Efficient virus assembly, but not infectivity, determines the magnitude of hepatitis C virus-induced interferon alpha responses of plasmacytoid dendritic cells

Journal of Virology

Volumn 89, Issue 6, 2015, Pages 3200-3208

  Grabski, Elena ^a   Wappler, Ilka ^a   Pfaender, Stephanie ^a   Steinmann, Eike ^a   Haid, Sibylle ^a   Dzionek, Andrzej ^b   Pietschmann, Thomas ^a   Kalinke, Ulrich ^a  

^a INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^b MILTENYI BIOTEC GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; TOLL LIKE RECEPTOR 7; CORE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIMERIZATION; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTER; GENOTYPE; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; INNATE IMMUNITY; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PURIFICATION; ULTRACENTRIFUGATION; VIRUS ASSEMBLY; VIRUS INFECTIVITY; VIRUS PARTICLE; VIRUS STRAIN; CELL LINE; CHEMISTRY; DENDRITIC CELL; FEMALE; GENETICS; HEPACIVIRUS; HEPATITIS C; IMMUNOLOGY; MALE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; VIROLOGY;

HEPATITIS C VIRUS;

CELL LINE; DENDRITIC CELLS; FEMALE; HEPACIVIRUS; HEPATITIS C; HUMANS; IMMUNITY, INNATE; INTERFERON-ALPHA; MALE; PROTEIN STRUCTURE, TERTIARY; VIRAL CORE PROTEINS; VIRUS ASSEMBLY;

EID: 84923172335     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03229-14     Document Type: Article

References (36)

