Replication, immunogenicity, and protective properties of live-attenuated simian immunodeficiency viruses expressing interleukin-4 or interferon-γ

Virology

Volumn 305, Issue 2, 2003, Pages 473-485

  Stahl Hennig, Christiane ^a   Gundlach, Björn R ^b   Dittmer, Ulf ^a,c   Ten Haaft, Peter ^d   Heeney, Jonathan ^d   Zou, Weiping ^e   Emilie, Dominique ^e   Sopper, Sieghart ^c   Überla, Klaus ^f  

^a GERMAN PRIMATE CENTER   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^e INSERM   (France)

^f RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Cytokines; HIV; Vaccine

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 4; MESSENGER RNA; NEF PROTEIN; NEUTRALIZING ANTIBODY; PERFORIN; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY AFFINITY; ANTIBODY TITER; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; GENE DELETION; IMMUNE RESPONSE; IN VIVO STUDY; LYMPH NODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; SPECIES COMPARISON; TH2 CELL; VIREMIA; VIRUS CHARACTERIZATION; VIRUS GENE; VIRUS HYBRID; VIRUS LOAD; VIRUS MUTANT; VIRUS REPLICATION;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; MACACA MULATTA; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 0037455552     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.2002.1763     Document Type: Article

References (62)

1. Baba T. W., Jeong Y. S., Pennick D., Bronson R., Greene M. F., Ruprecht R. M. Pathogenicity of live, attenuated SIV after mucosal infection of neonatal macaques. Science. 267:1995;1820-1825.
2. Baba T. W., Liska V., Khimani A. H., Ray N. B., Dailey P. J., Penninck D., Bronson R., Greene M. F., McClure H. M., Martin L. N., Ruprecht R. M. Live attenuated, multiply deleted simian immunodeficiency virus causes AIDS in infant and adult macaques. Nat. Med. 5:1999;194-203.
3. Blatt S. P., McCarthy W. F., Bucko Krasnicka B., Melcher G. P., Boswell R. N., Dolan J., Freeman T. M., Rusnak J. M., Hensley R. E., Ward W. W., Barnes D., Hendrix C. W. Multivariate models for predicting progression to AIDS and survival in human immunodeficiency virus-infected persons. J. Infect. Dis. 171:1995;837-844.
4. Bogers W. M., Niphuis H., ten Haaft P., Laman J. D., Koornstra W., Heeney J. L. Protection from HIV-1 envelope-bearing chimeric simian immunodeficiency virus (SHIV) in rhesus macaques infected with attenuated SIV: Consequences of challenge. AIDS. 9:1995;13-18.
5. Boyer J. D., Nath B., Schumann K., Curley E., Manson K., Kim J., Weiner D. B. IL-4 increases Simian immunodeficiency virus replication despite enhanced SIV immune responses in infected rhesus macaques. Int. J. Parasitol. 32:2002;543-550.
6. Buch S., Pinson D., King C. L., Raghavan R., Hou Y., Li Z., Adany I., Hicks A., Villinger F., Kumar A., Narayan O. Inhibitory and enhancing effects of IFN-gamma and IL-4 on SHIV(KU) replication in rhesus macaque macrophages: Correlation between Th2 cytokines and productive infection in tissue macrophages during late-stage infection. Cytokine. 13:2001;295-304.
7. Cole K. S., Rowles J. L., Jagerski B. A., Murphey-Corb M., Unangst T., Clements J. E., Robinson J., Wyand M. S., Desrosiers R. C., Montelaro R. C. Evolution of envelope-specific antibody responses in monkeys experimentally infected or immunized with simian immunodeficiency virus and its association with the development of protective immunity. J. Virol. 71:1997;5069-5079.
8. Desrosiers R. C. Live attenuated vaccines: Best hope to prevent HIV? HIV Adv. Res. Ther. 3:1996;3-9.
9. Dittmer U., Nisslein T., Bodemer W., Petry H., Sauermann U., Stahl Hennig C., Hunsmann G. Cellular immune response of rhesus monkeys infected with a partially attenuated nef deletion mutant of the simian immunodeficiency virus. Virology. 212:1995;392-397.
10. Dolan M. J., Clerici M., Blatt S. P., Hendrix C. W., Melcher G. P., Boswell R. N., Freeman T. M., Ward W., Hensley R., Shearer G. M. In vitro T cell function, delayed-type hypersensitivity skin testing, and CD4+ T cell subset phenotyping independently predict survival time in patients infected with human immunodeficiency virus. J. Infect. Dis. 172:1995;79-87.
