Transmitted/founder hepatitis c viruses induce cell-type- and genotype-specific differences in innate signaling within the liver

mBio

Volumn 6, Issue 2, 2015, Pages

  Mitchell, Angela M ^a   Stone, Amy E L ^a   Cheng, Linling ^a   Ballinger, Kimberly ^b   Edwards, Michael G ^c   Stoddard, Mark ^d   Li, Hui ^d   Golden Mason, Lucy ^a   Shaw, George M ^d   Khetani, Salman ^b   Rosen, Hugo R ^a,e  

^a UNIVERSITY OF COLORADO   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTERFERON; INTERLEUKIN 28A; INTERLEUKIN 29; RETINOIC ACID INDUCIBLE PROTEIN I; STAT1 PROTEIN; TOLL LIKE RECEPTOR 3; VIRUS RNA; INTERFERON;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL LINE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GEN22 CELL LINE; GENOTYPE; HEPATITIS C VIRUS; HEPG2 CELL LINE; HUH 751 CELL LINE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; LIVER; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; RIG I GENE; SIGNAL TRANSDUCTION; THP 1 CELL LINE; TMNK 1 CELL LINE; UPREGULATION; VIRUS GENE; VIRUS REPLICATION; BIOSYNTHESIS; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; HEPACIVIRUS; HEPATITIS C; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; VIROLOGY;

HEPACIVIRUS; HEPATITIS C VIRUS;

CELL LINE; GENE EXPRESSION PROFILING; GENOTYPE; HEPACIVIRUS; HEPATITIS C; HUMANS; INTERFERONS; LIVER; MOLECULAR SEQUENCE DATA; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84929492696     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02510-14     Document Type: Article

References (46)

