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References
Contents
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[1]AA Evans, WT London, RG Gish, C Cohen, TM Block. Chronic HBV infection outside treatment guidelines: is treatment needed? Antivir Ther 18:229-235 (2013)
[2]JD Yang, LR Roberts. Hepatocellular carcinoma: A global view. Nat Rev Gastroenterol Hepatol 7:448-458 (2010)
[3]WHO. HepC WHO fact sheet 164. http://www.hcvka.de/pdf/HepC%20WHO%20fact%20sheet%20164.pdf. (2011)
[4]P Sun, X Zhou, SL Farnworth, AH Patel, DC Hay. Modeling human liver biology using stem cell-derived hepatocytes. Int J Mol Sci 14:22011-22021 (2013)
[5]K Takahashi, S Yamanaka. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676 (2006)
[6]J Li, W Song, G Pan, J Zhou. Advances in understanding the cell types and approaches used for generating induced pluripotent stem cells. J Hematol Oncol 7:50 (2014)
[7]J Cai, Y Zhao, Y Liu, F Ye, Z Song, H Qin, S Meng, Y Chen, R Zhou, X Song, Y Guo, M Ding, H Deng. Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology 45:1229-1239 (2007)
[8]Y Duan, A Catana, Y Meng, N Yamamoto, S He, S Gupta, SS Gambhir, MA Zern. Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo. Stem Cells 25:3058-3068 (2007)
[9]DC Hay, J Fletcher, C Payne, JD Terrace, RC Gallagher, J Snoeys, JR Black, D Wojtacha, K Samuel, Z Hannoun, A Pryde, C Filippi, IS Currie, SJ Forbes, JA Ross, PN Newsome, JP Iredale. Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc Natl Acad Sci U S A 105:12301-12306 (2008)
[10]ST Rashid, S Corbineau, N Hannan, SJ Marciniak, E Miranda, G Alexander, I Huang-Doran, J Griffin, L Ahrlund-Richter, J Skepper, R Semple, A Weber, DA Lomas, L Vallier. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J Clin Invest 120:3127-3136 (2010)
[11]K Si-Tayeb, FK Noto, M Nagaoka, J Li, MA Battle, C Duris, PE North, S Dalton, SA Duncan. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51:297-305 (2010)
[12]RL Gieseck 3rd, NR Hannan, R Bort, NA Hanley, RA Drake, GW Cameron, TA Wynn, L Vallier. Maturation of induced pluripotent stem cell derived hepatocytes by 3D-culture. PLoS One 9:e86372 (2014)
[13]V Lohmann, F Korner, J Koch, U Herian, L Theilmann, R Bartenschlager. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-113 (1999)
[14]B Bartosch, J Dubuisson, FL Cosset. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 197:633-642 (2003)
[15]T Wakita, T Pietschmann, T Kato, T Date, M Miyamoto, Z Zhao, K Murthy, A Habermann, HG Krausslich, M Mizokami, R Bartenschlager, TJ Liang. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791-796 (2005)
[16]J Zhong, P Gastaminza, G Cheng, S Kapadia, T Kato, DR Burton, SF Wieland, SL Uprichard, T Wakita, FV Chisari. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102:9294-9299 (2005)
[17]BD Lindenbach, MJ Evans, AJ Syder, B Wolk, TL Tellinghuisen, CC Liu, T Maruyama, RO Hynes, DR Burton, JA McKeating, CM Rice. Complete replication of hepatitis C virus in cell culture. Science 309:623-626 (2005)
[18]JM Berke, D Moradpour. Hepatitis C virus comes full circle: production of recombinant infectious virus in tissue culture. Hepatology 42:1264-1269 (2005)
[19]T Pietschmann, A Kaul, G Koutsoudakis, A Shavinskaya, S Kallis, E Steinmann, K Abid, F Negro, M Dreux, FL Cosset, R Bartenschlager. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci U S A 103:7408-7413 (2006)
