Immunization with a modified vaccinia virus expressing simian immunodeficiency virus (SIV) Gag-Pol primes for an anamnestic Gag-specific cytotoxic T-lymphocyte response and is associated with reduction of viremia after SIV challenge

Journal of Virology

Volumn 74, Issue 6, 2000, Pages 2502-2509

  Seth, Aruna ^a   Ourmanov, Ilnour ^b   Schmitz, Jorn E ^a   Kuroda, Marcelo J ^a   Lifton, Michelle A ^a   Nickerson, Christine E ^a   Wyatt, Linda ^b   Carroll, Miles ^b   Moss, Bernard ^b   Venzon, David ^c   Letvin, Norman L ^a   Hirsch, Vanessa M ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

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

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; POL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNIZATION; IMMUNOMODULATION; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINIA VIRUS; VIREMIA; VIRUS GENE;

ANIMALS; FUSION PROTEINS, GAG-POL; GENETIC VECTORS; MACACA MULATTA; PREDICTIVE VALUE OF TESTS; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES, CYTOTOXIC; VACCINIA VIRUS; VIRAL LOAD; VIREMIA;

EID: 0034088113     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.6.2502-2509.2000     Document Type: Article

References (55)

1. Abimuki, A. G., M. Robert-Guroff, J. Benson, J. Tartaglia, E. Paoletti, R. C. Gallo, P. D. Markham, and G. Franchini. 1997. Long-term survival of SIV-mac251-infected macaques previously immunized with NYVAC-SIV vaccines. J. Acquired Immune Defic. Syndr. Hum. Retrovirol. 15;S78-S85.
2. Ahmad, S., B. Lohman, M. Marthas, L. Giavedoni, Z. el-Amad, N. L. Haigwood, C. J. Scandella, M. B. Gardner, P. A. Luciw, and T. Yilma. 1994. Reduced virus load in rhesus macaques immunized with recombinant gp160 and challenged with simian immunodeficiency virus. AIDS Res. Hum. Retroviruses 10:195-204.
3. Altman, J. D., P. A. H. Moss, P. J. R. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274:94-96.
4. Andersson, S., B. Makitalo, R. Thorstensson, G. Franchini, J. Tartaglia, K. Limbach, E. Paoletti, P. Putkonen, and G. Biberfeld. 1996. Immunogenicity and protective efficacy of a human immunodeficiency virus type 2 recombinant canarypox (ALVAC) vaccine candidate in cynomolgus monkeys. J. Infect. Dis. 174:977-985.
5. Antoine, G., F. Scheiflinger, F. Dorner, and F. G. Falkner. 1998. The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244:365-396.
6. Belyakov, I. M., L. S. Wyatt, J. D. Ahlers, P. Earl, C. D. Pendleton, B. L. Kelsall, W. Strober, B. Moss, and J. A. Berzofsky. 1998. Induction of a mucosal cytotoxic T-lymphocyte response by intrarectal immunization with a replication-deficient recombinant vaccinia virus expressing human immunodeficiency virus 89.6 envelope protein. J. Virol. 72:8264-8272.
7. Benson, J., C. Chougnet, M. Robert-Guroff, D. Montefiori, P. Markham, G. Shearer, R. C. Gallo, M. Cranage, E. Paoletti, K. Limbach, D. Venzon, J. Tartaglia, and G. Franchini. 1998. Recombinant vaccine-induced protection against the highly pathogenic simian immunodeficiency virus SIVmac251: dependence on route of challenge exposure. J. Virol. 72:4170-4182.
8. Berglund, P., M. Quesada-Rolander, P. Putkonen, G. Biberfeld, R. Thorstensson, and P. Liljestrom. 1997. Outcome of immunization of cynomolgus monkeys with recombinant Semliki Forest virus encoding human immunodeficiency virus type 1 envelope protein and challenge with a high dose of SHIV-4 virus. AIDS Res. Hum. Retroviruses 13:1487-1495.
9. Blanchard, T. J., A. Alcami, A. Panayota, and G. L. Smith. 1998. Modified vaccinia virus Ankara undergoes limited replication in human cells and lack several immunomodulatory proteins: implications for use as a human vaccine. J. Gen. Virol. 79:1159-1167.
10. Buge, S. L., E. Richardson, S. Alipanah, P. Markham, S. Cheng, N. Kalyan, C. J. Miller, M. Lubeck, S. Udem, J. Eldridge, and M. Robert-Guroff. 1997. An adenovirus simian immunodeficiency virus env vaccine elicits humoral, cellular, and mucosal immune responses in rhesus macaques and decreases viral burden following vaginal challenge. J. Virol. 71:8531-8541.