1. Rosen HR. 2013. Emerging concepts in immunity to hepatitis C virus infection. J Clin Invest 123:4121–4130.http://dx.doi.org/10.1172/JCI67714.
2. Li H, Stoddard MB, Wang S, Blair LM, Giorgi EE, Parrish EH, Learn GH, Hraber P, Goepfert PA, Saag MS, Denny TN, Haynes BF, Hahn BH, Ribeiro RM, Perelson AS, Korber BT, Bhattacharya T, Shaw GM. 2012. Elucidation of hepatitis C virus transmission and early diversification by single genome sequencing. PLoS Pathog 8:e1002880.http://dx.doi.org/10.1371/journal.ppat.1002880.
3. Au JS, Pockros PJ. 2014. Novel therapeutic approaches for hepatitis C. Clin Pharmacol Ther 95:78–88.http://dx.doi.org/10.1038/clpt.2013.206.
4. Racanelli V, Manigold T. 2007. Presentation of HCV antigens to naive CD8_T cells: why the where, when, what and how are important for virus control and infection outcome. Clin Immunol 124:5–12.http://dx.doi.org/10.1016/j.clim.2007.04.009.
5. Negash AA, Ramos HJ, Crochet N, Lau DT, Doehle B, Papic N, Delker DA, Jo J, Bertoletti A, Hagedorn CH, Gale M, Jr. 2013. IL-1beta production through the nlrp3 inflammasome by hepatic macrophages links hepatitis C virus infection with liver inflammation and disease. PLoS Pathog 9:e1003330.http://dx.doi.org/10.1371/journal.ppat.1003330.
6. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, Wei X, Jiang C, Kirchherr JL, Gao F, Anderson JA, Ping LH, Swanstrom R, Tomaras GD, Blattner WA, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Cohen MS, Montefiori DC, Haynes BF, Gaschen B, Athreya GS, Lee HY, Wood N, Seoighe C, Perelson AS, Bhattacharya T, Korber BT, Hahn BH, Shaw GM. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105:7552–7557.http://dx.doi.org/10.1073/pnas.0802203105.
7. Parrish NF, Gao F, Li H, Giorgi EE, Barbian HJ, Parrish EH, Zajic L, Iyer SS, Decker JM, Kumar A, Hora B, Berg A, Cai F, Hopper J, Denny TN, Ding H, Ochsenbauer C, Kappes JC, Galimidi RP, West AP, Jr, Bjorkman PJ, Wilen CB, Doms RW, O’Brien M, Bhardwaj N, Borrow P, Haynes BF, Muldoon M, Theiler JP, Korber B, Shaw GM, Hahn BH. 2013. Phenotypic properties of transmitted founder HIV-1. Proc Natl Acad Sci U S A 110:6626–6633.http://dx.doi.org/10.1073/pnas.1304288110.
8. Stoddard MB, Li H, Wang S, Saeed M, Andrus L, Ding W, Jiang X, Learn GH, von Schaewen M, Wen J, Goepfert PA, Hahn BH, Ploss A, Rice CM, Shaw GM. 2015. Identification, molecular cloning, and analysis of full-length hepatitis C virus transmitted/founder genotypes 1, 3, and 4. MBio 6(1):e02518-14.http://dx.doi.org/10.1128/mBio.02518-14.
9. Bartenschlager R, Pietschmann T. 2005. Efficient hepatitis C virus cell culture system: what a difference the host cell makes. Proc Natl Acad Sci U S A 102:9739–9740.http://dx.doi.org/10.1073/pnas.0504296102.
10. 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.
11. Ganesan LP, Mohanty S, Kim J, Clark KR, Robinson JM, Anderson CL. 2011. Rapid and efficient clearance of blood-borne virus by liver sinusoidal endothelium. PLoS Pathog 7:e1002281.http://dx.doi.org/10.1371/journal.ppat.1002281.
12. Matsumura T, Takesue M, Westerman KA, Okitsu T, Sakaguchi M, Fukazawa T, Totsugawa T, Noguchi H, Yamamoto S, Stolz DB, Tanaka N, Leboulch P, Kobayashi N. 2004. Establishment of an immortalized human-liver endothelial cell line with SV40T and hTERT. Transplant 77: 1357–1365.http://dx.doi.org/10.1097/01.TP.0000124286.82961.7E.
13. Lande R, Gilliet M. 2010. Plasmacytoid dendritic cells: key players in the initiation and regulation of immune responses. Ann N Y Acad Sci 1183: 89–103.http://dx.doi.org/10.1111/j.1749-6632.2009.05152.x.
14. 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.
15. Stone AE, Giugliano S, Schnell G, Cheng L, Leahy KF, Golden-Mason L, Gale M, Jr, Rosen HR. 2013. Hepatitis C virus pathogen associated molecular pattern (PAMP) triggers production of lambda-interferons by human plasmacytoid dendritic cells. PLoS Pathog. 9:e1003316.http://dx.doi.org/10.1371/journal.ppat.1003316.