[20]A Kaul, I Woerz, P Meuleman, G Leroux-Roels, R Bartenschlager. Cell culture adaptation of hepatitis C virus and in vivo viability of an adapted variant. J Virol 81:13168-13179 (2007)
[21]T Pietschmann, M Zayas, P Meuleman, G Long, N Appel, G Koutsoudakis, S Kallis, G Leroux-Roels, V Lohmann, R Bartenschlager. Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations. PLoS Pathog 5:e1000475 (2009)
[22]E Steinmann, T Pietschmann. Cell culture systems for hepatitis C virus. Curr Top Microbiol Immunol 369:17-48 (2013)
[23]R Bartenschlager, T Pietschmann. Efficient hepatitis C virus cell culture system: what a difference the host cell makes. Proc Natl Acad Sci U S A 102:9739-9740 (2005)
[24]K Melen, P Keskinen, A Lehtonen, I Julkunen. Interferon-induced gene expression and signaling in human hepatoma cell lines. J Hepatol 33:764-772 (2000)
[25]K Banaudha, JM Orenstein, T Korolnek, GC St Laurent 3rd, T Wakita, A Kumar. Primary hepatocyte culture supports hepatitis C virus replication: a model for infection-associated hepatocarcinogenesis. Hepatology 51:1922-1932 (2010)
[26]C Gondeau, P Briolotti, F Razafy, C Duret, PA Rubbo, F Helle, T Reme, MP Ripault, J Ducos, JM Fabre, J Ramos, EI Pecheur, D Larrey, P Maurel, M Daujat-Chavanieu. In vitro infection of primary human hepatocytes by HCV-positive sera: insights on a highly relevant model. Gut (2013)
[27]J Dias, M Gumenyuk, H Kang, M Vodyanik, J Yu, JA Thomson, II Slukvin. Generation of red blood cells from human induced pluripotent stem cells. Stem Cells Dev 20:1639-1647 (2011)
[28]C Terry, RD Hughes, RR Mitry, SC Lehec, A Dhawan. Cryopreservation-induced nonattachment of human hepatocytes: role of adhesion molecules. Cell Transplant 16:639-647 (2007)
[29]S Marukian, L Andrus, TP Sheahan, CT Jones, ED Charles, A Ploss, CM Rice, LB Dustin. Hepatitis C virus induces interferon-lambda and interferon-stimulated genes in primary liver cultures. Hepatology 54:1913-1923 (2011)
[30]O Hantz, R Parent, D Durantel, P Gripon, C Guguen-Guillouzo, F Zoulim. Persistence of the hepatitis B virus covalently closed circular DNA in HepaRG human hepatocyte-like cells. J Gen Virol 90:127-135 (2009)
[31]H Yan, G Zhong, G Xu, W He, Z Jing, Z Gao, Y Huang, Y Qi, B Peng, H Wang, L Fu, M Song, P Chen, W Gao, B Ren, Y Sun, T Cai, X Feng, J Sui, W Li. Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. Elife 3 (2014)
[32]SL Christian, TW Collier, D Zu, M Licursi, CM Hough, K Hirasawa. Activated Ras/MEK inhibits the antiviral response of alpha interferon by reducing STAT2 levels. J Virol 83:6717-6726 (2009)
[33]YT sukada, K Miyazawa, N Kitamura. High intensity ERK signal mediates hepatocyte growth factor-induced proliferation inhibition of the human hepatocellular carcinoma cell line HepG2. J Biol Chem 276:40968-40976 (2001)
[34]D Yang, C Zuo, X Wang, X Meng, B Xue, N Liu, R Yu, Y Qin, Y Gao, Q Wang, J Hu, L Wang, Z Zhou, B Liu, D Tan, Y Guan, H Zhu. Complete replication of hepatitis B virus and hepatitis C virus in a newly developed hepatoma cell line. Proc Natl Acad Sci U S A 111:E1264-1273 (2014)