11. Caley, I. J., M. R. Betts, D. M. Irlbeck, N. L. Davis, R. Swanstrom, J. A. Frelinger, and R. E. Johnston. 1997. Humoral, mucosal, and cellular immunity in response to a human immunodeficiency virus type 1 immunogen expressed by a Venezuelan equine encephalitis virus vaccine vector. J. Virol. 71:3031-3038.
12. Cao, Y., L. Qin, L. Zhang, J. Safrit, and D. Ho. 1995. Virologie and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N. Engl. J. Med. 332:201-208.
13. Carroll, M., and B. Moss. 1997. Host range and cytopathogenicity of the highly attenuated MVA strain of vaccinia virus: propagation and generation of recombinant viruses in nonhuman mammalian cell line. Virology 244:365-396.
14. Franchini, G., M. Robert-Guroff, J. Tartaglia, A. Aggarwal, A. Abimiku, J. Benson, P. Markham, K. Limbach, G. Hurteau, J. Fullen, et al. 1995. Highly attenuated HIV type 2 recombinant poxviruses, but not HIV-2 recombinant Salmonella vaccines, induce long-lasting protection in rhesus macaques. AIDS Res. Hum. Retroviruses 11:909-920.
15. Gallimore, A., M. Cranage, N. Cook, N. Almond, J. Bootman, E. Rud, P. Silvera, M. Dennis, T. Corcoran, J. Stott, A. McMichael, and F. Gotch. 1995. Early suppression of SIV replication by CD8+ nef-specific cytotoxic T cells in vaccinated macaques. Nat. Med. 1:1167-1173.
16. Goh, W. C., J. Markee, R. E. Akridge, M. Meldorf, L. Musey, T. Karchmer, M. Krone, A. Collier, L. Corey, M. Emerman, and M. J. McElrath. 1999. Protection against human immunodeficiency virus type 1 infection in persons with repeated exposure: evidence for T cell immunity in the absence of inherited CCR5 coreceptor defects. J. Infect. Dis. 179:548-557.
17. Hanke, T., T. J. Blanchard, J. Schneider, G. S. Ogg, R. Tan, M. Becker, S. C. Gilbert, A. V. S. Hill, G. L. Smith, and A. McMichael. 1998. Immunogenicity of intravenous and intramuscular administrations of modified vaccinia virus Ankara-based multi-CTL epitope vaccine for human immunodeficiency virus type 1 in mice. J. Gen. Virol. 79:83-90.
18. Hirsch, V. M., and P. R. Johnson. 1994. Pathogenic diversity of simian immunodeficiency viruses. Virus Res. 32:183-203.
19. Hirsch, V. M., T. R. Fuerst, G. Sutter, M. W. Carroll, L. C. Yang, S. Goldstein, M. Piatak, W. R. Elkins, W. G. Alvord, D. C. Montefiori, B. Moss, and J. D. Lifson. 1996. Patterns of viral replication correlate with outcome in simian immunodeficiency virus (SIV)-infected macaques: effect of prior immunization with a trivalent SIV vaccine in modified vaccinia virus Ankara. J. Virol. 70:3741-3752.
20. Hu, S. L., K. Abrams, G. N. Barber, P. Moran, J. M. Zarling, A. J. Langlois, L. Kuller, W. R. Morton, and R. E. Benveniste. 1992. Protection of macaques against SIV infection by recombinant subunit vaccines using SIV env glycoprotein gp 160. Science 255:456-459.
21. Joag, S. V., Z. Li, C. Y. Wang, F. L. Jia, L. Foresman, I. Adany, D. M. Pinson, E. B. Stephens, and O. Narayan. 1998. Chimeric SHIV that causes CD4(+) T cell loss and AIDS in rhesus macaques. J. Med. Primatol. 27:59-64.
22. Kent, S. J., A. Zhao, S. J. Best, J. D. Chandler, D. B. Boyle, and I. A. Ramshaw. 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.
23. Koup, R. A., J. T. Safrit, Y. Z. Cao, C. A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D. D. Ho. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-4655.
24. Kuroda, M. J., J. E. Schmitz, D. H. Barouch, A. Craiu, T. M. Allen, A. Sette, D. I. Watkins, M. A. Forman, and N. L. Letvin. 1998. Analysis of Gag-specific cytotoxic T lymphocytes in simian immunodeficiency virus-infected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J. Exp. Med. 187:1373-1381.
25. Kuroda, M. J., J. E. Schmitz, W. A. Charini, C. E. Nickerson, M. A. Lifton, C. I. Lord, M. A. Forman, and N. L. Letvin. 1999. Emergence of CTL coincides with clearance of virus during primary simian immunodeficiency virus infection in rhesus monkeys. J. Immunol. 162:5127-5133.
