Advertisement

Immunologic Research

, Volume 36, Issue 1–3, pp 51–60 | Cite as

Dissecting the humoral immune response to simian immunodeficiency virus

Mechanisms of antibody-mediated virus neutralization
  • Jonathan D. Steckbeck
  • Kelly Stefano Cole
Article
  • 58 Downloads

Abstract

The ultimate goal of an AIDS vaccine is to elicit potent cellular and humoral immune responses that will result in broadly enduring protective immunity. During the past several years, we have focused on characterizing the quantitative and qualitative properties of the antibody response, principally working to define the mechanism(s) of antibody-mediated neutralization in vitro. We have utilized a panel of monoclonal antibodies generated from monkeys infected with attenuated SIV for more than 8 mo to dissect the early events of virus infection involved in antibody-mediated neutralization. Presented herein are highlights from our studies that have identified potential mechanisms by which antibodies neutralize SIV in vitro.

Key Words

Neutralization Antibody Surface plasmon resonance SIV envelope Vaccine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Desrosiers RC: The simian immunodeficiency viruses. Annu Rev Immunol 1990;8: 557–578.PubMedCrossRefGoogle Scholar
  2. 2.
    Geretti AM: Simian immunodeficiency virus as a model of human HIV disease. Rev Med Virol 1999;9: 57–67.PubMedCrossRefGoogle Scholar
  3. 3.
    Metzner KJ, Jin X, Lee FV, et al: 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 2000;191: 1921–1931.PubMedCrossRefGoogle Scholar
  4. 4.
    Schmitz JE, Kuroda MJ, Santra S, et al: Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 1999;283: 857–860.PubMedCrossRefGoogle Scholar
  5. 5.
    Gardner M, Rosenthal A, Jennings M, Yee J, Antipa L, Robinson E, Jr: Passive immunization of rhesus macaques against SIV infection and disase. AIDS Res Hum Retroviruses 1995;11: 843–854.PubMedGoogle Scholar
  6. 6.
    Clements JE, Montelaro RC, Zink MC, et al: Cross-protective immune responses induced in rhesus, macaques by immunization with attenuated macrophage-tropic simian immunodeficiency virus. J Virol 1995;69 2737–2744.PubMedGoogle Scholar
  7. 7.
    Haigwood NL, Watson A, Sutton WF, et al: Passive immune globulin therapy in the SIV/macaque model: early intervention can alter disease profile. Immunol Lett 1996;51: 107–114.PubMedCrossRefGoogle Scholar
  8. 8.
    Van Rompay KK, Berardi CJ, Dillard-Telm S, et al: Passive immunization of newborn rhesus macaques prevents oral simian immunodeficiency virus infection. J Infect Dis 1998;177: 1247–1259.PubMedGoogle Scholar
  9. 9.
    Mascola JR, Lewis MG, Stiegler G, et al: Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J Virol 1999;73:4009–4018.PubMedGoogle Scholar
  10. 10.
    Mascola JR, Stiegler G, Van Cott TC, et al: Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion, of neutralizing antibodies. Nat Med 2000;6: 207–210.PubMedCrossRefGoogle Scholar
  11. 11.
    Li A, Baba TW, Sodroski J., et al: Synergistic neutralization of a chimeric SIV/HIV type 1 virus with combinations of human anti-HIV type 1 envelope monoclonal antibodies or hyperimmune globulins. AIDS Res Hum Retroviruses 1997;13: 647–656.PubMedGoogle Scholar
  12. 12.
    Li A, Katinger H, Posner MR, et al: Synergistic, neutralization of simian-human immunodeficiency virus SHIV-vpu+ by triple and quadruple combinations of human monoclonal antibodies and high-titer anti-human immunodeficiency virus type 1 immunoglobulins. J Virol 1998;72: 3235–3240.PubMedGoogle Scholar
  13. 13.