1. Lavanchy D. 2011. Evolving epidemiology of hepatitis C virus. Clin Microbiol Infect 17:107-115. http://dx.doi.org/10.1111/j.1469-0691.2010 .03432.x.
2. Freeman AJ, Dore GJ, Law MG, Thorpe M, Von Overbeck J, Lloyd AR, Marinos G, Kaldor JM. 2001. Estimating progression to cirrhosis in chronic hepatitis C virus infection. Hepatology 34:809-816. http://dx.doi .org/10.1053/jhep.2001.27831.
3. Afdhal NH, McHutchison JG, Zeuzem S, Mangia A, Pawlotsky JM, Murray JS, Shianna KV, Tanaka Y, Thomas DL, Booth DR, Goldstein DB. 2011. Hepatitis C pharmacogenetics: state of the art in 2010. Hepatology 53:336-345. http://dx.doi.org/10.1002/hep.24052.
4. Heim MH. 2013. 25 years of interferon-based treatment of chronic hepatitis C: an epoch coming to an end. Nat Rev Immunol 13:535-542. http://dx.doi.org/10.1038/nri3463.
5. Nakano T, Lau GM, Sugiyama M, Mizokami M. 2012. An updated analysis of hepatitis C virus genotypes and subtypes based on the complete coding region. Liver Int 32:339-345. http://dx.doi.org/10.1111/j.1478-3231.2011.02684.x.
6. Smith DB, Bukh J, Kuiken C, Muerhoff AS, Rice CM, Stapleton JT, Simmonds P. 2014. Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: Updated criteria and genotype assignment web resource. Hepatology 59:318-327. http://dx.doi.org/10.1002/hep .26744.
7. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172. http://dx.doi.org/10.1038/nature04193.
8. Cheng G, Zhong J, Chisari FV. 2006. Inhibition of dsRNA-induced signaling in hepatitis C virus-infected cells by NS3 protease-dependent and-independent mechanisms. Proc Natl Acad SciUSA103:8499-8504. http://dx.doi.org/10.1073/pnas.0602957103.
9. Li K, Foy E, Ferreon JC, Nakamura M, Ferreon AC, Ikeda M, Ray SC, Gale M, Jr, Lemon SM. 2005. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc Natl Acad Sci U S A 102:2992-2997. http://dx.doi.org/10.1073/pnas.0408824102.
10. Bigger CB, Brasky KM, Lanford RE. 2001. DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J Virol 75:7059-7066. http://dx.doi.org/10.1128/JVI.75.15.7059-7066.2001.
11. Su AI, Pezacki JP, Wodicka L, Brideau AD, Supekova L, Thimme R, Wieland S, Bukh J, Purcell RH, Schultz PG, Chisari FV. 2002. Genomic analysis of the host response to hepatitis C virus infection. Proc Natl Acad Sci U S A 99:15669-15674. http://dx.doi.org/10.1073/pnas.202608199.
12. Barchet W, Cella M, Colonna M. 2005. Plasmacytoid dendritic cells- virus experts of innate immunity. Semin Immunol 17:253-261. http://dx .doi.org/10.1016/j.smim.2005.05.008.
13. Reizis B, Bunin A, Ghosh HS, Lewis KL, Sisirak V. 2011. Plasmacytoid dendritic cells: recent progress and open questions. Annu Rev Immunol 29: 163-183. http://dx.doi.org/10.1146/annurev-immunol-031210-101345.
14. Ulsenheimer A, Gerlach JT, Jung MC, Gruener N, Wachtler M, Backmund M, Santantonio T, Schraut W, Heeg MH, Schirren CA, Zachoval R, Pape GR, Diepolder HM. 2005. Plasmacytoid dendritic cells in acute and chronic hepatitis C virus infection. Hepatology 41:643-651. http://dx .doi.org/10.1002/hep.20592.
15. Lau DT, Fish PM, Sinha M, Owen DM, Lemon SM, Gale M, Jr. 2008. Interferon regulatory factor-3 activation, hepatic interferon-stimulated gene expression, and immune cell infiltration in hepatitis C virus patients. Hepatology 47:799-809. http://dx.doi.org/10.1002/hep.22076.
16. Kanto T, Inoue M, Miyatake H, Sato A, Sakakibara M, Yakushijin T, Oki C, Itose I, Hiramatsu N, Takehara T, Kasahara A, Hayashi N. 2004. Reduced numbers and impaired ability of myeloid and plasmacytoid dendritic cells to polarize T helper cells in chronic hepatitis C virus infection. J Infect Dis 190:1919-1926. http://dx.doi.org/10.1086/425425.
17. Dolganiuc A, Chang S, Kodys K, Mandrekar P, Bakis G, Cormier M, Szabo G. 2006. Hepatitis C virus (HCV) core protein-induced, monocytemediated mechanisms of reduced IFN-alpha and plasmacytoid dendritic cell loss in chronic HCV infection. J Immunol 177:6758-6768. http://dx .doi.org/10.4049/jimmunol.177.10.6758.
18. Wertheimer AM, Bakke A, Rosen HR. 2004. Direct enumeration and functional assessment of circulating dendritic cells in patients with liver disease. Hepatology 40:335-345. http://dx.doi.org/10.1002/hep .20306.
19. Longman RS, Talal AH, Jacobson IM, Rice CM, Albert ML. 2005. Normal functional capacity in circulating myeloid and plasmacytoid dendritic cells in patients with chronic hepatitis C. J Infect Dis 192:497-503. http://dx.doi.org/10.1086/431523.