26. Letvin, N. L. 1998. Progress in the development of an HIV-1 vaccine. Science 280:1875-1880.
27. Lifson, J. D., M. A. Nowak, S. Goldstein, J. L. Rossio, A. Kinter, G. Vasquez, T. A. Wiltrout, C. Brown, D. Schneider, L. Wahl, A. L. Lloyd, J. Williams, W. R. Elkins, A. S. Fauci, and V. M. Hirsch. 1997. The extent of early virus replication is a critical determinant of the natural history of AIDS virus infection. J. Virol. 71:9508-9514.
28. Lu, Y. C., C. D. Pauza, X. S. Lu, D. C. Montefiori, and C. J. Miller. 1998. Rhesus macaques that become systemically infected with pathogenic SHIV 89.6-PD after intravenous, rectal, or vaginal inoculation and fail to make an antiviral antibody response rapidly develop AIDS. J. Acquired Immune Defic. Syndr. 19:6-18.
29. Mayr, A., V. Hochstein-Mintzel, and H. Stickl. 1975. Abstammung, Eigenschaften und Verwendung des attenuierten Vaccinia-stammes MVA. Infection 3:6-14.
30. Mayr, A., H. Stickl, H. K. Muller, K. Danner, and H. Singer. 1978. The smallpox vaccination strain MVA: marker, genetic structure, experience gained with the parenteral vaccination and behavior in organisms with a debilitated defence mechanism. Zentbl. Bakteriol. Hyg. B 167:375-390.
31. 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.
32. Meyer, H., G. Sutter, and A. Mayr. 1992. Mapping of deletions in the genome of the highly attenuated vaccinia virus MVA and their influence on virulence. J. Gen. Virol. 72:1031-1038.
33. Morrow, C. D., M. J. Novak, D. C. Ansardi, D. C. Porter, and Z. Moldoveanu. 1999. Recombinant viruses as vectors for mucosal immunity. Curr. Top. Microbiol. Immunol. 236:255-273.
34. Moss, B., M. W. Carroll, L. S. Wyatt, J. R. Bennink, V. M. Hirsch, S. Goldstein, W. R. Elkins, J. D. Lifson, M. Piatak, N. P. Restifo, W. Owerwijk, R. Chamberlain, S. A. Rosenberg, and G. Sutter. 1996. Host range restricted, non-replicating vaccinia virus vectors as vaccine candidates. Adv. Exp. Med. Biol. 397:7-13.
35. Mossman, S. P., F. Bex, P. Berglund, J. Arthos, S. P. ONeil, D. Riley, D. H. Maul, C. Bruck, P. Momin, A. Burny, P. N. Fultz, J. I. Mullins, P. Liljestrom, and E. A. Hoover. 1996. Protection against lethal simian immunodeficiency virus SIVsmmPBj14 disease by a recombinant Semliki Forest virus gp160 vaccine and by a gp120 subunit vaccine. J. Virol. 70:1953-1960.
36. Musey, L., J. Hughes, T. Schacker, T. Shea, L. Corey, and M. J. McElrath. 1997. Cytotoxic-T-cell responses, viral load, and disease progression in early human immunodeficiency virus type 1 infection. N. Engl. J. Med 337:1267-1274.
37. Myagkikh, M., S. Alipanah, P. D. Markham, J. Tartaglia, E. Paoletti, R. C. Gallo, G. Franchini, and M. Robert-Guroff. 1996. Multiple immunizations with attenuated poxvirus HIV type 2 recombinants and subunit boosts required for protection of rhesus macaques. AIDS Res. Hum. Retroviruses 12:985-992.
38. National Institutes of Health. 1985. Guide for the care and use of laboratory animals, rev. ed. Department of Health and Human Services publication no. (NIH) 85-23. National Institutes of Health. Bethesda, Md.
39. Ogg, G. S., X. Jin, S. Bonhoeffer, P. R. Dunbar, M. A. Nowak, S. Monard, J. P. Segal, Y. Z. Cao, S. L. Rowland-Jones, V. Cerundolo, A. Hurley, M. Markowitz, D. D. Ho, D. F. Nixon, and A. J. McMichael. 1998. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279:2103-2106.
40. Ourmanov, I., M. Bilska, V. M. Hirsch, and D. C. Montefiori. 2000. Recombinant modified vaccinia virus Ankara expressing the surface gp 120 of simian immunodeficiency virus (SIV) primes for a rapid neutralizing antibody response to SIV infection in macaques. J. Virol. 74:2960-2965.
41. Ourmanov, I., C. R. Brown, B. Moss, M. Carroll, L. Wyatt, L. Pletneva, S. Goldstein, D. Venzon, and V. M. Hirsch. 2000. Comparative efficacy of recombinant modified vaccinia virus Ankara expressing simian immunodeficiency virus (SIV) Gag-Pol and/or Env in macaques challenged with pathogenic SIV. J. Virol. 74:2740-2751.
