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PMID: 23980172 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Immunotherapy of chronic hepatitis C virus infection with antibodies against programmed cell death-1 (PD-1).

Fuller MJ, Callendret B, Zhu B, Freeman GJ, Hasselschwert DL, Satterfield W, Sharpe AH, Dustin LB, Rice CM, Grakoui A, Ahmed R, Walker CM

Abstract

Hepatitis C virus (HCV) persistence is facilitated by exhaustion of CD8+ T cells that express the inhibitory receptor programmed cell death 1 (PD-1). Blockade of PD-1 signaling improves in vitro proliferation of HCV-specific T lymphocytes, but whether antiviral function can be restored in infected individuals is unknown. To address this question, chimpanzees with persistent HCV infection were treated with anti-PD-1 antibodies. A significant reduction in HCV viremia was observed in one of three treated animals without apparent hepatocellular injury. Viremia rebounded in the responder animal when antibody treatment was discontinued. Control of HCV replication was associated with restoration of intrahepatic CD4+ and CD8+ T-cell immunity against multiple HCV proteins. The responder animal had a history of broader T-cell immunity to multiple HCV proteins than the two chimpanzees that did not respond to PD-1 therapy. The results suggest that successful PD-1 blockade likely requires a critical threshold of preexisting virus-specific T cells in liver and warrants consideration of therapeutic vaccination strategies in combination with PD-1 blockade to broaden narrow responses. Anti-PD-1 immunotherapy may also facilitate control of other persistent viruses, notably the hepatitis B virus where options for long-term control of virus replication are limited.