20. Shiina M, Rehermann B. 2008. Cell culture-produced hepatitis C virus impairs plasmacytoid dendritic cell function. Hepatology 47:385-395. http://dx.doi.org/10.1002/hep.21996.
21. Takahashi K, Asabe S, Wieland S, Garaigorta U, Gastaminza P, Isogawa M, Chisari FV. 2010. Plasmacytoid dendritic cells sense hepatitis C virusinfected cells, produce interferon, and inhibit infection. Proc Natl Acad Sci U S A 107:7431-7436. http://dx.doi.org/10.1073/pnas.1002301107.
22. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Kräusslich HG, Mizokami M. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791-796. http://dx.doi.org/10.1038/nm1268.
23. Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, Steinmann E, Abid K, Negro F, Dreux M, Cosset FL. 2006. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad SciUSA103:7408-7413. http://dx .doi.org/10.1073/pnas.0504877103.
24. Steinmann E, Doerrbecker J, Friesland M, Riebesehl N, Ginkel C, Hillung J, Gentzsch J, Lauber C, Brown R, Frentzen A, Pietschmann T. 2013. Characterization of hepatitis C virus intra-and intergenotypic chimeras reveals a role of the glycoproteins in virus envelopment. J Virol 87:13297-13306. http://dx.doi.org/10.1128/JVI.01708-13.
25. Shavinskaya A, Boulant S, Penin F, McLauchlan J, Bartenschlager R. 2007. The lipid droplet binding domain of hepatitis C virus core protein is a major determinant for efficient virus assembly. J Biol Chem 282:37158-37169. http://dx.doi.org/10.1074/jbc.M707329200.
26. Steinmann E, Brohm C, Kallis S, Bartenschlager R, Pietschmann T. 2008. Efficient trans-encapsidation of hepatitis C virus RNAs into infectious virus-like particles. J Virol 82:7034-7046. http://dx.doi.org/10.1128/JVI.00118-08.
27. Zahn A, Allain JP. 2005. Hepatitis C virus and hepatitis B virus bind to heparin: purification of largely IgG-free virions from infected plasma by heparin chromatography. J Gen Virol 86:677-685. http://dx.doi.org/10 .1099/vir.0.80614-0.
28. Lindenbach BD, Evans MJ, Syder AJ, Wölk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626. http://dx.doi.org/10.1126/science.1114016.
29. Waibler Z, Detje CN, Bell JC, Kalinke U. 2007. Matrix protein mediated shutdown of host cell metabolism limits vesicular stomatitis virusinduced interferon-alpha responses to plasmacytoid dendritic cells. Immunobiology 212:887-894. http://dx.doi.org/10.1016/j.imbio.2007.09 .003.
30. Blight KJ, McKeating JA, Rice CM. 2002. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 76:13001-13014. http://dx.doi.org/10.1128/JVI.76.24.13001-13014 .2002.
31. Bitzegeio J, Bankwitz D, Hueging K, Haid S, Brohm C, Zeisel MB, Herrmann E, Iken M, Ott M, Baumert TF, Pietschmann T. 2010. Adaptation of hepatitisCvirus to mouse CD81 permits infection of mouse cells in the absence of human entry factors. PLoS Pathog 6:e1000978. http://dx.doi.org/10.1371/journal.ppat.1000978.
32. Ahmed M, Mitchell LM, Puckett S, Brzoza-Lewis KL, Lyles DS, Hiltbold EM. 2009. Vesicular stomatitis virus M protein mutant stimulates maturation of Toll-like receptor 7 (TLR7)-positive dendritic cells through TLRdependent and-independent mechanisms. J Virol 83:2962-2975. http://dx.doi.org/10.1128/JVI.02030-08.
33. Appel N, Zayas M, Miller S, Krijnse-Locker J, Schaller T, Friebe P, Kallis S, Engel U, Bartenschlager R. 2008. Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly. PLoS Pathog 4:e1000035. http://dx.doi.org/10.1371/journal .ppat.1000035.
34. Gentzsch J, Brohm C, Steinmann E, Friesland M, Menzel N, Vieyres G, Perin PM, Frentzen A, Kaderali L, Pietschmann T. 2013. Hepatitis C virus p7 is critical for capsid assembly and envelopment. PLoS Pathog 9:e1003355. http://dx.doi.org/10.1371/journal.ppat.1003355.
35. Cocquerel L, Wychowski C, Minner F, Penin F, Dubuisson J. 2000. Charged residues in the transmembrane domains of hepatitis C virus glycoproteins play a major role in the processing, subcellular localization, and assembly of these envelope proteins. J Virol 74:3623-3633. http://dx .doi.org/10.1128/JVI.74.8.3623-3633.2000.
36. Dreux M, Garaigorta U, Boyd B, Decembre E, Chung J, Whitten-Bauer C, Wieland S, Chisari FV. 2012. Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe 12:558-570. http://dx.doi.org/10.1016/j .chom.2012.08.010.