42. Panteleo, G., S. Menzo, M. Vaccarezza, C. Graziosi, O. J. Cohen, J. F. Demarest, D. C. Montefiori, J. M. Orenstein, C. Fox, L. K. Schrager, and A. S. Fauci. 1995. Studies in subjects with long-term nonprogressive human immunodeficiency virus infection. N. Engl. J. Med. 332:209-216.
43. Paoletti, E. 1996. Applications of pox virus vectors to vaccination: an update. Proc. Natl. Acad. Sci. USA 93:11349-11353.
44. Polacino, P., V. Stallard, J. E. Klaniecki, D. C. Montefiori, A. J. Langlois, B. A. Richardson, J. Overbaugh, W. R. Morton, R. E. Benveniste, and S. L. Hu. 1999. Limited breadth of the protective immunity elicited by simian immunodeficiency virus SIVmne gp160 vaccines in a combination immunization regimen. J. Virol. 73:618-630.
45. Polacino, P., V. Stallard, D. C. Montefiori, C. R. Brown, B. A. Richardson, W. R. Morton, R. E. Benveniste, and S. L. Hu. 1999. Protection of macaques against intrarectal infection by a combination immunization regimen with recombinant simian immunodeficiency virus SIVmne gp160 vaccines. J. Virol. 73:3134-3146.
46. Polacino, P. S., V. Stallard, J. E. Klaniecki, S. Pennathur, D. C. Montefiori, A. J. Langlois, B. A. Richardson, W. R. Morton, R. E. Benveniste, and S. L. Hu. 1999. Role of immune responses against the envelope and the core antigens of simian immunodeficiency virus SIVmne in protection against homologous cloned and uncloned virus challenge in macaques. J. Virol. 73:8201-8215.
47. Redfield, R. R., D. C. Wright, W. D. James, T. S. Jones, C. Brown, and D. S. Burke. 1987. Disseminated vaccinia in a military recruit with human immunodeficiency virus (HIV) disease. N. Engl. J. Med. 316:673-676.
48. Robert-Guroff, M., H. Kaur, L. J. Patterson, M. Leno, A. J. Conley, P. M. McKenna, P. D. Markham, E. Richardson, K. Aldrich. K. Arora, L. Murty, L. Carter, S. Zolla-Pazner, and F. Sinangil. 1998. Vaccine protection against a heterologous, non-syncytium-inducing. primary human immunodeficiency virus. J. Virol. 72:10275-111280.
49. Robinson, H. L., D. C. Monteftori, R. P. Johnson, K. H. Manson, M. L. Kalish, J. D. Lifson, T. A. Rizvi, S. Lu, S. L. Hu, G. P. Mazzara, D. L. Panicali, J. G. Herndon, R. Glickman, M. A. Candido, S. L. Lydy, M. S. Wyand, and H. M. McClure. 1999. Neutralizing antibody-independent containment of immunodeficiency virus challenges by DNA priming and recombinant pox virus booster immunization. Nat. Med. 5:526-534.
50. Seth, A., I. Ourmanov, M. Kuroda, J. E. Schmitz, M. W. Carroll, L. S. Wyatt, B. Moss, M. A. Forman, V. M. Hirsch, and N. L. Letvin. 1998. Recombinant modified vaccinia virus Ankara-simian immunodeficiency virus gag pol elicits cytotoxic T lymphocytes in rhesus monkeys detected by major histocompatibility complex class 1/peptide tetramer. Proc. Natl. Acad. Sci. USA 95: 10112-10116.
51. Shibata, R., F. Maldarelli, C. Siemon, T. Matano, M. Parta, G. Miller, T. Fredrickson, and M. A. Martin. 1997. Infection and pathogenicity of chimeric simian-human immunodeficiency viruses in macaques: determinants of high virus loads and CD4 cell killing. J. Infect. Dis. 176:362-373.
52. Staprans, S. I., P. J. Dailey, A. Rosenthal, C. Horton, R. M. Grant, N. Lerche, and M. B. Feinberg. 1999. Simian immunodeficiency virus disease course is predicted by the extent of virus replication during primary infection. J. Virol. 73:4829-4839.
53. Suryanarayana, K., T. A. Wiltrout, G. M. Vasques, V. M. Hirsch, and J. D. Lifson. 1998. Plasma SIV RNA viral load determination by real-time quantification of product generation in reverse transcriptase-polymerase chain reaction. AIDS Res. Hum. Retroviruses 14:183-189.
54. Sutter, G., and B. Moss. 1992. Nonreplicating vaccinia vector efficiently express recombinant genes. Proc. Natl. Acad. Sci. USA 89:10847-10851.
55. Watson, A., J. Ranchalis, B. Travis, J. McClure, W. Sutton, P. R. Johnson, S. L. Hu, and N. L. Haigwood. 1997. Plasma viremia in macaques infected with simian immunodeficiency virus: plasma viral load early in infection predicts survival. J. Virol. 71:284-290.