MeSH Terms
Animals Antibodies, Monoclonal/therapeutic use CD8-Positive T-Lymphocytes/immunology Disease Models, Animal Hepacivirus/immunology Hepatitis C, Chronic/immunology,therapy,virology Immunotherapy Pan troglodytes Programmed Cell Death 1 Receptor/antagonists & inhibitors,immunology Viremia/immunology,therapy Virus Replication
Chemicals
Antibodies, Monoclonal Programmed Cell Death 1 Receptor
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Fuller Michael J
Center for Vaccines and Immunity, Nationwide Children's Hospital, Columbus, OH 43205.
Callendret Benoit
Zhu Baogong
Freeman Gordon J
Hasselschwert Dana L
Satterfield William
Sharpe Arlene H
Dustin Lynn B
Rice Charles M
Grakoui Arash
Ahmed Rafi
Walker Christopher M
References (36)
36 references, click to expand
  1. Restoring function in exhausted CD8 T cells during chronic viral infection.
    Nature. 2006 Feb 9;439(7077):682-7 PMID: 16382236
  2. Blockade of programmed death-1 ligands on dendritic cells enhances T cell activation and cytokine production.
    J Immunol. 2003 Feb 1;170(3):1257-66 PMID: 12538684
  3. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer.
    N Engl J Med. 2012 Jun 28;366(26):2443-54 PMID: 22658127
  4. In-fusion assembly: seamless engineering of multidomain fusion proteins, modular vectors, and mutations.
    Biotechniques. 2007 Sep;43(3):354-9 PMID: 17907578
  5. CD8 epitope escape and reversion in acute HCV infection.
    J Exp Med. 2004 Dec 20;200(12):1593-604 PMID: 15611288
  6. A spatial view of the CD8+ T-cell response: the case of HCV.
    Rev Med Virol. 2011 Nov;21(6):347-57 PMID: 21732472
  7. T cell responses in hepatitis C: the good, the bad and the unconventional.
    Gut. 2012 Aug;61(8):1226-34 PMID: 21873736
  8. Viral and immunological determinants of hepatitis C virus clearance, persistence, and disease.
    Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15661-8 PMID: 12441397
  9. PD-L2 is a second ligand for PD-1 and inhibits T cell activation.
    Nat Immunol. 2001 Mar;2(3):261-8 PMID: 11224527
  10. Novel infectious cDNA clones of hepatitis C virus genotype 3a (strain S52) and 4a (strain ED43): genetic analyses and in vivo pathogenesis studies.
    J Virol. 2010 May;84(10):5277-93 PMID: 20200247
  11. Immune evasion versus recovery after acute hepatitis C virus infection from a shared source.
    J Exp Med. 2005 Jun 6;201(11):1725-31 PMID: 15939788
  12. Vaccine-induced early control of hepatitis C virus infection in chimpanzees fails to impact on hepatic PD-1 and chronicity.
    Hepatology. 2007 Mar;45(3):602-13 PMID: 17326154
  13. Mutational escape from CD8+ T cell immunity: HCV evolution, from chimpanzees to man.
    J Exp Med. 2005 Jun 6;201(11):1709-14 PMID: 15939787
  14. Hepatitis C virus-specific CTL responses in the liver of chimpanzees with acute and chronic hepatitis C.
    J Immunol. 1993 Oct 15;151(8):4189-99 PMID: 7691940
  15. Variable patterns of programmed death-1 expression on fully functional memory T cells after spontaneous resolution of hepatitis C virus infection.
    J Virol. 2008 May;82(10):5109-14 PMID: 18337576
  16. Cellular immune selection with hepatitis C virus persistence in humans.
    J Exp Med. 2005 Jun 6;201(11):1741-52 PMID: 15939790
  17. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer.
    N Engl J Med. 2012 Jun 28;366(26):2455-65 PMID: 22658128
  18. Pathogenesis of hepatitis B virus infection.
    Pathol Biol (Paris). 2010 Aug;58(4):258-66 PMID: 20116937
  19. Role of the coinhibitory receptor cytotoxic T lymphocyte antigen-4 on apoptosis-Prone CD8 T cells in persistent hepatitis B virus infection.
    Hepatology. 2011 May;53(5):1494-503 PMID: 21360567
  20. Programmed death-1 (PD-1) is a marker of germinal center-associated T cells and angioimmunoblastic T-cell lymphoma.
    Am J Surg Pathol. 2006 Jul;30(7):802-10 PMID: 16819321
  21. Adaptive immunity to the hepatitis C virus.
    Adv Virus Res. 2010;78:43-86 PMID: 21040831
  22. Analysis of CD8+ T-cell-mediated inhibition of hepatitis C virus replication using a novel immunological model.
    Gastroenterology. 2009 Apr;136(4):1391-401 PMID: 19185579
  23. CD40L-Tri, a novel formulation of recombinant human CD40L that effectively activates B cells.
    Cancer Immunol Immunother. 2013 Feb;62(2):347-57 PMID: 22926059
  24. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA.
    Science. 1997 Jul 25;277(5325):570-4 PMID: 9228008
  25. Inhibitory molecules that regulate expansion and restoration of HCV-specific CD4+ T cells in patients with chronic infection.
    Gastroenterology. 2011 Oct;141(4):1422-31, 1431.e1-6 PMID: 21763239
  26. Enhancing SIV-specific immunity in vivo by PD-1 blockade.
    Nature. 2009 Mar 12;458(7235):206-10 PMID: 19078956
  27. HCV persistence and immune evasion in the absence of memory T cell help.
    Science. 2003 Oct 24;302(5645):659-62 PMID: 14576438
  28. PD-1 blockade during chronic SIV infection reduces hyperimmune activation and microbial translocation in rhesus macaques.
    J Clin Invest. 2012 May;122(5):1712-6 PMID: 22523065
  29. The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes.
    Immunity. 2001 Dec;15(6):883-95 PMID: 11754811
  30. Revealing the role of CD4(+) T cells in viral immunity.
    J Exp Med. 2012 Jul 30;209(8):1391-5 PMID: 22851641
  31. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence.
    J Clin Invest. 2009 Jul;119(7):1745-54 PMID: 19587449
  32. Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection.
    J Exp Med. 2008 Mar 17;205(3):543-55 PMID: 18332181
  33. Divergent and convergent evolution after a common-source outbreak of hepatitis C virus.
    J Exp Med. 2005 Jun 6;201(11):1753-9 PMID: 15939791
  34. Determinants of viral clearance and persistence during acute hepatitis C virus infection.
    J Exp Med. 2001 Nov 19;194(10):1395-406 PMID: 11714747
  35. Towards an HIV cure: a global scientific strategy.
    Nat Rev Immunol. 2012 Jul 20;12(8):607-14 PMID: 22814509
  36. Inhibitory receptors on lymphocytes: insights from infections.
    J Immunol. 2012 Apr 1;188(7):2957-65 PMID: 22442493
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2013-09-10
Epub
2013-00-26
Pages
15001-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3773803
Subset
IM
Grants
NIDDK NIH HHS · R01 DK083356 · United States
NIAID NIH HHS · R37 AI47367 · United States
NIAID NIH HHS · P01 AI080192 · United States
NIAID NIH HHS · U19 AI48231 · United States
NCRR NIH HHS · P51 RR000165 · United States
NIH HHS · U42 OD014838 · United States
NIAID NIH HHS · U19 AI048231 · United States
NIAID NIH HHS · R01 AI074417 · United States
NIDDK NIH HHS · DK083356 · United States
NIAID NIH HHS · R37 AI047367 · United States
NIAID NIH HHS · P01 AI056299 · United States
NIAID NIH HHS · AI070101 · United States
NIH HHS · 9U42 OD014838 · United States
NIAID NIH HHS · R56 AI070101 · United States
NCRR NIH HHS · RR-00165 · United States
NIAID NIH HHS · R01 AI070101 · United States
NIAID NIH HHS · U19 AI082630 · United States
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