CD8+ lymphocytes do not mediate protection against acute superinfection 20 days after vaccination with a live attenuated simian immunodeficiency virus

Journal of Virology

Volumn 79, Issue 19, 2005, Pages 12264-12272

  Stebbings, Richard ^a   Berry, Neil ^a   Waldmann, Herman ^b   Bird, Pru ^c   Hale, Geoff ^c   Stott, Jim ^a   North, David ^a   Hull, Robin ^a   Hall, Joanna ^a   Lines, Jenny ^a   Brown, Stuart ^a   D'Arcy, Nikki ^a,d   Davis, Leanne ^a   Elsley, William ^a   Edwards, Cherry ^a   Ferguson, Deborah ^a   Allen, Jane ^a   Almond, Neil ^a  

^a NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LIVE VACCINE; OKT 8; VIRUS RNA; VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; IMMUNITY; INOCULATION; LYMPHOID TISSUE; NONHUMAN; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; SUPERINFECTION; VACCINATION; VIREMIA; VIRUS IMMUNITY; VIRUS LOAD;

ANIMALS; ANTIBODIES, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; MACACA FASCICULARIS; RNA, VIRAL; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; SUPERINFECTION; TIME FACTORS; VACCINES, ATTENUATED; VIRAL LOAD; VIREMIA;

SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 25144442232     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.19.12264-12272.2005     Document Type: Article

References (59)

1. Abdel-Motal, U. M., J. Gillis, K. Manson, M. Wyand, D. Montefiori, K. Stefano-Cole, R. C. Montelaro, J. D. Altman, and R. P. Johnson. 2005. Kinetics of expansion of SIV Gag-specific CD8+ T lymphocytes following challenge of vaccinated macaques. Virology 333:226-238.
2. Abel, K., L. Compton, T. Rourke, D. Montefiori, D. Lu, K. Rothaeusler, L. Fritts, K. Bost, and C. J. Miller. 2003. Simian-human immunodeficiency virus SHIV89.6-induced protection against intravaginal challenge with pathogenic SIVmac239 is independent of the route of immunization and is associated with a combination of cytotoxic T-lymphocyte and alpha interferon responses. J. Virol. 77:3099-3118.
3. Almond, N., K. Kent, M. Cranage, E. Rud, B. Clarke, and E. J. Stott. 1995. Protection by attenuated simian immunodeficiency virus in macaques against challenge with virus-infected cells. Lancet 345:1342-1344.
4. Almond, N., M. Page, K. Mills, A. Jenkins, C. Ling, R. Thorpe, P. Kitchin, and M. Williams. 1990. The production and purification of PCR-derived recombinant simian immunodeficiency virus p27 gag protein; its use in detecting serological and T-cell responses in macaques. J. Virol. Methods 28:305-319.
5. Almond, N., J. Rose, R. Sangster, P. Silvera, R. Stebbings, B. Walker, and E. J. Stott. 1997. Mechanisms of protection induced by attenuated simian immunodeficiency virus. I. Protection cannot be transferred with immune serum. J. Gen. Virol. 78:1919-1922.
6. Baba, T. W., Y. S. Jeong, D. Pennick, R. Bronson, M. F. Greene, and R. M. Ruprecht. 1995. Pathogenicity of live, attenuated SIV after mucosal infection of neonatal macaques. Science 267:1820-1825.
7. Bogers, W. M., H. Niphuis, P. ten Haaft, J. D. Laman, W. Koornstra, and J. L. Heeney. 1995. Protection from HIV-1 envelope-bearing chimeric simian immunodeficiency virus (SHIV) in rhesus macaques infected with attenuated SIV: consequences of challenge. AIDS 9:F13-F8.
8. Clarke, S., N. Almond, and N. Berry. 2003. Simian immunodeficiency virus Nef gene regulates the production of 2-LTR circles in vivo. Virology 306: 100-108.
9. Connor, R. I., D. C. Montefiori, J. M. Binley, J. P. Moore, S. Bonhoeffer, A. Gettie, E. A. Fenamore, K. E. Sheridan, D. D. Ho, P. J. Dailey, and P. A. Marx. 1998. Temporal analyses of virus replication, immune responses, and efficacy in rhesus macaques immunized with a live, attenuated simian immunodeficiency virus vaccine. J. Virol. 72:7501-7509.
