Human stem cell-derived hepatocytes as a model for hepatitis B virus infection, spreading and virus-host interactions

Journal of Hepatology

Volumn 66, Issue 3, 2017, Pages 494-503

  Xia, Yuchen ^a   Carpentier, Arnaud ^a   Cheng, Xiaoming ^a   Block, Peter Daniel ^a   Zhao, Yao ^a   Zhang, Zhensheng ^a   Protzer, Ulrike ^b,c   Liang, T Jake ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c German Center for Infection Research   (Germany)

Author keywords

Antiviral agents; Antivirals; DNA; Hepatitis B virus; Hepatocytes; Model; Stem cell; Viral

Indexed keywords

ANTIVIRUS AGENT; GENISTIN; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B(E) ANTIGEN; PA 452; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; CELL MATURATION; CONTROLLED STUDY; DNA VIRUS; EMBRYO; HEPATITIS B; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; INDUCED PLURIPOTENT STEM CELL; LIVER CELL; PRIORITY JOURNAL; VIRUS CELL INTERACTION; BIOLOGICAL MODEL; CELL CULTURE; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; DRUG DEVELOPMENT; EMBRYONIC STEM CELL; HEPATITIS B VIRUS; HOST PATHOGEN INTERACTION; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; STEM CELL; VIROLOGY; VIRUS REPLICATION;

ANTIVIRAL AGENTS; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; DRUG DISCOVERY; EMBRYONIC STEM CELLS; HEPATITIS B; HEPATITIS B VIRUS; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MODELS, BIOLOGICAL; STEM CELLS; VIRUS REPLICATION;

EID: 85007248127     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2016.10.009     Document Type: Article

References (40)