16. Chaperot L, Blum A, Manches O, Lui G, Angel J, Molens JP, Plumas J. 2006. Virus or TLR agonists induce TRAIL-mediated cytotoxic activity of plasmacytoid dendritic cells. J Immunol 176:248–255.http://dx.doi.org/10.4049/jimmunol.176.1.248.
17. Lehmann M, Meyer MF, Monazahian M, Tillmann HL, Manns MP, Wedemeyer H. 2004. High rate of spontaneous clearance of acute hepatitis C virus genotype 3 infection. J Med Virol 73:387–391.http://dx.doi.org/10.1002/jmv.20103.
18. Pol S, Vallet-Pichard A, Corouge M. 2014. Treatment of hepatitis C virus genotype 3-infection. Liver Int 34(Suppl 1):18–23.http://dx.doi.org/10.1111/liv.12405.
19. Archer KJ, Mas VR, David K, Maluf DG, Bornstein K, Fisher RA. 2009. Identifying genes for establishing a multigenic test for hepatocellular carcinoma surveillance in hepatitisCvirus-positive cirrhotic patients. Cancer Epidemiol Biomarkers Prev 18:2929–2932.http://dx.doi.org/10.1158/1055-9965.EPI-09-0767.
20. Vollmar B, Menger MD. 2009. The hepatic microcirculation: mechanistic contributions and therapeutic targets in liver injury and repair. Physiol Rev 89:1269–1339.http://dx.doi.org/10.1152/physrev.00027.2008.
21. Giugliano S, Kriss M, Golden-Mason L, Dobrinskikh E, Stone AE, Soto-Gutierrez A, Mitchell A, Khetani SR, Yamane D, Stoddard M, Li H, Shaw GM, Edwards MG, Lemon SM, Gale M, Jr, Shah VH, Rosen HR. 4 November 2014. Hepatitis C virus infection induces autocrine interferon signaling by human liver endothelial cell and release of exo- somes, which inhibits viral replication. Gastroenterology http://dx.doi.org/10.1053/j.gastro.2014.10.040.
22. Khetani SR, Kanchagar C, Ukairo O, Krzyzewski S, Moore A, Shi J, Aoyama S, Aleo M, Will Y. 2013. Use of micropatterned cocultures to detect compounds that cause drug-induced liver injury in humans. Toxicol Sci 132:107–117.http://dx.doi.org/10.1093/toxsci/kfs326.
23. Ingram JL, Antao-Menezes A, Mangum JB, Lyght O, Lee PJ, Elias JA, Bonner JC. 2006. Opposing actions of Stat1 and Stat6 on IL-13-induced up-regulation of early growth response-1 and platelet-derived growth factor ligands in pulmonary fibroblasts. J Immunol 177:4141–4148.http://dx.doi.org/10.4049/jimmunol.177.6.4141.
24. Kumagai Y, Kumar H, Koyama S, Kawai T, Takeuchi O, Akira S. 2009. Cutting edge: TLR-dependent viral recognition along with type I IFN positive feedback signaling masks the requirement of viral replication for IFN-_ production in plasmacytoid dendritic cells. J Immunol 182: 3960–3964.http://dx.doi.org/10.4049/jimmunol.0804315.
25. Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, David M. 2007. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449:919–922.http://dx.doi.org/10.1038/nature06205.
26. Hadziyannis SJ, Sette H, Jr, Morgan TR, Balan V, Diago M, Marcellin P, Ramadori G, Bodenheimer H, Jr, Bernstein D, Rizzetto M, Zeuzem S, Pockros PJ, Lin A, Ackrill AM, PEGASYS International Study Group. 2004. Peginterferon-alpha2a and ribavirin combination therapy in chronic hepatitis C: a randomized study of treatment duration and ribavirin dose. Ann Intern Med 140:346–355.http://dx.doi.org/10.7326/0003-4819-140-5-200403020-00010.
27. Noureddin M, Wright EC, Alter HJ, Clark S, Thomas E, Chen R, Zhao X, Conry-Cantilena C, Kleiner DE, Liang TJ, Ghany MG. 2013. Association of IL28B genotype with fibrosis progression and clinical outcomes in patients with chronic hepatitis C: a longitudinal analysis. Hepatology 58:1548–1557.http://dx.doi.org/10.1002/hep.26506.
28. Bochud PY, Bibert S, Kutalik Z, Patin E, Guergnon J, Nalpas B, Goossens N, Kuske L, Müllhaupt B, Gerlach T, Heim MH, Moradpour D, Cerny A, Malinverni R, Regenass S, Dollenmaier G, Hirsch H, Martinetti G, Gorgiewski M, Bourlière M, Poynard T, Theodorou I, Abel L, Pol S, Dufour JF, Negro F, Swiss Hepatitis C Cohort Study Group, ANRS HC EP 26 Genoscan Study Group. 2012. IL28B alleles associated with poor hepatitis C virus (HCV) clearance protect against inflammation and fibrosis in patients infected with non-1 HCV genotypes. Hepatology 55:384–394.http://dx.doi.org/10.1002/hep.24678.
