Volkin, D. Montefiori, A. Miura, G. R. Krivulka, M. A. Lifton, M. J. Kuroda, J. E. Schmitz, N. L. Letvin, M. J. Caulfield, A. J. Bett, R. Youil, D. C. Kaslow, and E. A. Emini. 2002. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency virus immunity. Nature 415:331-335.
43. Tang, Y., F. Villinger, S. I. Staprans, R. R. Amara, J. M. Smith, J. G. Herndon, and H. L. Robinson. 2002. Slowly declining levels of viral RNA and DNA in DNA/recombinant modified vaccinia virus Ankara-vaccinated macaques with controlled simian-human immunodeficiency virus SHIV-89.6P challenges. J. Virol. 76:10147-10154.
44. Wherry, E. J., J. N. Blattman, K. Murali-Krishna, R. van der Most, and R. Ahmed. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77:4911-4927.
45. Wherry, E. J., K. A. Puorro, A. Porgador, and L. C. Eisenlohr. 1999. The induction of virus-specific CTL as a function of increasing epitope expression: responses rise steadily until excessively high levels of epitope are attained. J. Immunol. 163:3735-3745.
46. Yokomaku, Y., H. Miura, H. Tomiyama, A. Kawana-Tachikawa, M. Takiguchi, A. Kojima, Y. Nagai, A. Iwamoto, Z. Matsuda, and K. Ariyoshi. 2004. Impaired processing and presentation of cytotoxic-T-lymphocyte (CTL) epitopes are major escape mechanisms from CTL immune pressure in human immunodeficiency virus type 1 infection. J. Virol. 78:1324-1332.
47. Younes, S. A., B. Yassine-Diab, A. R. Dumont, M. R. Boulassel, Z. Grossman, J. P. Routy, and R. P. Sekaly. 2003. HIV-1 viremia prevents the establishment of interleukin 2-producing HIV-specific memory CD4+ T cells endowed with proliferative capacity. J. Exp. Med. 198:1909-1922.
48. Zajac, A. J., J. N. Blattman, K. Murali-Krishna, D. J. Sourdive, M. Suresh, J. D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188:2205-2213.