• Please log in or register to access this feature.

Viral Hepatitis

You have full text access to this OnlineOpen article

CD4+ immune escape and subsequent T-cell failure following chimpanzee immunization against hepatitis C virus†

  1. Montserrat Puig1,
  2. Kathleen Mihalik1,
  3. John C. Tilton2,
  4. Ollie Williams3,
  5. Michael Merchlinsky3,
  6. Mark Connors2,
  7. Stephen M. Feinstone1,
  8. Marian E. Major1,‡,*

Article first published online: 29 AUG 2006

DOI: 10.1002/hep.21319

Issue

Hepatology

Hepatology

Volume 44, Issue 3, pages 736–745, September 2006

Additional Information

How to Cite

Puig, M., Mihalik, K., Tilton, J. C., Williams, O., Merchlinsky, M., Connors, M., Feinstone, S. M. and Major, M. E. (2006), CD4+ immune escape and subsequent T-cell failure following chimpanzee immunization against hepatitis C virus. Hepatology, 44: 736–745. doi: 10.1002/hep.21319

Author Information

  1. 1

    Laboratory of Hepatitis Viruses, Center for Biologics Evaluation and Research, Food and Drug Administration, Bethesda, MD

  2. 2

    Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD

  3. 3

    Laboratory of Viral Diseases, Center for Biologics Evaluation and Research, Food and Drug Administration, Bethesda, MD

  1. ‡

    fax: (301) 402-5585.

*Laboratory of Hepatitis Viruses, Division of Viral Products, Bldg. 29A/Room 1D10/HFM 448, 8800 Rockville Pike, Bethesda, MD 20892

  1. †

    Potential conflict of interest: Nothing to report.

  2. ‡

    fax: (301) 402-5585.

Publication History

  1. Issue published online: 29 AUG 2006
  2. Article first published online: 29 AUG 2006
  3. Manuscript Accepted: 23 JUN 2006
  4. Manuscript Received: 21 DEC 2005

Funded by

  • FDA
  • National Vaccine Program Office
  • National Cancer Institute. Grant Number: CA85883
Corrected by:

Correction: Correction

Vol. 55, Issue 3, 983, Article first published online: 23 FEB 2012

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (614K)