[35]P Gripon, C Diot, N Theze, I Fourel, O Loreal, C Brechot, C Guguen-Guillouzo. Hepatitis B virus infection of adult human hepatocytes cultured in the presence of dimethyl sulfoxide. J Virol 62:4136-4143 (1988)
[36]P Gripon, C Diot, C Guguen-Guillouzo. Reproducible high level infection of cultured adult human hepatocytes by hepatitis B virus: effect of polyethylene glycol on adsorption and penetration. Virology 192:534-540 (1993)
[37]A Shlomai, RE Schwartz, V Ramanan, A Bhatta, YP de Jong, SN Bhatia, CM Rice. Modeling host interactions with hepatitis B virus using primary and induced pluripotent stem cell-derived hepatocellular systems. Proc Natl Acad Sci U S A 111:12193-12198 (2014)
[38]D Kremsdorf, N Brezillon. New animal models for hepatitis C viral infection and pathogenesis studies. World J Gastroenterol 13:2427-2435 (2007)
[39]E Billerbeck, Y de Jong, M Dorner, C de la Fuente, A Ploss. Animal models for hepatitis C. Curr Top Microbiol Immunol 369:49-86 (2013)
[40]JL Heckel, EP Sandgren, JL Degen, RD Palmiter, RL Brinster. Neonatal bleeding in transgenic mice expressing urokinase-type plasminogen activator. Cell 62:447-456 (1990)
[41]M Grompe, M al-Dhalimy, M Finegold, CN Ou, T Burlingame, NG Kennaway, P Soriano. Loss of fumarylacetoacetate hydrolase is responsible for the neonatal hepatic dysfunction phenotype of lethal albino mice. Genes Dev 7:2298-2307 (1993)
[42]L Sandmann, A Ploss. Barriers of hepatitis C virus interspecies transmission. Virology 435:70-80 (2013)
[43]Z Song, J Cai, Y Liu, D Zhao, J Yong, S Duo, X Song, Y Guo, Y Zhao, H Qin, X Yin, C Wu, J Che, S Lu, M Ding, H Deng. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res 19:1233-1242 (2009)
[44]T Touboul, NR Hannan, S Corbineau, A Martinez, C Martinet, S Branchereau, S Mainot, H Strick-Marchand, R Pedersen, J Di Santo, A Weber, L Vallier. Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology 51:1754-1765 (2010)
[45]J Ge D, Fellay, AJ Thompson, JS Simon, KV Shianna, TJ Urban, EL Heinzen, P Qiu, AH Bertelsen, AJ Muir, M Sulkowski, JG McHutchison, DB Goldstein. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461:399-401 (2009)
[46]MA Feitelson, RH Miller. X gene-related sequences in the core gene of duck and heron hepatitis B viruses. Proc Natl Acad Sci U S A 85:6162-6166 (1988)
[47]T Yoshida, K Takayama, M Kondoh, F Sakurai, H Tani, N Sakamoto, Y Matsuura, H Mizuguchi, K Yagi. Use of human hepatocyte-like cells derived from induced pluripotent stem cells as a model for hepatocytes in hepatitis C virus infection. Biochem Biophys Res Commun 416:119-124 (2011)
[48]RE Schwartz, K Trehan, L Andrus, TP Sheahan A, Ploss, SA Duncan, CM Rice, SN Bhatia. Modeling hepatitis C virus infection using human induced pluripotent stem cells. Proc Natl Acad Sci U S A 109:2544-2548 (2012)
[49]X Wu, JM Robotham, E Lee, S Dalton, NM Kneteman, DM Gilbert, H Tang. Productive hepatitis C virus infection of stem cell-derived hepatocytes reveals a critical transition to viral permissiveness during differentiation. PLoS Pathog 8:e1002617 (2012)
[50]X Zhou, P Sun, B Lucendo-Villarin, AG Angus, D Szkolnicka, K Cameron, SL Farnworth, AH Patel, DC Hay. Modulating innate immunity improves hepatitis C virus infection and replication in stem cell-derived hepatocytes. Stem Cell Reports 3:204-214 (2014)