10. Cooper, M. A., T. A. Fehniger, and M. A. Caligiuri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22:633-640.
11. Cranage, M. P., S. A. Sharpe, A. M. Whatmore, N. Polyanskaya, S. Norley, N. Cook, S. Leech, M. J. Dennis, and G. A. Hall. 1998. In vivo resistance to simian immunodeficiency virus superinfection depends on attenuated virus dose. J Gen. Virol. 79:1935-1944.
12. Cranage, M. P., A. M. Whatmore, S. A. Sharpe, N. Cook, N. Polyanskaya, S. Leech, J. D. Smith, E. W. Rud, M. J. Dennis, and G. A. Hall. 1997. Macaques infected with live attenuated SIVmac are protected against superinfection via the rectal mucosa. Virology 229:143-154.
13. Daniel, M. D., F. Kirchhoff, S. C. Czajak, P. K. Sehgal, and R. C. Desrosiers. 1992. Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science 258:1938-1941.
14. Desrosiers, R. C. 1990. The simian immunodeficiency viruses. Annu. Rev. Immunol. 8:557-578.
15. Dittmer, U., and K. J. Hasenkrug. 1999. Alternative interpretation of lymphocyte depletion studies using monoclonal antibodies in animals previously vaccinated with attenuated retroviral vaccines. AIDS Res. Hum. Retrovir. 15:785.
16. Dittmer, U., T. Nisslein, W. Bodemer, H. Petry, U. Sauermann, C. Stahl-Hennig, and G. Hunsmann. 1995. Cellular immune response of rhesus monkeys infected with a partially attenuated nef deletion mutant of the simian immunodeficiency virus. Virology 212:392-397.
17. Doherty, P. C., and J. P. Christensen. 2000. Accessing complexity: the dynamics of virus-specific T cell responses. Annu. Rev. Immunol. 18:561-592.
18. Dunn, C. S., B. Hurtrel, C. Beyer, L. Gloeckler, T. N. Ledger, C. Moog, M. P. Kieny, M. Mehtali, D. Schmitt, J. P. Gut, A. Kirn, and A. M. Aubertin. 1997. Protection of SIVmac-infected macaque monkeys against superinfection by a simian immunodeficiency virus expressing envelope glycoproteins of HIV type 1. AIDS Res. Hum. Retrovir. 13:913-922.
19. Flynn, K. J., J. M. Riberdy, J. P. Christensen, J. D. Altman, and P. C. Doherty. 1999. In vivo proliferation of naive and memory influenza-specific CD8(+) T cells. Proc. Natl. Acad. Sci. USA 96:8597-8602.
20. Gallimore, A., M. Cranage, N. Cook, N. Almond, J. Bootman, E. Rud, P. Silvera, M. Dennis, T. Corcoran, J. Stott, and et al. 1995. Early suppression of SIV replication by CD8+ nef-specific cytotoxic T cells in vaccinated macaques. Nat. Med. 1:1167-1173.
21. Haigwood, N. L., A. Watson, W. F. Sutton, J. McClure, A. Lewis, J. Ranchalis, B. Travis, G. Voss, N. L. Letvin, S. L. Hu, V. M. Hirsch, and P. R. Johnson. 1996. Passive immune globulin therapy in the SIV/macaque model: early intervention can alter disease profile. Immunol. Lett. 51:107-114.
22. Hofmann-Lehmann, R., J. Vlasak, A. L. Williams, A. L. Chenine, H. M. McClure, D. C. Anderson, S. O'Neil, and R. M. Ruprecht. 2003. Live attenuated, nef-deleted SIV is pathogenic in most adult macaques after prolonged observation. AIDS 17:157-166.
23. Jin, X., D. E. Bauer, S. E. Tuttleton, S. Lewin, A. Gettie, J. Blanchard, C. E. Irwin, J. T. Safrit, J. Mittler, L. Weinberger, L. G. Kostrikis, L. Zhang, A. S. Perelson, and D. D. Ho. 1999. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 189:991-998.