References

  • 1
    Alter MJ, Kruszon-Moran D, Nainan OV, McQuillan GM, Gao F, Moyer LA, et al. The prevalence of hepatitis C virus infection in the United States, 1988 through 1994. N Engl J Med 1999; 341: 556–562.
  • 2
    Manns MP, McHutchison JG, Gordon SC, Rustgi VK, Shiffman M, Reindollar R, et al. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet 2001; 358: 958–965.
  • 3
    Fried MW, Shiffman ML, Reddy KR, Smith C, Marinos G, Goncales FL Jr, et al. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 2002; 347: 975–982.
  • 4
    Farci P, Alter HJ, Govindarajan S, Wong DC, Engle R, Lesniewski R, et al. Lack of protective immunity against reinfection with hepatitis C virus. Science 1992; 258: 140.
  • 5
    Prince AM, Brotman B, Huima T, Pascual D, Jaffery M, Inchauspe G. Immunity in hepatitis C infection. J Infect Dis 1992; 165: 438–443.
  • 6
    Major ME, Mihalik K, Puig M, Rehermann B, Nascimbeni M, Rice CM, et al. Previously infected and recovered chimpanzees exhibit rapid responses that control hepatitis C virus replication upon rechallenge. J Virol 2002; 76: 6586–6595.
  • 7
    Weiner AJ, Paliard X, Selby MJ, Medina-Selby A, Coit D, Nguyen S, et al. Intrahepatic genetic inoculation of hepatitis C virus RNA confers cross-protective immunity. J Virol 2001; 75: 7142–7148.
  • 8
    Bassett SE, Guerra B, Brasky K, Miskovsky E, Houghton M, Klimpel GR, et al. Protective immune response to hepatitis C virus in chimpanzees rechallenged following clearance of primary infection. HEPATOLOGY 2001; 33: 1479–1487.
    Direct Link:
  • 9
    Nascimbeni M, Mizukoshi E, Bosmann M, Major ME, Mihalik K, Rice CM, et al. Kinetics of CD4+ and CD8+ memory T-cell responses during hepatitis C virus rechallenge of previously recovered chimpanzees. J Virol 2003; 77: 4781–4793.
  • 10
    Mehta SH, Cox A, Hoover DR, Wang XH, Mao Q, Ray S, et al. Protection against persistence of hepatitis C. Lancet 2002; 359: 1478–1483.
  • 11
    Mercer DF, Schiller DE, Elliott JF, Douglas DN, Hao C, Rinfret A, et al. Hepatitis C virus replication in mice with chimeric human livers. Nat Med 2001; 7: 927–933.
  • 12
    Lanford RE, Bigger C. Advances in model systems for hepatitis C virus research. Virology 2002; 293(1): 1–9.
  • 13
    Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 2005; 11: 791–796.
  • 14
    Farci P, Shimoda A, Coiana A, Diaz G, Peddis G, Melpolder JC, et al. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 2000; 288: 339–344.
  • 15
    Erickson AL, Kimura Y, Igarashi S, Eichelberger J, Houghton M, Sidney J, et al. The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes. Immunity 2001; 15: 883–895.
  • 16
    Ward S, Lauer G, Isba R, Walker B, Klenerman P. Cellular immune responses against hepatitis C virus: the evidence base 2002. Clin Exp Immunol 2002; 128: 195–203.
    Direct Link:
  • 17
    Farci P, Alter HJ, Wong DC, Miller RH, Govindarajan S, Engle R, et al. Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc Natl Acad Sci U S A 1994; 91: 7792–7796.
  • 18
    Yu MY, Bartosch B, Zhang P, Guo ZP, Renzi PM, Shen LM, et al. Neutralizing antibodies to hepatitis C virus (HCV) in immune globulins derived from anti-HCV-positive plasma. Proc Natl Acad Sci U S A 2004; 101: 7705–7710.
  • 19
    Choo QL, Kuo G, Ralston R, Weiner A, Chien D, Van Nest G, et al. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc Natl Acad Sci U S A 1994; 91: 1294–1298.
  • 20
    Forns X, Payette PJ, Ma X, Satterfield W, Eder G, Mushahwar IK, et al. Vaccination of chimpanzees with plasmid DNA encoding the hepatitis C virus (HCV) envelope E2 protein modified the infection after challenge with homologous monoclonal HCV. HEPATOLOGY 2000; 32: 618–625.
    Direct Link:
  • 21
    Puig M, Major ME, Mihalik K, Yu MY, Feinstone SM. Immunization of chimpanzees with an envelope protein-based vaccine enhances specific humoral and cellular immune responses that delay hepatitis C virus infection. Vaccine 2004; 22: 991–1000.
  • 22
    Bartosch B, Bukh J, Meunier JC, Granier C, Engle RE, Blackwelder WC, et al. In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc Natl Acad Sci U S A 2003; 100: 14199–14204.
  • 23
    Logvinoff C, Major ME, Oldach D, Heyward S, Talal A, Balfe P, et al. Neutralizing antibody response during acute and chronic hepatitis C virus infection. Proc Natl Acad Sci U S A 2004; 101: 10149–10154.
  • 24
    Diepolder HM, Gerlach JT, Zachoval R, Hoffmann RM, Jung MC, Wierenga EA, et al. Immunodominant CD4+ T-cell epitope within nonstructural protein 3 in acute hepatitis C virus infection. J Virol 1997; 71: 6011–6019.
  • 25
    Grüner NH, Gerlach TJ, Jung MC, Diepolder HM, Schirren CA, Schraut WW, et al. Association of hepatitis C virus-specific CD8+ T cells with viral clearance in acute hepatitis C. J Infect Dis 2000; 181: 1528–1536.
  • 26
    Thimme R, Oldach D, Chang KM, Steiger C, Ray SC, Chisari FV. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 2001; 194: 1395–1406.
  • 27