[51]T Takebe, K Sekine, M Enomura, H Koike, M Kimura, T Ogaeri, RR Zhang, Y Ueno, YW Zheng, N Koike, S Aoyama, Y Adachi, H Taniguchi. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499:481-484 (2013)
[52]T Takebe, RR Zhang, H Koike, M Kimura, E Yoshizawa, M Enomura, N Koike, K Sekine, H Taniguchi. Generation of a vascularized and functional human liver from an iPSC-derived organ bud transplant. Nat Protoc 9:396-409 (2014)
[53]A Carpentier, A Tesfaye, V Chu, I Nimgaonkar, F Zhang, SB Lee, SS Thorgeirsson, SM Feinstone, TJ Liang. Engrafted human stem cell-derived hepatocytes establish an infectious HCV murine model. J Clin Invest 124:4953-4964 (2014)
[54]P Roelandt, S Obeid, J Paeshuyse, J Vanhove, A Van Lommel, Y Nahmias, F Nevens, J Neyts, CM Verfaillie. Human pluripotent stem cell-derived hepatocytes support complete replication of hepatitis C virus. J Hepatol. 57:246-251 (2012)
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Frontiers in Bioscience-Scholar (FBS) is published by IMR Press from Volume 13 Issue 1 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
Modeling of HBV and HCV hepatitis with Hepatocyte-like cells
1 Biobanque de Picardie, CHU Amiens-Picardie, Amiens cedex 1 France
2 Virology Research Unit, EA 4294, Jules Verne University of Picardie, Amiens, France
3 Department of Virology, CBH, CHU Amiens-Picardie, Amiens cedex 1 France
*Author to whom correspondence should be addressed.
Abstract
Chronic liver diseases caused by either hepatitis B or C viruses are a major health problem around the world. Despite major advances accomplished in recent years in understanding the physiology of both viruses using in vitro and/or in vivo models, there is no vaccine for HCV available. Moreover, susceptibility to acute and chronic infection and the response to treatments are different between HBV or HCV infected patients. Crucial information can be collected using a robust cell model that permits the culture of clinical isolates along with the investigation of the virus-host interaction. The recent progress in the field of cell reprogramming and differentiation has opened new opportunities in viral hepatitis research raising the hopes of developing new improved therapeutics. In this review, we discuss current models for hepatitis B and C studies and their limitations, and also the iPSC model, and its relevance to the viral host cell interactions.
Keywords
- iPSC
- Hepatocyte-like cells
- HBV
- HCV
- Differentiation
- Review
References
- [1] AA Evans, WT London, RG Gish, C Cohen, TM Block. Chronic HBV infection outside treatment guidelines: is treatment needed? Antivir Ther 18:229-235 (2013)
- [2] JD Yang, LR Roberts. Hepatocellular carcinoma: A global view. Nat Rev Gastroenterol Hepatol 7:448-458 (2010)
- [3] WHO. HepC WHO fact sheet 164. http://www.hcvka.de/pdf/HepC%20WHO%20fact%20sheet%20164.pdf. (2011)
- [4] P Sun, X Zhou, SL Farnworth, AH Patel, DC Hay. Modeling human liver biology using stem cell-derived hepatocytes. Int J Mol Sci 14:22011-22021 (2013)
- [5] K Takahashi, S Yamanaka. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676 (2006)
- [6] J Li, W Song, G Pan, J Zhou. Advances in understanding the cell types and approaches used for generating induced pluripotent stem cells. J Hematol Oncol 7:50 (2014)