    Shibata R, Igarashi T, Haigwood N, et al: Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat Med 1999;5: 204–210.PubMedCrossRefGoogle Scholar
  14. 14.
    Foresman L, Jia F, Li Z, et al: Neutralizing antibodies administered before, but not after, virulent SHIV prevent infection in macaques. AIDS Res Hum Retroviruses 1998;14: 1035–1043.PubMedGoogle Scholar
  15. 15.
    Baba TW, Liska V, Hofmann-Lehmann R, et al: Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat Med 2000;6:200–206.PubMedCrossRefGoogle Scholar
  16. 16.
    Cole KS, Rowles JL, Jagerski BA, et al: 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 1997;71: 5069–5079.PubMedGoogle Scholar
  17. 17.
    Van Rompay KK, Greenier JL, Cole KS, et al: Immunization of newborn rhesus macaques with simian immunodeficiency virus (SIV) vaccines prolongs survival after oral challenge with virulent SIVmac251. J Virol 2003;77: 179–190.PubMedCrossRefGoogle Scholar
  18. 18.
    Johnson RP, Lifson JD, Czajak SC, et al: Highly attenuated vaccine strains of simian immunodeficiency virus protect against vaginal challenge: inverse relationship of degree of protection with level of attenuation. J Virol 1999;73: 4952–4961.PubMedGoogle Scholar
  19. 19.
    Fuller DH, Simpson L, Cole KS, et al: Gene gun-based nucleic acid immunization alone or in combination with recombinant vaccinia vectors suppresses virus burden in rhesus macaques challenged with a heterologous SIV. Immunol Cell Biol 1997;75: 389–396.PubMedCrossRefGoogle Scholar
  20. 20.
    Hammond SA, Cook SJ, Lichtenstein DL, Issel CJ, Montelaro RC: Maturation of the cellular and humoral immune responses to persistent infection in horses by equine infectious anemia virus is a complex and lengthy process. J Virol 1997;71: 3840–3852.PubMedGoogle Scholar
  21. 21.
    Cole KS, Murphey-Corb M, Narayan O, Joag SV, Shaw GM, Montelaro RC, et al: Common themes of antibody maturation to simian immunodeficiency virus, simian-human immunodeficiency virus, and human immunodeficiency virus type 1 infections. J Virol 1998;72: 7852–7859.PubMedGoogle Scholar
  22. 22.
    Montelaro RC, Cole KS, Hammond SA: Maturation of immune responses to lentivirus infection: implications for AIDS vaccine development. AIDS Res Hum Retroviruses 1998;14 (Suppl 3): S255-S259.PubMedGoogle Scholar
  23. 23.
    Robinson JE, Cole KS, Elliott DH, et al: Production and characterization of SIV envelope-specific rhesus monoclonal antibodies from a macaque asymptomatically infected with a live, SIV vaccine. AIDS Res Hum Retroviruses 1998;14: 1253–1262.PubMedGoogle Scholar
  24. 24.
    Cole KS, Alvarez M, Elliott DH, et al: Characterization of neutralization epitopes of simian immunodeficiency virus (SIV) recognized by rhesus monoclonal antibodies derived from monkeys infected with an attenuated SIV strain. Virology 2001;290: 59–73.PubMedCrossRefGoogle Scholar
  25. 25.
    Choi WS, Collignon C, Thiriart C, et al: Effects of natural sequence variation, on recognition by monoclonal antibodies neutralize simian immunodeficiency virus infectivity. J Virol 1994;68: 5395–5402.PubMedGoogle Scholar
  26. 26.
    Steckbeck JD, Orlov I, Chow A, et al: Kinetic rates of antibody binding correlate with neutralization sensitivity of variant simian immunodeficiency virus strains. J Virol 2005;79: 12311–12320.PubMedCrossRefGoogle Scholar
  27. 27.
    Trkola A, Dragic T, Arthos J, et al: CD4-dependent, antibody-sensitive interactions between HIV-1 and its coreceptor CCR-5. Nature 1996;384: 184–187.PubMedCrossRefGoogle Scholar
  28. 28.