11. Dunn C. S., Hurtel B., Beyer C., Gloecker L., Ledger T. N., Moog C., Kieny M. P., Methali M., Schmitt D., Gut J. P., Kirn A., Aubertin A. M. Protection of SIVmac-infected macaque monkeys against superinfection by a simian immunodeficiency virus expressing envelope glycoproteins of HIV type 1. AIDS Res. Hum. Retroviruses. 13:1997;913-922.
12. Emilie D., Maillot M. C., Nicolas J. F., Fior R., Galanaud P. Antagonistic effect of interferon-gamma on tat-induced transactivation of HIV long terminal repeat. J. Biol. Chem. 267:1992;20565-20570.
13. Galli G., Annunziato F., Mavilia C., Romagnani P., Cosmi L., Manetti R., Pupilli C., Maggi E., Romagnani S. Enhanced HIV expression during Th2-oriented responses explained by the opposite regulatory effect of IL-4 and IFN-gamma of fusin/CXCR4. Eur. J. Immunol. 28:1998;3280-3290.
14. Gauduin M. C., Glickman R. L., Ahmad S., Yilma T., Johnson R. P. Immunization with live attenuated simian immunodeficiency virus induces strong type 1 T helper responses and beta-chemokine production. Proc. Natl. Acad. Sci. USA. 96:1999;14031-14036.
15. Gauduin M. C., Glickman R. L., Means R., Johnson R. P. Inhibition of simian immunodeficiency virus (SIV) replication by CD8(+) T lymphocytes from macaques immunized with live attenuated SIV. J. Virol. 72:1998;6315-6324.
16. Giavedoni L., Ahmad S., Jones L., Yilma T. Expression of gamma interferon by simian immunodeficiency virus increases attenuation and reduces postchallenge virus load in vaccinated rhesus macaques. J. Virol. 71:1997;866-872.
17. Giavedoni L. D., Yilma T. Construction and characterization of replication-competent simian immunodeficiency virus vectors that express gamma interferon. J. Virol. 70:1996;2247-2251.
18. Gundlach B. R., Lewis M. G., Sopper S., Schnell T., Sodroski J., Stahl-Hennig C., Überla K. Evidence for recombination of live, attenuated immunodeficiency virus vaccine with challenge virus to a more virulent strain. J. Virol. 74:2000;3537-3542.
19. Gundlach B. R., Linhart H., Dittmer U., Sopper S., Reiprich S., Fuchs D., Fleckenstein B., Hunsmann G., Stahl-Hennig C., Überla K. Construction, replication, and immunogenic properties of a simian immunodeficiency virus expressing interleukin 2. J. Virol. 71:1997;2225-2232.
20. Gundlach B. R., Reiprich S., Sopper S., Means R. E., Dittmer U., Matz-Rensing K., Stahl-Hennig C., Überla K. Env-independent protection induced by live, attenuated simian immunodeficiency virus vaccines. J. Virol. 72:1998;7846-7851.
21. Hariharan D., Douglas S. D., Lee B., Lai J. P., Campbell D. E., Ho W. Z. Interferon-gamma upregulates CCR5 expression in cord and adult blood mononuclear phagocytes. Blood. 93:1999;1137-1144.
22. Hoch J., Lang S. M., Weeger M., Stahl Hennig C., Coulibaly C., Dittmer U., Hunsmann G., Fuchs D., Müller J., Sopper S., Fleckenstein B., Überla K. vpr deletion mutant of simian immunodeficiency virus induces AIDS in rhesus monkeys. J. Virol. 69:1995;4807-4813.
23. Jackson R. J., Ramsay A. J., Christensen C. D., Beaton S., Hall D. F., Ramshaw I. A. Expression of mouse interleukin-4 by a recombinant ectromelia virus suppresses cytolytic lymphocyte responses and overcomes genetic resistance to mousepox. J. Virol. 75:2001;1205-1210.
24. Johnson R. P. Live attenuated AIDS vaccines: Hazards and hopes. Nat. Med. 5:1999;154-155.
25. Johnson R. P., Glickman R. L., Yang J. Q., Kaur A., Dion J. T., Mulligan M. J., Desrosiers R. C. Induction of vigorous cytotoxic T-lymphocyte responses by live attenuated simian immunodeficiency virus. J. Virol. 71:1997;7711-7718.
26. Johnson R. P., Lifson J. D., Czajak S. C., Cole K. S., Manson K. H., Glickman R., Yang J., Montefiori D. C., Montelaro R., Wyand M. S., Desrosiers R. C. Highly attenuated vaccine strains of simian immunodeficiency virus protect against vaginal challenge: Inverse relationship of degree of protection with level of attenuation. J. Virol. 73:1999;4952-4961.
27. Johnson V., Byington R. E. Quantitative assays for virus infectivity. Aldovini A., Walker B. D. Techniques in HIV Research. 1990;71-76 Stockton Press, New York.
