CD40 inhibits replication of hepatitis C virus in primary human hepatocytes by c-jun N terminal kinase activation independent from the interferon pathway

Hepatology

Volumn 57, Issue 1, 2013, Pages 23-36

  Rau, Sibylle J ^a   Hildt, Eberhard ^b,c   Himmelsbach, Kiyoshi ^b   Thimme, Robert ^a   Wakita, Takaji ^d   Blum, Hubert E ^a   Fischer, Richard ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b PAUL EHRLICH INSTITUT   (Germany)

^c DZIF Deutsches Zentrum für Infektionsforschung   (Germany)

^d NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CD40 ANTIGEN; CD40 LIGAND; INTERFERON; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 5A; STAT PROTEIN; STRESS ACTIVATED PROTEIN KINASE;

ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; COCULTURE; CYTOKINE PRODUCTION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS PARTICLE; VIRUS REPLICATION;

ANTIGENS, CD40; APOPTOSIS; CD40 LIGAND; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DOWN-REGULATION; ENZYME ACTIVATION; HEPACIVIRUS; HEPATITIS C; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON-ALPHA; JANUS KINASES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; STAT TRANSCRIPTION FACTORS; TNF RECEPTOR-ASSOCIATED FACTOR 2; TNF RECEPTOR-ASSOCIATED FACTOR 3; VIRION; VIRUS REPLICATION;

EID: 84872133969     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.25966     Document Type: Article

References (43)

