An effective interferon-gamma-mediated inhibition of hepatitis C virus replication by natural killer cells is associated with spontaneous clearance of acute hepatitis C in human immunodeficiency virus-positive patients

Hepatology

Volumn 59, Issue 3, 2014, Pages 814-827

  Kokordelis, Pavlos ^a,b   Krämer, Benjamin ^a,b   Körner, Christian ^a   Boesecke, Christoph ^a,b   Voigt, Esther ^c   Ingiliz, Patrick ^d   Glässner, Andreas ^a,b   Eisenhardt, Marianne ^a,b   Wolter, Franziska ^a,b   Kaczmarek, Dominik ^a,b   Nischalke, Hans Dieter ^a,b   Rockstroh, Jürgen K ^a,b   Spengler, Ulrich ^a,b   Nattermann, Jacob ^a,b  

^a UNIVERSITY OF BONN   (Germany)

^b German Center for Infection Research (DZIF)   (Germany)

^c Praxis am Ebertplatz   (Germany)

^d Medical Center for Infectious Diseases   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GAMMA INTERFERON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; VIRUS RNA;

ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CELL ACTIVITY; CHRONIC DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DEGRANULATION; DISEASE COURSE; FEMALE; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; INFECTION; INFECTION RISK; LYMPHOCYTE FUNCTION; MALE; MIXED INFECTION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SELF LIMITING INFECTION; VIRAL CLEARANCE; VIRUS INHIBITION; VIRUS LOAD; VIRUS REPLICATION;

ADULT; AGED; CELL LINE, TUMOR; COINFECTION; FEMALE; HEPACIVIRUS; HEPATITIS C; HIV INFECTIONS; HUMANS; IMMUNOPHENOTYPING; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MALE; MIDDLE AGED; VIRUS REPLICATION;

EID: 84896701199     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26782     Document Type: Article

References (37)