24. Johnson, R. P. 2002. Mechanisms of protection against simian immunodeficiency virus infection. Vaccine 20:1985-1987.
25. Johnson, R. P., R. L. Glickman, J. Q. Yang, A. Kaur, J. T. Dion, M. J. Mulligan, and R. C. Desrosiers. 1997. Induction of vigorous cytotoxic T-lymphocyte responses by live attenuated simian immunodeficiency virus. J. Virol. 71:7711-7718.
26. Johnson, R. P., J. D. Lifson, S. C. Czajak, K. S. Cole, K. H. Manson, R. Glickman, J. Yang, D. C. Montefiori, R. Montelaro, M. S. Wyand, and R. C. Desrosiers. 1999. Highly attenuated vaccine strains of simian immunodeficiency virus protect against vaginal challenge: inverse relationship of degree of protection with level of attenuation. J. Virol. 73:4952-4961.
27. Kent, K. A., P. Kitchin, K. H. Mills, M. Page, F. Taffs, T. Corcoran, P. Silvera, B. Flanagan, C. Powell, J. Rose, et al. 1994. Passive immunization of cynomolgus macaques with immune sera or a pool of neutralizing monoclonal antibodies failed to protect against challenge with SIVmac251. AIDS Res. Hum. Retrovir. 10:189-194.
28. + lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J. Virol. 75:10187-10199.
29. Lohman, B. L., M. B. McChesney, C. J. Miller, E. McGowan, S. M. Joye, K. K. Van Rompay, E. Reay, L. Antipa, N. C. Pedersen, and M. L. Marthas. 1994. A partially attenuated simian immunodeficiency virus induces host immunity that correlates with resistance to pathogenic virus challenge. J. Virol. 68:7021-7029.
30. Metzner, K. J., X. Jin, F. V. Lee, A. Gettie, D. E. Bauer, M. Di Mascio, A. S. Perelson, P. A. Marx, D. D. Ho, L. G. Kostrikis, and R. I. Connor. 2000. Effects of in vivo CD8(+) T cell depletion on virus replication in rhesus macaques immunized with a live, attenuated simian immunodeficiency virus vaccine. J. Exp. Med. 191:1921-1931.
31. Nilsson, C., B. Makitalo, R. Thorstensson, S. Norley, D. Binninger-Schinzel, M. Cranage, E. Rud, G. Biberfeld, and P. Putkonen. 1998. Live attenuated simian immunodeficiency virus (SIV)mac in macaques can induce protection against mucosal infection with SIVsm. AIDS 12:2261-2270.
32. Nixon, D. F., S. M. Donahoe, W. M. Kakimoto, R. V. Samuel, K. J. Metzner, A. Gettie, T. Hanke, P. A. Marx, and R. I. Connor. 2000. Simian immunodeficiency virus-specific cytotoxic T lymphocytes and protection against challenge in rhesus macaques immunized with a live attenuated simian immunodeficiency virus vaccine. Virology 266:203-210.
33. Putkonen, P., B. Makitalo, D. Bottiger, G. Biberfeld, and R. Thorstensson. 1997. Protection of human immunodeficiency virus type 2-exposed seronegative macaques from mucosal simian immunodeficiency virus transmission. J. Virol. 71:4981-4984.
34. Robertson, M. J., and J. Ritz. 1990. Biology and clinical relevance of human natural killer cells. Blood 76:2421-2438.
35. Rose, J., P. Silvera, B. Flanagan, P. Kitchin, and N. Almond. 1995. The development of PCR based assays for the detection and differentiation of simian immunodeficiency virus in vivo. J. Virol. Methods 51:229-239.
36. Rud, E. W., M. Cranage, J. Yon, J. Quirk, L. Ogilvie, N. Cook, S. Webster, M. Dennis, and B. E. Clarke. 1994. Molecular and biological characterization of simian immunodeficiency virus macaque strain 32H proviral clones containing nef size variants. J. Gen. Virol. 75:529-543.