    Cooper S, Erickson AL, Adams EJ, Kansopon J, Weiner AJ, Chien DY, et al. Analysis of a successful immune response against hepatitis C virus. Immunity 1999; 10: 439–449.
  • 28
    Thimme R, Bukh J, Spangenberg HC, Wieland S, Pemberton J, Steiger C, et al. Viral and immunological determinants of hepatitis C virus clearance, persistence, and disease. Proc Natl Acad Sci U S A 2002; 99: 15661–15668.
  • 29
    Grakoui A, Shoukry NH, Woollard DJ, Han JH, Hanson HL, Ghrayeb J, et al. HCV persistence and immune evasion in the absence of memory T cell help. Science 2003; 302: 659–662.
  • 30
    Shoukry NH, Grakoui A, Houghton M, Chien DY, Ghrayeb J, Reimann KA, et al. Memory CD8+ T cells are required for protection from persistent hepatitis C virus infection. J Exp Med 2003; 197: 1645–1655.
  • 31
    Rollier C, Depla E, Drexhage JA, Verschoor EJ, Verstrepen BE, Fatmi A, et al. Control of heterologous hepatitis C virus infection in chimpanzees is associated with the quality of vaccine-induced peripheral T-helper immune response. J Virol 2004; 78(1): 187–196.
  • 32
    Youn JW, Park SH, Lavillette D, Cosset FL, Yang SH, Lee CG, et al. Sustained E2 antibody response correlates with reduced peak viremia after hepatitis C virus infection in the chimpanzee. HEPATOLOGY 2005; 42: 1429–1436.
    Direct Link:
  • 33
    Folgori A, Capone S, Ruggeri L, Meola A, Sporeno E, Ercole BB, et al. A T-cell HCV vaccine eliciting effective immunity against heterologous virus challenge in chimpanzees. Nat Med 2006; 12(2): 190–197.
  • 34
    Kolykhalov AA, Agapov EV, Blight K, Mihalik K, Feinstone SM, Rice CM. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 1997; 277: 570–574.
  • 35
    MargolisHS, AlterMJ, LiangTJ, DienstagJL, eds. Protective antibodies in immune globulins prepared from anti-hepatitis C virus (HCV)-positive plasma units: update of a chimpanzee study. In: Viral Hepatitis and Liver Disease. London: International Medical Press, 2002.
  • 36
    Earl PL, Moss B. Generation of recombinant vaccinia viruses. In: AusubelFM, BrentR, KingstonetRE, eds. Current Protocols in Molecular Biology. New York: Green Publishing Associates/Wiley Interscience, 1991: 16.17.1–16.17.16.
  • 37
    Verthelyi D, Kenney RT, Seder RA, Gam AA, Friedag B, Klinman DM. CpG oligodeoxynucleotides as vaccine adjuvants in primates. J Immunol 2002; 168: 1659–1663.
  • 38
    Major ME, Mihalik K, Fernandez J, Seidman J, Kleiner D, Kolykhalov AA, et al. Long-term follow-up of chimpanzees inoculated with the first infectious clone for hepatitis C virus. J Virol 1999; 73: 3317–3325.
  • 39
    Puig M, Mihalik K, Yu MY, Feinstone SM, Major ME. Sensitivity and reproducibility of HCV quantitation in chimpanzee sera using TaqMan real-time PCR assay. J Virol Methods 2002; 105(2): 253–263.
  • 40
    Holmes K, Fowlkes B, Schmid I. In: ColiganJ, KruisbeekA, MarguliesD, SheevacE, StroberWJ, eds. Current Protocols in Immunology. New York: Green Publishing Associates/Wiley Interscience, 1995: 5.3.1–5.3.23.
  • 41
    Major ME, Dahari H, Mihalik K, Puig M, Rice CM, Neumann AU, et al. Hepatitis C virus kinetics and host responses associated with disease and outcome of infection in chimpanzees. HEPATOLOGY 2004; 39: 1709–1720.
    Direct Link:
  • 42
    Whitmire JK, Flavell RA, Grewal IS, Larsen CP, Pearson TC, Ahmed R. CD40-CD40 ligand costimulation is required for generating antiviral CD4 T cell responses but is dispensable for CD8 T cell responses. J Immunol 1999; 163: 3194–3201.
  • 43
    Gerlach JT, Diepolder HM, Jung MC, Gruener NH, Schraut WW, Zachoval R, et al. Recurrence of hepatitis C virus after loss of virus-specific CD4(+) T- cell response in acute hepatitis C. Gastroenterology 1999; 117: 933–941.
  • 44
    Eckels DD, Wang H, Bian TH, Tabatabai N, Gill JC. Immunobiology of hepatitis C virus (HCV) infection: the role of CD4 T cells in HCV infection. Immunol Rev 2000; 174: 90–97.
    Direct Link:
  • 45
    Wang JH, Layden TJ, Eckels DD. Modulation of the peripheral T-Cell response by CD4 mutants of hepatitis C virus: transition from a Th1 to a Th2 response. Hum Immunol 2003; 64: 662–673.
  • 46
    Diepolder HM, Zachoval R, Hoffmann RM, Wierenga EA, Santantonio T, Jung MC, et al. Possible mechanism involving T-lymphocyte response to non-structural protein 3 in viral clearance in acute hepatitis C virus infection. Lancet 1995; 346: 1006–1007.
  • 47
    Missale G, Bertoni R, Lamonaca V, Valli A, Massari M, Mori C, et al. Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. J Clin Invest 1996; 98: 706–714.
  • 48
    Murali-Krishna K, Altman JD, Suresh M, Sourdive DJ, Zajac AJ, Miller JD, et al. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 1998; 8: 177–187.
  • 49
    Migueles SA, Connors M. The Role of CD4(+) and CD8(+) T Cells in Controlling HIV Infection. Curr Infect Dis Rep 2002; 4: 461–467.
  • 50
    Wedemeyer H, He XS, Nascimbeni M, Davis AR, Greenberg HB, Hoofnagle JH, et al. Impaired effector function of hepatitis C virus-specific CD8+ T cells in chronic hepatitis C virus infection. J Immunol 2002; 169: 3447–3458.
View Full Article (HTML) Get PDF (614K)