1. Lacombe K, Rockstroh J. HIV and viral hepatitis coinfections: advances and challenges. Gut 2012;61(Suppl 1):i47-i58.
2. Boesecke C, Rockstroh JK. Acute hepatitis C in patients with HIV. Semin Liver Dis 2012;32:130-137.
3. Benhamou Y, Bochet M, Di Martino V, Charlotte F, Azria F, Coutellier A, et al. Liver fibrosis progression in human immunodeficiency virus and hepatitis C virus coinfected patients.The Multivirc Group. Hepatology 1999;30:1054-1058.
4. Martin P, Di Bisceglie AM, Kassianides C, Lisker-Melman M, Hoofnagle JH. Rapidly progressive non-A, non-B hepatitis in patients with human immunodeficiency virus infection. Gastroenterology 1989;97:1559-1561.
5. Rockstroh JK, Spengler U, Sudhop T, Ewig S, Theisen A, Hammerstein U, et al. Immunosuppression may lead to progression of hepatitis C virus-associated liver disease in hemophiliacs coinfected with HIV. Am J Gastroenterol 1996;91:2563-2568.
6. Alter G, Jost S, Rihn S, Reyor LL, Nolan BE, Ghebremichael M, et al. Reduced frequencies of NKp30+NKp46+, CD161+, and NKG2D+ NK cells in acute HCV infection may predict viral clearance. J Hepatol 2011;55:278-288.
7. Amadei B, Urbani S, Cazaly A, Fisicaro P, Zerbini A, Ahmed P, et al. Activation of natural killer cells during acute infection with hepatitis C virus. Gastroenterology 2010;138:1536-1545.
8. Pelletier S, Drouin C, Bédard N, Khakoo SI, Bruneau J, Shoukry NH. Increased degranulation of natural killer cells during acute HCV correlates with the magnitude of virus-specific T cell responses. J Hepatol 2010;53:805-816.
9. Norris S, Collins C, Doherty DG, Smith F, McEntee G, Traynor O, et al. Resident human hepatic lymphocytes are phenotypically different from circulating lymphocytes. J Hepatol 1998;28:84-90.
10. Waggoner SN, Cornberg M, Selin LK, Welsh RM. Natural killer cells act as rheostats modulating antiviral T cells. Nature 2011;481:394-398.
11. Narni-Mancinelli E, Jaeger BN, Bernat C, Fenis A, Kung S, De Gassart A, et al. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science 2012;335:344-348.
12. Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol 2001;22:633-640.
13. Khakoo SI, Thio CL, Martin MP, Brooks CR, Gao X, Astemborski J, et al. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 2004;305:872-874.
14. Dring MM, Morrison MH, McSharry BP, Guinan KJ, Hagan R;Irish HCV Research Consortium, O'Farrelly C, Gardiner CM. Innate immune genes synergize to predict increased risk of chronic disease in hepatitis C virus infection. Proc Natl Acad Sci U S A 2011;108:5736-5741.
15. Knapp S, Warshow U, Hegazy D, Brackenbury L, Guha IN, Fowell A, et al. Consistent beneficial effects of killer cell immunoglobulin-like receptor 2DL3 and group 1 human leukocyte antigen-C following exposure to hepatitis C virus. Hepatology 2009;51:1168-1175.
16. Rauch A, Laird R, McKinnon E, Telenti A, Furrer H, Weber R, et al. Influence of inhibitory killer immunoglobulin-like receptors and their HLA-C ligands on resolving hepatitis C virus infection. Tissue Antigens 2007;69(Suppl 1):237-240.
17. Li Y, Zhang T, Ho C, Orange JS, Douglas SD, Ho WZ. Natural killer cells inhibit hepatitis C virus expression. J Leukoc Biol 2004;76:1171-1179.
18. Larkin J, Bost A, Glass JI, Tan SL. Cytokine-activated natural killer cells exert direct killing of hepatoma cells harboring hepatitis C virus replicons. J Interferon Cytokine Res 2006;26:854-865.
19. Jost S, Altfeld M. Control of human viral infections by natural killer cells. Annu Rev Immunol 2013;31:163-194.
20. Kramer B, Korner C, Kebschull M, Glassner A, Eisenhardt M, Nischalke HD, et al. Natural killer p46High expression defines a natural killer cell subset that is potentially involved in control of hepatitis C virus replication and modulation of liver fibrosis. Hepatology 2012;56:1201-1213.
21. Stegmann KA, Bjorkstrom NK, Veber H, Ciesek S, Riese P, Wiegand J, et al. Interferon-alpha-induced TRAIL on natural killer cells is associated with control of hepatitis C virus infection. Gastroenterology;138:1885-1897.
22. Ahlenstiel G, Edlich B, Hogdal LJ, Rotman Y, Noureddin M, Feld JJ, et al. Early changes in natural killer cell function indicate virologic response to interferon therapy for hepatitis C. Gastroenterology;141:1231-1239, 1239.e1-2.
23. Jo J, Aichele U, Kersting N, Klein R, Aichele P, Bisse E, et al. Analysis of CD8+ T-cell-mediated inhibition of hepatitis C virus replication using a novel immunological model. Gastroenterology 2009;136:1391-1401.
24. 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.
25. Shoukry NH, Grakoui A, Houghton M, Chien DY, Ghrayeb J, Reimann KA, Walker CM. Memory CD8+ T cells are required for protection from persistent hepatitis C virus infection. J Exp Med 2003;197:1645-1655.
26. Bowen DG, Walker CM. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 2005;436:946-952.
27. Pembroke T, Christian A, Jones E, Hills RK, Wang EC, Gallimore AM, Godkin A. The paradox of NKp46+ natural killer cells: drivers of severe hepatitis C virus-induced pathology but in-vivo resistance to interferon alpha treatment. Gut 2013 May 11. doi: 10.1136/gutjnl-2013-304472.
28. Golden-Mason L, Stone AE, Bambha KM, Cheng L, Rosen HR. Race- and gender-related variation in natural killer p46 expression associated with differential anti-hepatitis C virus immunity. Hepatology 2012;56:1214-1222.
29. Sène D, Levasseur F, Abel M, Lambert M, Camous X, Hernandez C, et al. Hepatitis C virus (HCV) evades NKG2D-dependent NK cell responses through NS5A-mediated imbalance of inflammatory cytokines. PLoS Pathog 2010;6:e1001184.
30. Nattermann J, Feldmann G, Ahlenstiel G, Langhans B, Sauerbruch T, Spengler U. Surface expression and cytolytic function of natural killer cell receptors is altered in chronic hepatitis C. Gut 2006;55:869-877.
31. Oliviero B, Varchetta S, Paudice E, Michelone G, Zaramella M, Mavilio D, et al. Natural killer cell functional dichotomy in chronic hepatitis B and chronic hepatitis C virus infections. Gastroenterology 2009;137:1151-1160
32. De Maria A, Fogli M, Mazza S, Basso M, Picciotto A, Costa P, et al. Increased natural cytotoxicity receptor expression and relevant IL-10 production in NK cells from chronically infected viremic HCV patients. Eur J Immunol 2007;37:445-455.
33. De Maria A, Fogli M, Costa P, Murdaca G, Puppo F, Mavilio D, et al. The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur J Immunol 2003;33:2410-2418.
34. Mavilio D, Benjamin J, Daucher M, Lombardo G, Kottilil S, Planta MA, et al. Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc Natl Acad Sci U S A. 2003;100:15011-15016.
35. Stegmann KA, Bjorkstrom NK, Ciesek S, Lunemann S, Jaroszewicz J, Wiegand J, et al. Interferon alpha-stimulated natural killer cells from patients with acute hepatitis C virus (HCV) infection recognize HCV-infected and uninfected hepatoma cells via DNAX accessory molecule-1. J Infect Dis 2011;205:1351-1362.
36. Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 2004;294:15-22.
37. Binder M, Quinkert D, Bochkarova O, Klein R, Kezmic N, Bartenschlager R, Lohmann V. Identification of determinants involved in initiation of hepatitis C virus RNA synthesis by using intergenotypic replicase chimeras. J Virol 2007;81:5270-5283.