37. Rud, E. W., L. Ogilvie, B. E. Clarke, N. Almond, K. Kent, L. Chan, M. Page, P. Kitchin, E. J. Stott, N. Cook, S. Sharpe, T. Ashwork, M. Dennis, G. Hall, and M. Cranage. 1994. A naturally attenuated SIVmac32H vaccine or viral interference? p. 217-223. In F. Brown, R. M. Chanock, H. S. Ginsberg, and E. Norrby (ed.), Vaccines 94: modern approaches to new vaccines including prevention of AIDS. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
38. Ruprecht, R. M. 1999. Live attenuated AIDS viruses as vaccines: promise or peril? Immunol. Rev. 170:135-149.
39. Sawai, E. T., M. S. Hamza, M. Ye, K. E. Shaw, and P. A. Luciw. 2000. Pathogenic conversion of live attenuated simian immunodeficiency virus vaccines is associated with expression of truncated Nef. J. Virol. 74:2038-2045.
40. + lymphocyte depletion on virus containment after simian immunodeficiency virus SIVmac251 challenge of live attenuated SIVmac239Δ3-vaccinated rhesus macaques. J. Virol. 79:8131-8141.
41. Schmitz, J. E., M. J. Kuroda, S. Santra, V. G. Sasseville, M. A. Simon, M. A. Lifton, P. Racz, K. Tenner-Racz, M. Dalesandro, B. J. Scallon, J. Ghrayeb, M. A. Forman, D. C. Montefiori, E. P. Rieber, N. L. Letvin, and K. A. Reimann. 1999. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283:857-860.
42. Schmitz, J. E., M. J. Kuroda, S. Santra, M. A. Simon, M. A. Lifton, W. Lin, R. Khunkhun, M. Piatak, J. D. Lifson, G. Grosschupff, R. S. Gelman, P. Racz, K. Tenner-Racz, K. A. Mansfield, N. L. Letvin, D. C. Montefiori, and K. A. Reimann. 2003. Effect of humoral immune responses on controlling viremia during primary infection of rhesus monkeys with simian immunodeficiency virus. J. Virol. 77:2165-2173.
43. Schmitz, J. E., M. A. Simon, M. J. Kuroda, M. A. Lifton, M. W. Ollert, C. W. Vogel, P. Racz, K. Tenner-Racz, B. J. Scallon, M. Dalesandro, J. Ghrayeb, E. P. Rieber, V. G. Sasseville, and K. A. Reimann. 1999. A nonhuman primate model for the selective elimination of CD8+ lymphocytes using a mouse-human chimeric monoclonal antibody. Am. J. Pathol. 154:1923-1932.
44. Sharpe, S. A., A. Cope, S. Dowall, N. Berry, C. Ham, J. L. Heeney, D. Hopkins, L. Easlerbrook, M. Dennis, N. Almond, and M. Cranage. 2004. Macaques infected long-term with attenuated simian immunodeficiency virus (SIVmac) remain resistant to wild-type challenge, despite declining cytotoxic T lymphocyte responses to an immunodominant epitope. J. Gen. Virol. 85:2591-2602.
45. Sharpe, S. A., A. M. Whatmore, G. A. Hall, and M. P. Cranage. 1997. Macaques infected with attenuated simian immunodeficiency virus resist superinfection with virulence-revertant virus. J. Gen. Virol. 78:1923-1927.
46. Shibata, R., C. Siemon, S. C. Czajak, R. C. Desrosiers, and M. A. Martin. 1997. Live, attenuated simian immunodeficiency virus vaccines elicit potent resistance against a challenge with a human immunodeficiency virus type 1 chimeric virus. J. Virol. 71:8141-8148.
47. Silvera, P., B. Flanagan, K. Kent, E. Rud, C. Powell, T. Corcoran, C. Bruck, C. Thiriart, N. L. Haigwood, and E. J. Stott. 1994. Fine analysis of humoral antibody response to envelope glycoprotein of SIV in infected and vaccinated macaques. AIDS Res. Hum. Retrovir. 10:1295-1304.