- [7] J Cai, Y Zhao, Y Liu, F Ye, Z Song, H Qin, S Meng, Y Chen, R Zhou, X Song, Y Guo, M Ding, H Deng. Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology 45:1229-1239 (2007)
- [8] Y Duan, A Catana, Y Meng, N Yamamoto, S He, S Gupta, SS Gambhir, MA Zern. Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo. Stem Cells 25:3058-3068 (2007)
- [9] DC Hay, J Fletcher, C Payne, JD Terrace, RC Gallagher, J Snoeys, JR Black, D Wojtacha, K Samuel, Z Hannoun, A Pryde, C Filippi, IS Currie, SJ Forbes, JA Ross, PN Newsome, JP Iredale. Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc Natl Acad Sci U S A 105:12301-12306 (2008)
- [10] ST Rashid, S Corbineau, N Hannan, SJ Marciniak, E Miranda, G Alexander, I Huang-Doran, J Griffin, L Ahrlund-Richter, J Skepper, R Semple, A Weber, DA Lomas, L Vallier. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J Clin Invest 120:3127-3136 (2010)
- [11] K Si-Tayeb, FK Noto, M Nagaoka, J Li, MA Battle, C Duris, PE North, S Dalton, SA Duncan. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51:297-305 (2010)
- [12] RL Gieseck 3rd, NR Hannan, R Bort, NA Hanley, RA Drake, GW Cameron, TA Wynn, L Vallier. Maturation of induced pluripotent stem cell derived hepatocytes by 3D-culture. PLoS One 9:e86372 (2014)
- [13] V Lohmann, F Korner, J Koch, U Herian, L Theilmann, R Bartenschlager. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-113 (1999)
- [14] B Bartosch, J Dubuisson, FL Cosset. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 197:633-642 (2003)
- [15] T Wakita, T Pietschmann, T Kato, T Date, M Miyamoto, Z Zhao, K Murthy, A Habermann, HG Krausslich, M Mizokami, R Bartenschlager, TJ Liang. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791-796 (2005)
- [16] J Zhong, P Gastaminza, G Cheng, S Kapadia, T Kato, DR Burton, SF Wieland, SL Uprichard, T Wakita, FV Chisari. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102:9294-9299 (2005)
- [17] BD Lindenbach, MJ Evans, AJ Syder, B Wolk, TL Tellinghuisen, CC Liu, T Maruyama, RO Hynes, DR Burton, JA McKeating, CM Rice. Complete replication of hepatitis C virus in cell culture. Science 309:623-626 (2005)
- [18] JM Berke, D Moradpour. Hepatitis C virus comes full circle: production of recombinant infectious virus in tissue culture. Hepatology 42:1264-1269 (2005)
- [19] T Pietschmann, A Kaul, G Koutsoudakis, A Shavinskaya, S Kallis, E Steinmann, K Abid, F Negro, M Dreux, FL Cosset, R Bartenschlager. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci U S A 103:7408-7413 (2006)
- [20] A Kaul, I Woerz, P Meuleman, G Leroux-Roels, R Bartenschlager. Cell culture adaptation of hepatitis C virus and in vivo viability of an adapted variant. J Virol 81:13168-13179 (2007)
- [21] T Pietschmann, M Zayas, P Meuleman, G Long, N Appel, G Koutsoudakis, S Kallis, G Leroux-Roels, V Lohmann, R Bartenschlager. Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations. PLoS Pathog 5:e1000475 (2009)
- [22] E Steinmann, T Pietschmann. Cell culture systems for hepatitis C virus. Curr Top Microbiol Immunol 369:17-48 (2013)
- [23] R Bartenschlager, T Pietschmann. Efficient hepatitis C virus cell culture system: what a difference the host cell makes. Proc Natl Acad Sci U S A 102:9739-9740 (2005)
- [24] K Melen, P Keskinen, A Lehtonen, I Julkunen. Interferon-induced gene expression and signaling in human hepatoma cell lines. J Hepatol 33:764-772 (2000)