1. Dustin LB, Rice CM. Flying under the radar: the immunobiology of hepatitis C. Annu Rev Immunol 2007; 25: 71-99.
2. 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.
3. Frese M, Schwarzle V, Barth K, Krieger N, Lohmann V, Mihm S, et al. Interferon-gamma inhibits replication of subgenomic and genomic hepatitis C virus RNAs. HEPATOLOGY 2002; 35: 694-703.
4. Elgueta R, Benson MJ, de Vries VC, Wasiuk A, Guo Y, Noelle RJ. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol Rev 2009; 229: 152-172.
5. Mazzei GJ, Edgerton MD, Losberger C, Lecoanet-Henchoz S, Graber P, Durandy A, et al. Recombinant soluble trimeric CD40 ligand is biologically active. J Biol Chem 1995; 270: 7025-7028.
6. Bishop GA, Moore CR, Xie P, Stunz LL, Kraus ZJ. TRAF proteins in CD40 signaling. Adv Exp Med Biol 2007; 597: 131-151.
7. Gallagher E, Enzler T, Matsuzawa A, Anzelon-Mills A, Otero D, Holzer R, et al. Kinase MEKK1 is required for CD40-dependent activation of the kinases Jnk and p38, germinal center formation, B cell proliferation and antibody production. Nat Immunol 2007; 8: 57-63.
8. Foltz IN, Gerl RE, Wieler JS, Luckach M, Salmon RA, Schrader JW. Human mitogen-activated protein kinase kinase 7 (MKK7) is a highly conserved c-Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK) activated by environmental stresses and physiological stimuli. J Biol Chem 1998; 273: 9344-9351.
9. Sasaki T, Wada T, Kishimoto H, Irie-Sasaki J, Matsumoto G, Goto T, et al. The stress kinase mitogen-activated protein kinase kinase (MKK)7 is a negative regulator of antigen receptor and growth factor receptor-induced proliferation in hematopoietic cells. J Exp Med 2001; 194: 757-768.
10. Nishina H, Bachmann M, Oliveira-dos-Santos AJ, Kozieradzki I, Fischer KD, Odermatt B, et al. Impaired CD28-mediated interleukin 2 production and proliferation in stress kinase SAPK/ERK1 kinase (SEK1)/mitogen-activated protein kinase kinase 4 (MKK4)-deficient T lymphocytes. J Exp Med 1997; 186: 941-953.
11. Hanissian SH, Geha RS. Jak3 is associated with CD40 and is critical for CD40 induction of gene expression in B cells. Immunity 1997; 6: 379-387.
12. Gough DJ, Levy DE, Johnstone RW, Clarke CJ. IFNgamma signaling-does it mean JAK-STAT? Cytokine Growth Factor Rev 2008; 19: 383-394.
13. Polyak SJ, Morishima C, Shuhart MC, Wang CC, Liu Y, Lee DY. Inhibition of T-cell inflammatory cytokines, hepatocyte NF-kappaB signaling, and HCV infection by standardized Silymarin. Gastroenterology 2007; 132: 1925-1936.
14. Trujillo-Murillo K, Rincon-Sanchez AR, Martinez-Rodriguez H, Bosques-Padilla F, Ramos-Jimenez J, Barrera-Saldana HA, et al. Acetylsalicylic acid inhibits hepatitis C virus RNA and protein expression through cyclooxygenase 2 signaling pathways. HEPATOLOGY 2008; 47: 1462-1472.
15. Travert M, Ame-Thomas P, Pangault C, Morizot A, Micheau O, Semana G, et al. CD40 ligand protects from TRAIL-induced apoptosis in follicular lymphomas through NF-kappaB activation and up-regulation of c-FLIP and Bcl-xL. J Immunol 2008; 181: 1001-1011.
16. Younes A. CD40 ligand therapy of lymphoma patients. J Clin Oncol 2001; 19: 4351-4353.
17. Loskog A, Totterman TH. CD40L - a multipotent molecule for tumor therapy. Endocr Metab Immune Disord Drug Targets 2007; 7: 23-28.
18. Vonderheide RH, Flaherty KT, Khalil M, Stumacher MS, Bajor DL, Hutnick NA, et al. Clinical activity and immune modulation in cancer patients treated with CP-870, 893, a novel CD40 agonist monoclonal antibody. J Clin Oncol 2007; 25: 876-883.
19. Lan L, Gorke S, Rau SJ, Zeisel MB, Hildt E, Himmelsbach K, et al. Hepatitis C virus infection sensitizes human hepatocytes to TRAIL-induced apoptosis in a caspase 9-dependent manner. J Immunol 2008; 181: 4926-4935.
20. Volkmann X, Cornberg M, Wedemeyer H, Lehner F, Manns MP, Schulze-Osthoff K, et al. Caspase activation is required for antiviral treatment response in chronic hepatitis C virus infection. HEPATOLOGY 2006; 43: 1311-1316.
21. Afford SC, Randhawa S, Eliopoulos AG, Hubscher SG, Young LS, Adams DH. CD40 activation induces apoptosis in cultured human hepatocytes via induction of cell surface fas ligand expression and amplifies fas-mediated hepatocyte death during allograft rejection. J Exp Med 1999; 189: 441-446.
22. Shiraki K, Sugimoto K, Okano H, Wagayama H, Fujikawa K, Yamanaka T, et al. CD40 expression in HCV-associated chronic liver diseases. Int J Mol Med 2006; 18: 559-563.
23. Sugimoto K, Shiraki K, Ito T, Fujikawa K, Takase K, Tameda Y, et al. Expression of functional CD40 in human hepatocellular carcinoma. HEPATOLOGY 1999; 30: 920-926.
24. Zhou F, Ajuebor MN, Beck PL, Le T, Hogaboam CM, Swain MG. CD154-CD40 interactions drive hepatocyte apoptosis in murine fulminant hepatitis. HEPATOLOGY 2005; 42: 372-380.
25. 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.
26. Friebe P, Lohmann V, Krieger N, Bartenschlager R. Sequences in the 5′ nontranslated region of hepatitis C virus required for RNA replication. J Virol 2001; 75: 12047-12057.
27. Krieger N, Lohmann V, Bartenschlager R. Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J Virol 2001; 75: 4614-4624.
28. Kaul A, Woerz I, Meuleman P, Leroux-Roels G, Bartenschlager R. Cell culture adaptation of hepatitis C virus and in vivo viability of an adapted variant. J Virol 2007; 81: 13168-13179.
29. Targett-Adams P, McLauchlan J. Development and characterization of a transient-replication assay for the genotype 2a hepatitis C virus subgenomic replicon. J Gen Virol 2005; 86: 3075-3080.
30. Binder M, Quinkert D, Bochkarova O, Klein R, Kezmic N, Bartenschlager R, et al. Identification of determinants involved in initiation of hepatitis C virus RNA synthesis by using intergenotypic replicase chimeras. J Virol 2007; 81: 5270-5283.
31. Fischer R, Baumert T, Blum HE. Hepatitis C virus infection and apoptosis. World J Gastroenterol 2007; 13: 4865-4872.
32. Ahmed-Choudhury J, Russell CL, Randhawa S, Young LS, Adams DH, Afford SC. Differential induction of nuclear factor-kappaB and activator protein-1 activity after CD40 ligation is associated with primary human hepatocyte apoptosis or intrahepatic endothelial cell proliferation. Mol Biol Cell 2003; 14: 1334-1345.
33. Fischer R, Cariers A, Reinehr R, Haussinger D. Caspase 9-dependent killing of hepatic stellate cells by activated Kupffer cells. Gastroenterology 2002; 123: 845-861.
34. Liu M, Mendicino M, Ning Q, Ghanekar A, He W, McGilvray I, et al. Cytokine-induced hepatic apoptosis is dependent on FGL2/fibroleukin: the role of Sp1/Sp3 and STAT1/PU.1 composite cis elements. J Immunol 2006; 176: 7028-7038.
35. Hazari S, Taylor L, Haque S, Garry RF, Florman S, Luftig R, et al. Reduced expression of Jak-1 and Tyk-2 proteins leads to interferon resistance in hepatitis C virus replicon. Virol J 2007; 4: 89.
36. Park KJ, Choi SH, Choi DH, Park JM, Yie SW, Lee SY, et al. 1Hepatitis C virus NS5A protein modulates c-Jun N-terminal kinase through interaction with tumor necrosis factor receptor-associated factor 2. J Biol Chem 2003; 278: 30711-30718.
37. Ng TI, Mo H, Pilot-Matias T, He Y, Koev G, Krishnan P, et al. Identification of host genes involved in hepatitis C virus replication by small interfering RNA technology. HEPATOLOGY 2007; 45: 1413-1421.
38. Volkmann X, Fischer U, Bahr MJ, Ott M, Lehner F, Macfarlane M, et al. Increased hepatotoxicity of tumor necrosis factor-related apoptosis-inducing ligand in diseased human liver. HEPATOLOGY 2007; 46: 1498-1508.
39. Rehermann B. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J Clin Invest 2009; 119: 1745-1754.
40. Duttagupta PA, Boesteanu AC, Katsikis PD. Costimulation signals for memory CD8+ T cells during viral infections. Crit Rev Immunol 2009; 29: 469-486.
41. Mueller M, Spangenberg HC, Kersting N, Altay T, Blum HE, Klenerman P, et al. Virus-specific CD4+ T cell responses in chronic HCV infection in blood and liver identified by antigen-specific upregulation of CD154. J Hepatol 2010; 52: 800-811.
42. Munroe ME. Functional roles for T cell CD40 in infection and autoimmune disease: the role of CD40 in lymphocyte homeostasis. Semin Immunol 2009; 21: 283-288.
43. Feng X. Regulatory roles and molecular signaling of TNF family members in osteoclasts. Gene 2005; 350: 1-13.