48. Silvera, P., A. Wade-Evans, E. Rud, R. Hull, K. Silvera, R. Sangster, N. Almond, and J. Stott. 2001. Mechanisms of protection induced by live attenuated simian immunodeficiency virus. III. Viral interference and the role of CD8+ T-cells and beta-chemokines in the inhibition of virus infection of PBMCs in vitro. J. Med. Primatol. 30:1-13.
49. Stahl-Hennig, C., U. Dittmer, T. Nisslein, H. Petry, E. Jurkiewicz, D. Fuchs, H. Wachter, K. Matz-Rensing, E. M. Kuhn, F. J. Kaup, E. W. Rud, and G. Hunsmann. 1996. Rapid development of vaccine protection in macaques by live-attenuated simian immunodeficiency virus. J. Gen. Virol. 77:2969-2981.
50. Stebbings, R., N. M. Almond, E. J. Stott, N. Berry, A. M. Wade-Evans, R. Hull, J. Lines, P. Silvera, R. Sangster, T. Corcoran, J. Rose, and K. B. Walker. 2002. Mechanisms of protection induced by attenuated simian immunodeficiency virus. V. No evidence for lymphocyte-regulated cytokine responses upon rechallenge. Virology 296:338-353.
51. Stebbings, R., N. Berry, J. Stott, R. Hull, B. Walker, J. Lines, W. Elsley, S. Brown, A. Wade-Evans, G. Davis, J. Cowie, M. Sethi, and N. Almond. 2004. Vaccination with live attenuated simian immunodeficiency virus for 21 days protects against superinfection. Virology 330:249-260.
52. Stebbings, R., J. Stott, N. Almond, R. Hull, J. Lines, P. Silvera, R. Sangster, T. Corcoran, J. Rose, S. Cobbold, F. Gotch, A. McMichael, and B. Walker. 1998. Mechanisms of protection induced by attenuated simian immunodeficiency virus. II. Lymphocyte depletion does not abrogate protection. AIDS Res. Hum. Retrovir. 14:1187-1198.
53. Stott, E. J., W. L. Chan, K. H. Mills, M. Page, F. Taffs, M. Cranage, P. Greenaway, and P. Kitchin. 1990. Preliminary report: protection of cynomolgus macaques against simian immunodeficiency virus by fixed infected-cell vaccine. Lancet 336:1538-1541.
54. Tenner-Racz, K., C. S. Hennig, K. Uberla, H. Stoiber, R. Ignatius, J. Heeney, R. M. Steinman, and P. Racz. 2004. Early protection against pathogenic virus infection at a mucosal challenge site after vaccination with attenuated simian immunodeficiency virus. Proc. Natl. Acad. Sci. USA 101:3017-3022.
55. Vogel, T. U., B. E. Beer, J. zur Megede, H. G. Ihlenfeldt, G. Jung, S. Holzammer, D. I. Watkins, J. D. Altman, R. Kurth, and S. Norley. 2002. Induction of anti-simian immunodeficiency virus cellular and humoral immune responses in rhesus macaques by peptide immunogens: correlation of CTL activity and reduction of cell-associated but not plasma virus load following challenge. J. Gen. Virol. 83:81-91.
56. Vogel, T. U., J. Fournier, A. Sherring, D. Ko, M. Parenteau, D. Bogdanovic, J. Mihowich, and E. W. Rud. 1998. Presence of circulating CTL induced by infection with wild-type or attenuated SIV and their correlation with protection from pathogenic SHIV challenge. J. Med. Primatol. 27:65-72.
57. Whatmore, A. M., N. Cook, G. A. Hall, S. Sharpe, E. W. Rud, and M. P. Cranage. 1995. Repair and evolution of nef in vivo modulates simian immunodeficiency virus virulence. J. Virol. 69:5117-5123.
58. Wyand, M. S., K. Manson, D. C. Montefiori, J. D. Lifson, R. P. Johnson, and R. C. Desrosiers. 1999. Protection by live, attenuated simian immunodeficiency virus against heterologous challenge. J. Virol. 73:8356-8363.
59. Wyand, M. S., K. H. Manson, M. Garcia-Moll, D. Montefiori, and R. C. Desrosiers. 1996. Vaccine protection by a triple deletion mutant of simian immunodeficiency virus. J. Virol. 70:3724-3733.