28. Kinzer C. A., Keegan A. D., Beckmann M. P., Widmer M., Idelson G. H., Ben-Sasson S. Z., Paul W. E. CT.h4S cells, a murine cell line expressing human IL-4 receptors and capable of assaying human IL-4. FASEB J. 8:1994;A506.
29. Kneitz C., Kerkau T., Müller J., Coulibaly C., Stahl-Hennig C., Hunsmann G., Hünig T., Schimpl A. Early phenotypic and functional alterations in lymphocytes from simian immunodeficiency virus infected macaques. Vet. Immunol. Immunopathol. 36:1993;239-255.
30. Kornbluth R. S., Oh P. S., Munis J. R., Cleveland P. H., Richman D. D. Interferons and bacterial lipopolysaccharide protect macrophages from productive infection by human immunodeficiency virus in vitro. J. Exp. Med. 169:1989;1137-1151.
31. Koyanagi Y., O'Brien W. A., Zhao J. Q., Golde D. W., Gasson J. C., Chen I. S. Cytokines alter production of HIV-1 from primary mononuclear phagocytes. Science. 241:1988;1673-1675.
32. Lewis M. G., Bellah S., McKinnon K., Yalley-Ogunro J., Zack P. M., Elkins W. R., Desrosiers R. C., Eddy G. A. Titration and characterization of two rhesus derived SIVmac challenge stocks. AIDS Res. Hum. Retroviruses. 10:1994;213-220.
33. Lewis M. G., Yalley-Ogunro J., Greenhouse J. J., Brennan T. P., Jiang J. B., VanCott T. C., Lu Y., Eddy G. A., Birx D. L. Limited protection from a pathogenic chimeric simian-human immunodeficiency virus challenge following immunization with attenuated simian immunodeficiency virus. J. Virol. 73:1999;1262-1270.
34. Lohman B. L., McChesney M. B., Miller C. J., McGowan E., Joye S. M., Van Rompay K. K., Reay E., Antipa L., Pedersen N. C., Marthas M. L. A partially attenuated simian immunodeficiency virus induces host immunity that correlates with resistance to pathogenic virus challenge. J. Virol. 68:1994;7021-7029.
35. Matsuyama T., Kobayashi N., Yamamoto N. Cytokines and HIV infection: Is AIDS a tumor necrosis factor disease? AIDS. 5:1991;1405-1417.
36. Miller C. J., McChesney M. B., Lu X., Dailey P. J., Chutkowski C., Lu D., Brosio P., Roberts B., Lu Y. Rhesus macaques previously infected with simian/human immunodeficiency virus are protected from vaginal challenge with pathogenic SIVmac239. J. Virol. 71:1997;1911-1921.
37. Morphey-Corb M., Martin L. N., Davison-Fairburn B., Montelaro R. C., Miller M., West M., Ohkawa S., Baskin G., Zhang J.-Y., Putney S. D., Allison A. C., Eppstein D. A. A formalin-inactivated whole SIV vaccine confers protection in macaques. Science. 246:1989;1293-1297.
38. Naif H. M., Li S., Ho-Shon M., Mathijs J. M., Williamson P., Cunningham A. L. The state of maturation of monocytes into macrophages determines the effects of IL-4 and IL-13 on HIV replication. J. Immunol. 158:1997;501-511.
39. Pantaleo G. How immune-based interventions can change HIV therapy. Nat. Med. 3:1997;483-486.
40. Poli G., Fauci A. S. Cytokine modulation of HIV expression. Semin. Immunol. 5:1993;165-173.
41. Potts B. J. Mini reverse transcriptase (RT) assay. Aldovini A., Walker B. D. Techniques in HIV Research. 1990;103-106 Stockton Press, New York.
42. sm challenge in macaques infected with a chimeric SIV that expresses HIV type 1 envelope. AIDS Res. Hum. Retroviruses. 12:1996;993-999.
43. Reimann K. A., Li J. T., Veazey R., Halloran M., Park I. W., Karlsson G. B., Sodroski J., Letvin N. L. A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J. Virol. 70:1996a;6922-6928.
44. Reimann K. A., Li J. T., Voss G., Lekutis C., Tenner-Racz K., Racz P., Lin W., Montefiori D. C., Lee-Paritz D. E., Collman R., Sodroski J., Letvin N. L. An env gene derived from a primary HIV-1 isolate confers high in vivo replicative capacity to a chimeric simian/human immunodeficiency virus in rhesus monkeys. J. Virol. 70:1996b;3198-3206.
45. Schmitz J. E., Kuroda M. J., Santra S., Sasseville V. G., Simon M. A., Lifton M. A., Racz P., Tenner-Racz K., Dalesandro M., Scallon B. J., Ghrayeb J., Forman M. A., Montefiori D. C., Rieber E. P., Letvin N. L., Reimann K. A. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science. 283:1999;857-860.