1. [1] Trepo, C., Chan, H.L., Lok, A., Hepatitis B virus infection. Lancet 384 (2014), 2053–2063.
2. [2] Liang, T.J., Block, T.M., McMahon, B.J., Ghany, M.G., Urban, S., Guo, J.T., et al. Present and future therapies of hepatitis B: From discovery to cure. Hepatology 62 (2015), 1893–1908.
3. [3] Yan, H., Zhong, G., Xu, G., He, W., Jing, Z., Gao, Z., et al. Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. eLife, 1, 2012, e00049.
4. [4] Kock, J., Rosler, C., Zhang, J.J., Blum, H.E., Nassal, M., Thoma, C., Generation of covalently closed circular DNA of hepatitis B viruses via intracellular recycling is regulated in a virus specific manner. PLoS Pathog, 6, 2010, e1001082.
5. [5] Blumberg, B.S., Alter, H.J., Visnich, S., A “New” antigen in leukemia sera. JAMA 191 (1965), 541–546.
6. [6] Hantz, O., Parent, R., Durantel, D., Gripon, P., Guguen-Guillouzo, C., Zoulim, F., Persistence of the hepatitis B virus covalently closed circular DNA in HepaRG human hepatocyte-like cells. J Gen Virol 90 (2009), 127–135.
7. [7] Carpentier, A., Tesfaye, A., Chu, V., Nimgaonkar, I., Zhang, F., Lee, S.B., et al. Engrafted human stem cell-derived hepatocytes establish an infectious HCV murine model. J Clin Invest 124 (2014), 4953–4964.
8. [8] Carpentier, A., Nimgaonkar, I., Chu, V., Xia, Y., Hu, Z., Liang, T.J., Hepatic differentiation of human pluripotent stem cells in miniaturized format suitable for high-throughput screen. Stem Cell Res 16 (2016), 640–650.
9. [9] Gripon, P., Rumin, S., Urban, S., Le Seyec, J., Glaise, D., Cannie, I., et al. Infection of a human hepatoma cell line by hepatitis B virus. Proc Natl Acad Sci USA 99 (2002), 15655–15660.
10. [10] Shlomai, A., Schwartz, R.E., Ramanan, V., Bhatta, A., de Jong, Y.P., Bhatia, S.N., et al. Modeling host interactions with hepatitis B virus using primary and induced pluripotent stem cell-derived hepatocellular systems. Proc Natl Acad Sci USA 111 (2014), 12193–12198.
11. [11] Konig, A., Doring, B., Mohr, C., Geipel, A., Geyer, J., Glebe, D., Kinetics of the bile acid transporter and hepatitis B virus receptor Na+/taurocholate cotransporting polypeptide (NTCP) in hepatocytes. J Hepatol 61 (2014), 867–875.
12. [12] Gripon, P., Cannie, I., Urban, S., Efficient inhibition of hepatitis B virus infection by acylated peptides derived from the large viral surface protein. J Virol 79 (2005), 1613–1622.
13. [13] Langley, D.R., Walsh, A.W., Baldick, C.J., Eggers, B.J., Rose, R.E., Levine, S.M., et al. Inhibition of hepatitis B virus polymerase by entecavir. J Virol 81 (2007), 3992–4001.
14. [14] Lucifora, J., Xia, Y., Reisinger, F., Zhang, K., Stadler, D., Cheng, X., et al. Specific and nonhepatotoxic degradation of nuclear hepatitis B virus cccDNA. Science 343 (2014), 1221–1228.
15. [15] Xia, Y., Stadler, D., Lucifora, J., Reisinger, F., Webb, D., Hosel, M., et al. Interferon-gamma and tumor necrosis factor-alpha produced by T cells reduce the HBV persistence form, cccDNA, without cytolysis. Gastroenterology 150 (2016), 194–205.
16. [16] Gripon, P., Diot, C., Theze, N., Fourel, I., Loreal, O., Brechot, C., et al. Hepatitis B virus infection of adult human hepatocytes cultured in the presence of dimethyl sulfoxide. J Virol 62 (1988), 4136–4143.
17. [17] Allweiss, L., Dandri, M., Experimental in vitro and in vivo models for the study of human hepatitis B virus infection. J Hepatol 64 (2016), S17–S31.
18. [18] Heslop, J.A., Rowe, C., Walsh, J., Sison-Young, R., Jenkins, R., Kamalian, L., et al. Mechanistic evaluation of primary human hepatocyte culture using global proteomic analysis reveals a selective dedifferentiation profile. Arch Toxicol, 2016.
19. [19] Tuttleman, J.S., Pourcel, C., Summers, J., Formation of the pool of covalently closed circular viral DNA in hepadnavirus-infected cells. Cell 47 (1986), 451–460.
20. [20] Petersen, J., Dandri, M., Mier, W., Lutgehetmann, M., Volz, T., von Weizsacker, F., et al. Prevention of hepatitis B virus infection in vivo by entry inhibitors derived from the large envelope protein. Nat Biotechnol 26 (2008), 335–341.