29. Bochud PY, Cai T, Overbeck K, Bochud M, Dufour JF, Mullhaupt B, Borovicka J, Heim M, Moradpour D, Cerny A, Malinverni R, Francioli P, Negro F, Swiss Hepatitis C Cohort Study Group. 2009. Genotype 3 is associated with accelerated fibrosis progression in chronic hepatitis C. J Hepatol 51:655–666.http://dx.doi.org/10.1016/j.jhep.2009.05.016.
30. Goossens N, Negro F. 2014. Is genotype 3 of the hepatitis C virus the new villain? Hepatology 59:2403–2412.http://dx.doi.org/10.1002/hep.26905.
31. Probst A, Dang T, Bochud M, Egger M, Negro F, Bochud PY. 2011. Role of hepatitis C virus genotype 3 in liver fibrosis progression—a systematic review and meta-analysis. J Viral Hepat 18:745–759.http://dx.doi.org/10.1111/j.1365-2893.2011.01481.x.
32. Kanwal F, Kramer JR, Ilyas J, Duan Z, El-Serag HB. 2014. HCV genotype 3 is associated with an increased risk of cirrhosis and hepatocellular cancer in a national sample of U.S. veterans with HCV. Hepatology 60:98–105.http://dx.doi.org/10.1002/hep.27095.
33. McMahon BJ, Bruden D, Bruce MG, Livingston S, Christensen C, Homan C, Hennessy TW, Williams J, Sullivan D, Rosen HR, Gretch D. 2010. Adverse outcomes in Alaska natives who recovered from or have chronic hepatitis C infection. Gastroenterology 138:922–931.e1.http://dx.doi.org/10.1053/j.gastro.2009.10.056.
34. van der Meer AJ, Veldt BJ, Feld JJ, Wedemeyer H, Dufour JF, Lammert F, Duarte-Rojo A, Heathcote EJ, Manns MP, Kuske L, Zeuzem S, Hofmann WP, de Knegt RJ, Hansen BE, Janssen HL. 2012. Association between sustained virological response and all-cause mortality among patients with chronic hepatitis C and advanced hepatic fibrosis. JAMA 308: 2584–2593.http://dx.doi.org/10.1001/jama.2012.144878.
35. Metz P, Dazert E, Ruggieri A, Mazur J, Kaderali L, Kaul A, Zeuge U, Windisch MP, Trippler M, Lohmann V, Binder M, Frese M, Bartenschlager R. 2012. Identification of type I and type II interferon-induced effectors controlling hepatitis C virus replication. Hepatology 56: 2082–2093.http://dx.doi.org/10.1002/hep.25908.
36. Brass A, Brenndörfer ED. 2014. The role of chemokines in hepatitis C virus-mediated liver disease. Int J Mol Sci 15:4747–4779.http://dx.doi.org/10.3390/ijms15034747.
37. Negro F. 2010. Hepatitis C virus-induced steatosis: an overview. Dig Dis 28:294–299.http://dx.doi.org/10.1159/000282105.
38. Huang W, Metlakunta A, Dedousis N, Zhang P, Sipula I, Dube JJ, Scott DK, O’Doherty RM. 2010. Depletion of liver Kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance. Diabetes 59:347–357.http://dx.doi.org/10.2337/db09-0016.
39. Li Q, Zou C, Zou C, Han Z, Xiao H, Wei H, Wang W, Zhang L, Zhang X, Tang Q, Zhang C, Tao J, Wang X, Gao X. 2013. MicroRNA-25 functions as a potential tumor suppressor in colon cancer by targeting Smad7. Cancer Lett 335:168–174.http://dx.doi.org/10.1016/j.canlet.2013.02.029.
40. Xin C, Zhang H, Liu Z. 2014. MiR-154 suppresses colorectal cancer cell growth and motility by targeting TLR2. Mol Cell Biochem 387:271–277.http://dx.doi.org/10.1007/s11010-013-1892-3.
41. Zhu C, Shao P, Bao M, Li P, Zhou H, Cai H, Cao Q, Tao L, Meng X, Ju X, Qin C, Li J, Yin C. 2014. miR-154 inhibits prostate cancer cell proliferation by targeting CCND 2. Urol Oncol 32:e39–e16.http://dx.doi.org/10.1016/j.urolonc.2012.11.013.
42. Khetani SR, Bhatia SN. 2008. Microscale culture of human liver cells for drug development. Nat Biotechnol 26:120–126.http://dx.doi.org/10.1038/nbt1361.
43. Rheinwald JG, Green H. 1975. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6:331–343.http://dx.doi.org/10.1016/S0092-8674(75)80001-8.
44. Sui Y, Zhao X, Speed TP, Wu Z. 2009. Background adjustment for DNA microarrays using a database of microarray experiments. J Comput Biol 16:1501–1515.http://dx.doi.org/10.1089/cmb.2009.0063.
45. Krämer A, Green J, Pollard J, Jr, Tugendreich S. 2014. Causal analysis approaches in ingenuity pathway analysis. Bioinformatics 30:523–530.http://dx.doi.org/10.1093/bioinformatics/btt703.
46. Racanelli V, Rehermann B. 2006. The liver as an immunological organ. Hepatology 43(2 Suppl 1):S54–S62.