46. Schuitemaker H., Kootstra N. A., Koppelman M. H., Bruisten S. M., Huisman H. G., Tersmette M., Miedema F. Proliferation-dependent HIV-1 infection of monocytes occurs during differentiation into macrophages. J. Clin. Invest. 89:1992;1154-1160.
47. Shibata R., Siemon C., Czajak S. C., Desrosiers R. C., Martin M. A. Live, attenuated simian immunodeficiency virus vaccines elicit potent resistance against a challenge with a human immunodeficiency virus type 1 chimeric virus. J. Virol. 71:1997;8141-8148.
48. Sopper S., Sauer U., Hemm S., Demuth M., Müller J., Stahl-Hennig C., Hunsmann G., ter Meulen V., Dörries R. Protective role of the virus-specific immune response for development of severe neurologic signs in simian immunodeficiency virus-infected macaques. J. Virol. 72:1998;9940-9947.
49. Sopper S., Sauer U., Müller J. G., tahl-Hennig C., er Meulen V. Early activation and proliferation of T cells in simian immunodeficiency virus-infected rhesus monkeys. AIDS Res. Hum. Retroviruses. 16:2000;689-697.
50. Stahl-Hennig C., Herchenröder O., Nick S., Evers M., Stille-Siegener M., Jentsch K. D., Kirchhoff F., Tolle T., Gatesman T. J., Lüke W., Hunsmann G. Experimental infection of macaques with HIV-2ben, a novel HIV-2 isolate. AIDS. 4:1990;611-617.
51. Stahl-Hennig C., Voss G., Nick S., Petry H., Fuchs D., Wachter H., Coulibaly C., Lüke W., Hunsmann G. Immunization with tween-ether-treated SIV adsorbed onto aluminum hydroxide protects monkeys against experimental SIV infection. Virology. 186:1992;588-596.
52. ten Haaft P., Verstrepen B., Überla K., Rosenwirth B., Heeney J. A pathogenic threshold of virus load defined in simian immunodeficiency virus- or simian-human immunodeficiency virus-infected macaques. J. Virol. 72:1998;10281-10285.
53. Überla K., Stahl Hennig C., Böttiger D., Mätz-Rensing K., Kaup F. J., Li J., Haseltine W. A., Fleckenstein B., Hunsmann G., Öberg B., Sodroski J. Animal model for the therapy of acquired immunodeficiency syndrome with reverse transcriptase inhibitors. Proc. Natl. Acad. Sci. USA. 92:1995;8210-8214.
54. Valentin A., Lu W., Rosati M., Schneider R., Albert J., Karlsson A., Pavlakis G. N. Dual effect of interleukin 4 on HIV-1 expression: Implications for viral phenotypic switch and disease progression. Proc. Natl. Acad. Sci. USA. 95:1998;8886-8891.
55. Villinger F., Brar S. S., Mayne A., Chikkala N., Ansari A. A. Comparative sequence analysis of cytokine genes from human and nonhuman primates. J. Immunol. 155:1995;3946-3954.
56. Vyakarnam A., McKeating J., Meager A., Beverley P. C. Tumour necrosis factors (alpha, beta) induced by HIV-1 in peripheral blood mononuclear cells potentiate virus replication. AIDS. 4:1990;21-27.
57. Wang J., Harada A., Matsushita S., Matsumi S., Zhang Y., Shioda T., Nagai Y., Matsushima K. IL-4 and a glucocorticoid up-regulate CXCR4 expression on human CD4+ T lymphocytes and enhance HIV-1 replication. J. Leukoc. Biol. 64:1998;642-649.
58. Wei X., Ghosh S. K., Taylor M. E., Johnson V. A., Emini E. A., Deutsch P., Lifson J. D., Bonhoeffer S., Nowak M. A., Hahn B. H., Saag M. S., Shaw G. M. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 373:1995;117-122.
59. Wyand M. S., Manson K., Montefiori D. C., Lifson J. D., Johnson R. P., Desrosiers R. C. Protection by live, attenuated simian immunodeficiency virus against heterologous challenge. J. Virol. 73:1999;8356-8363.
60. Wyand M. S., Manson K. H., Garcia-Moll M., Montefiori D., Desrosiers R. C. Vaccine protection by a triple deletion mutant of simian immunodeficiency virus. J. Virol. 70:1996;3724-3733.
61. Wyand M. S., Manson K. H., Lackner A. A., Desrosiers R. C. Resistance of neonatal monkeys to live attenuated vaccine strains of simian immunodeficiency virus. Nat. Med. 3:1997;32-36.
62. Zou W., Lackner A. A., Simon M., Durand-Gasselin I., Galanaud P., Desrosiers R. C., Emilie D. Early cytokine and chemokine gene expression in lymph nodes of macaques infected with simian immunodeficiency virus is predictive of disease outcome and vaccine efficacy. J. Virol. 71:1997;1227-1236.