- [25] K Banaudha, JM Orenstein, T Korolnek, GC St Laurent 3rd, T Wakita, A Kumar. Primary hepatocyte culture supports hepatitis C virus replication: a model for infection-associated hepatocarcinogenesis. Hepatology 51:1922-1932 (2010)
- [26] C Gondeau, P Briolotti, F Razafy, C Duret, PA Rubbo, F Helle, T Reme, MP Ripault, J Ducos, JM Fabre, J Ramos, EI Pecheur, D Larrey, P Maurel, M Daujat-Chavanieu. In vitro infection of primary human hepatocytes by HCV-positive sera: insights on a highly relevant model. Gut (2013)
- [27] J Dias, M Gumenyuk, H Kang, M Vodyanik, J Yu, JA Thomson, II Slukvin. Generation of red blood cells from human induced pluripotent stem cells. Stem Cells Dev 20:1639-1647 (2011)
- [28] C Terry, RD Hughes, RR Mitry, SC Lehec, A Dhawan. Cryopreservation-induced nonattachment of human hepatocytes: role of adhesion molecules. Cell Transplant 16:639-647 (2007)
- [29] S Marukian, L Andrus, TP Sheahan, CT Jones, ED Charles, A Ploss, CM Rice, LB Dustin. Hepatitis C virus induces interferon-lambda and interferon-stimulated genes in primary liver cultures. Hepatology 54:1913-1923 (2011)
- [30] O Hantz, R Parent, D Durantel, P Gripon, C Guguen-Guillouzo, F Zoulim. Persistence of the hepatitis B virus covalently closed circular DNA in HepaRG human hepatocyte-like cells. J Gen Virol 90:127-135 (2009)
- [31] H Yan, G Zhong, G Xu, W He, Z Jing, Z Gao, Y Huang, Y Qi, B Peng, H Wang, L Fu, M Song, P Chen, W Gao, B Ren, Y Sun, T Cai, X Feng, J Sui, W Li. Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. Elife 3 (2014)
- [32] SL Christian, TW Collier, D Zu, M Licursi, CM Hough, K Hirasawa. Activated Ras/MEK inhibits the antiviral response of alpha interferon by reducing STAT2 levels. J Virol 83:6717-6726 (2009)
- [33] YT sukada, K Miyazawa, N Kitamura. High intensity ERK signal mediates hepatocyte growth factor-induced proliferation inhibition of the human hepatocellular carcinoma cell line HepG2. J Biol Chem 276:40968-40976 (2001)
- [34] D Yang, C Zuo, X Wang, X Meng, B Xue, N Liu, R Yu, Y Qin, Y Gao, Q Wang, J Hu, L Wang, Z Zhou, B Liu, D Tan, Y Guan, H Zhu. Complete replication of hepatitis B virus and hepatitis C virus in a newly developed hepatoma cell line. Proc Natl Acad Sci U S A 111:E1264-1273 (2014)
- [35] P Gripon, C Diot, N Theze, I Fourel, O Loreal, C Brechot, C Guguen-Guillouzo. Hepatitis B virus infection of adult human hepatocytes cultured in the presence of dimethyl sulfoxide. J Virol 62:4136-4143 (1988)
- [36] P Gripon, C Diot, C Guguen-Guillouzo. Reproducible high level infection of cultured adult human hepatocytes by hepatitis B virus: effect of polyethylene glycol on adsorption and penetration. Virology 192:534-540 (1993)
- [37] A Shlomai, RE Schwartz, V Ramanan, A Bhatta, YP de Jong, SN Bhatia, CM Rice. Modeling host interactions with hepatitis B virus using primary and induced pluripotent stem cell-derived hepatocellular systems. Proc Natl Acad Sci U S A 111:12193-12198 (2014)
- [38] D Kremsdorf, N Brezillon. New animal models for hepatitis C viral infection and pathogenesis studies. World J Gastroenterol 13:2427-2435 (2007)
- [39] E Billerbeck, Y de Jong, M Dorner, C de la Fuente, A Ploss. Animal models for hepatitis C. Curr Top Microbiol Immunol 369:49-86 (2013)