21. [21] Asabe, S., Wieland, S.F., Chattopadhyay, P.K., Roederer, M., Engle, R.E., Purcell, R.H., et al. The size of the viral inoculum contributes to the outcome of hepatitis B virus infection. J Virol 83 (2009), 9652–9662.
22. [22] Wang, S.H., Yeh, S.H., Lin, W.H., Yeh, K.H., Yuan, Q., Xia, N.S., et al. Estrogen receptor alpha represses transcription of HBV genes via interaction with hepatocyte nuclear factor 4alpha. Gastroenterology 142 (2012), 989–998, e984.
23. [23] Martin, P.M., Horwitz, K.B., Ryan, D.S., McGuire, W.L., Phytoestrogen interaction with estrogen receptors in human breast cancer cells. Endocrinology 103 (1978), 1860–1867.
24. [24] Huan, B., Kosovsky, M.J., Siddiqui, A., Retinoid X receptor alpha transactivates the hepatitis B virus enhancer 1 element by forming a heterodimeric complex with the peroxisome proliferator-activated receptor. J Virol 69 (1995), 547–551.
25. [25] Liu, Y., Kagechika, H., Ishikawa, J., Hirano, H., Matsukuma, S., Tanaka, K., et al. Effects of retinoic acids on the dendritic morphology of cultured hippocampal neurons. J Neurochem 106 (2008), 1104–1116.
26. [26] Sells, M.A., Chen, M.L., Acs, G., Production of hepatitis B virus particles in Hep G2 cells transfected with cloned hepatitis B virus DNA. Proc Natl Acad Sci USA 84 (1987), 1005–1009.
27. [27] Delaney, W.E., Isom, H.C., Hepatitis B virus replication in human HepG2 cells mediated by hepatitis B virus recombinant baculovirus. Hepatology 28 (1998), 1134–1146.
28. [28] Sprinzl, M.F., Oberwinkler, H., Schaller, H., Protzer, U., Transfer of hepatitis B virus genome by adenovirus vectors into cultured cells and mice: crossing the species barrier. J Virol 75 (2001), 5108–5118.
29. [29] Iwamoto, M., Watashi, K., Tsukuda, S., Aly, H.H., Fukasawa, M., Fujimoto, A., et al. Evaluation and identification of hepatitis B virus entry inhibitors using HepG2 cells overexpressing a membrane transporter NTCP. Biochem Biophys Res Commun 443 (2014), 808–813.
30. [30] Fraczek, J., Bolleyn, J., Vanhaecke, T., Rogiers, V., Vinken, M., Primary hepatocyte cultures for pharmaco-toxicological studies: at the busy crossroad of various anti-dedifferentiation strategies. Arch Toxicol 87 (2013), 577–610.
31. [31] Zeisberg, M., Kramer, K., Sindhi, N., Sarkar, P., Upton, M., Kalluri, R., De-differentiation of primary human hepatocytes depends on the composition of specialized liver basement membrane. Mol Cell Biochem 283 (2006), 181–189.
32. [32] Elaut, G., Henkens, T., Papeleu, P., Snykers, S., Vinken, M., Vanhaecke, T., et al. Molecular mechanisms underlying the dedifferentiation process of isolated hepatocytes and their cultures. Curr Drug Metab 7 (2006), 629–660.
33. [33] Godoy, P., Hengstler, J.G., Ilkavets, I., Meyer, C., Bachmann, A., Muller, A., et al. Extracellular matrix modulates sensitivity of hepatocytes to fibroblastoid dedifferentiation and transforming growth factor beta-induced apoptosis. Hepatology 49 (2009), 2031–2043.
34. [34] Funk, A., Hohenberg, H., Mhamdi, M., Will, H., Sirma, H., Spread of hepatitis B viruses in vitro requires extracellular progeny and may be codetermined by polarized egress. J Virol 78 (2004), 3977–3983.
35. [35] Schulze, A., Mills, K., Weiss, T.S., Urban, S., Hepatocyte polarization is essential for the productive entry of the hepatitis B virus. Hepatology 55 (2012), 373–383.
36. [36] Tong, S., Li, J., Wands, J.R., Carboxypeptidase D is an avian hepatitis B virus receptor. J Virol 73 (1999), 8696–8702.
37. [37] Dandri, M., Petersen, J., Chimeric mouse model of hepatitis B virus infection. J Hepatol 56 (2012), 493–495.
38. [38] Gieseck, R.L. 3rd, Hannan, N.R., Bort, R., Hanley, N.A., Drake, R.A., Cameron, G.W., et al. Maturation of induced pluripotent stem cell derived hepatocytes by 3D-culture. PLoS One, 9, 2014, e86372.
39. [39] Koniger, C., Wingert, I., Marsmann, M., Rosler, C., Beck, J., Nassal, M., Involvement of the host DNA-repair enzyme TDP2 in formation of the covalently closed circular DNA persistence reservoir of hepatitis B viruses. Proc Natl Acad Sci USA 111 (2014), E4244–E4253.
40. [40] Peng, L., Zhao, Q., Li, Q., Li, M., Li, C., Xu, T., et al. The p.Ser267Phe variant in SLC10A1 is associated with resistance to chronic hepatitis B. Hepatology 61 (2015), 1251–1260.