    Thali M, Olshevsky U, Furman C, Gabuzda D, Posner M. Sodroski J: Characterization of a discontinuous human immunodeficiency virus type 1 gp120 epitope recognized by a broadly reactive neutralizing human monoclonal antibody. J Virol 1991;65: 6188–6193.PubMedGoogle Scholar
  29. 29.
    Thali, M, Furman C, Ho DD, et al: Discontinuous, conserved neutralization epitopes overlapping the CD4-binding region of human immunodeficiency virus type 1 gp120 envelope glycoprotein. J Virol 1992;66: 5635–5641.PubMedGoogle Scholar
  30. 30.
    Thali M, Moore JP, Furman C, et al: Characterization of conserved human immunodeficiency virus type 1 gp120 neutralization epitopes exposed upon gp120-CD4 binding. J Virol 1993;67: 3978–3988.PubMedGoogle Scholar
  31. 31.
    Roben P, Moore JP, Thali M, Sodroski J, Barbas CF, 3rd, Burton DR: Recognition properties of panel of human recombinant Fab fragments to the CD4 binding site of gp120 that show differing abilities to neutralize human immunodeficiency virus type 1. J Virol 1994;68: 4821–4828.PubMedGoogle Scholar
  32. 32.
    Moore JP, Sattentau QJ, Wyatt R, Sodroski J: Probing the structure of the human immunodeficiency virus surface glycoprotein gp120 with a panel of monoclonal antibodies. J Virol 1994;68: 469–484.PubMedGoogle Scholar
  33. 33.
    Kent KA, Bjorling E: B-cell epitopes on the envelope glycoprotiens of SIV and HIV-2; in Korber BTM, Brander C, Moore JP, et al: (eds). HIV Molecular Immunology Database. Theoretical Biology and Biophysics, Los Alamos, NM, 1996, pp 5–21.Google Scholar
  34. 34.
    Babas T, Le Grand R, Dormont D, Bahraoui E: Production and characterization of monoclonal antibodies to simian immunodeficiency virus envelope glycoproteins. AIDS Res Hum Retroviruses 1997;13: 1109–1119.PubMedGoogle Scholar
  35. 35.
    Steckbeck JD, Grieser HJ, Sturgeon TJ, et al: Dynamic evolution of antibody populations in a rhesus macaque infected with attenuated simian immunodeficiency virus identified by surface plasmon resonance. J. Med. Primatol 2006;35: 248–260.PubMedCrossRefGoogle Scholar
  36. 36.
    Kestler H, Kodama T, Ringler D, et al: Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus. Science 1990;248: 1109–1112.PubMedCrossRefGoogle Scholar
  37. 37.
    Burns DP, Collignon C, Desrosiers RC: Simian immunodeficiency virus mutants resistant to serum neutralization arise during persistent infection of rhesus monkeys. J Virol 1993;67: 4104–4113.PubMedGoogle Scholar
  38. 38.
    Chang MI, Panorchan P, Dobrowsky TM, Tseng Y, Wirtz D: Single-molecule analysis of human immunodeficiency virus type 1 gp120-receptor interactions in living cells. J Virol 2005;79: 14748–14755.PubMedCrossRefGoogle Scholar
  39. 39.
    Hoxie JA: Hypothetical assignment of intrachain disulfide bonds for HIV-2 and SIV envelope glycoproteins. AIDS Res Hum Retroviruses 1991;7: 495–499.PubMedGoogle Scholar
  40. 40.
    Leonard CK, Spellman MW, Riddle L, Harris RJ, Thomas JN, Gregory TJ: Assigment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotien (gp120) expressed in Chinese hamster ovary cells. J Biol Chem 1990;265: 10373–10382.PubMedGoogle Scholar
  41. 41.
    Gallaher WR, Ball JM, Garry RF, Martin-Amedee AM, Montelaro RC: A general model for the surface glycoprotiens of HIV and other retroviruses. AIDS Res Hum Retroviruses 1995;11: 191–202.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc. 2006

Authors and Affiliations

  1. 1.Department of Medicine, Infections Diseases DivisionUniversity of Pittsburgh School of MedicinePittsburgh

Personalised recommendations