- [40] JL Heckel, EP Sandgren, JL Degen, RD Palmiter, RL Brinster. Neonatal bleeding in transgenic mice expressing urokinase-type plasminogen activator. Cell 62:447-456 (1990)
- [41] M Grompe, M al-Dhalimy, M Finegold, CN Ou, T Burlingame, NG Kennaway, P Soriano. Loss of fumarylacetoacetate hydrolase is responsible for the neonatal hepatic dysfunction phenotype of lethal albino mice. Genes Dev 7:2298-2307 (1993)
- [42] L Sandmann, A Ploss. Barriers of hepatitis C virus interspecies transmission. Virology 435:70-80 (2013)
- [43] Z Song, J Cai, Y Liu, D Zhao, J Yong, S Duo, X Song, Y Guo, Y Zhao, H Qin, X Yin, C Wu, J Che, S Lu, M Ding, H Deng. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res 19:1233-1242 (2009)
- [44] T Touboul, NR Hannan, S Corbineau, A Martinez, C Martinet, S Branchereau, S Mainot, H Strick-Marchand, R Pedersen, J Di Santo, A Weber, L Vallier. Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology 51:1754-1765 (2010)
- [45] J Ge D, Fellay, AJ Thompson, JS Simon, KV Shianna, TJ Urban, EL Heinzen, P Qiu, AH Bertelsen, AJ Muir, M Sulkowski, JG McHutchison, DB Goldstein. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461:399-401 (2009)
- [46] MA Feitelson, RH Miller. X gene-related sequences in the core gene of duck and heron hepatitis B viruses. Proc Natl Acad Sci U S A 85:6162-6166 (1988)
- [47] T Yoshida, K Takayama, M Kondoh, F Sakurai, H Tani, N Sakamoto, Y Matsuura, H Mizuguchi, K Yagi. Use of human hepatocyte-like cells derived from induced pluripotent stem cells as a model for hepatocytes in hepatitis C virus infection. Biochem Biophys Res Commun 416:119-124 (2011)
- [48] RE Schwartz, K Trehan, L Andrus, TP Sheahan A, Ploss, SA Duncan, CM Rice, SN Bhatia. Modeling hepatitis C virus infection using human induced pluripotent stem cells. Proc Natl Acad Sci U S A 109:2544-2548 (2012)
- [49] X Wu, JM Robotham, E Lee, S Dalton, NM Kneteman, DM Gilbert, H Tang. Productive hepatitis C virus infection of stem cell-derived hepatocytes reveals a critical transition to viral permissiveness during differentiation. PLoS Pathog 8:e1002617 (2012)
- [50] X Zhou, P Sun, B Lucendo-Villarin, AG Angus, D Szkolnicka, K Cameron, SL Farnworth, AH Patel, DC Hay. Modulating innate immunity improves hepatitis C virus infection and replication in stem cell-derived hepatocytes. Stem Cell Reports 3:204-214 (2014)
- [51] T Takebe, K Sekine, M Enomura, H Koike, M Kimura, T Ogaeri, RR Zhang, Y Ueno, YW Zheng, N Koike, S Aoyama, Y Adachi, H Taniguchi. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499:481-484 (2013)
- [52] T Takebe, RR Zhang, H Koike, M Kimura, E Yoshizawa, M Enomura, N Koike, K Sekine, H Taniguchi. Generation of a vascularized and functional human liver from an iPSC-derived organ bud transplant. Nat Protoc 9:396-409 (2014)
- [53] A Carpentier, A Tesfaye, V Chu, I Nimgaonkar, F Zhang, SB Lee, SS Thorgeirsson, SM Feinstone, TJ Liang. Engrafted human stem cell-derived hepatocytes establish an infectious HCV murine model. J Clin Invest 124:4953-4964 (2014)
- [54] P Roelandt, S Obeid, J Paeshuyse, J Vanhove, A Van Lommel, Y Nahmias, F Nevens, J Neyts, CM Verfaillie. Human pluripotent stem cell-derived hepatocytes support complete replication of hepatitis C virus. J Hepatol. 57:246-251 (2012)
