A robust model of natural hepatitis C infection using hepatocyte-like cells derived from human induced pluripotent stem cells as a long-term host

Virology Journal

Volumn 13, Issue 1, 2016, Pages

  Sa ngiamsuntorn, Khanit ^a   Wongkajornsilp, Adisak ^b   Phanthong, Phetcharat ^a   Borwornpinyo, Suparerk ^c   Kitiyanant, Narisorn ^a   Chantratita, Wasun ^d   Hongeng, Suradej ^e  

^a MAHIDOL UNIVERSITY   (Thailand)

^b MAHIDOL UNIVERSITY   (Thailand)

^c Mahidol University   (Thailand)

^d MAHIDOL UNIVERSITY   (Thailand)

^e MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Cell culture model; Cytochrome P450; Differentiation; Drug metabolism; HCV; Hepatitis C virus; Hepatocyte; Hepatocyte like cell; Induced pluripotent stem cell; iPSC; JFH 1

Indexed keywords

ALPHA INTERFERON; ALPHA TOCOPHEROL; CD81 ANTIGEN; CLAUDIN 1; CYTOCHROME P450; INTERLEUKIN 28B; INTERLEUKIN 29; LOW DENSITY LIPOPROTEIN RECEPTOR; MICRORNA 122; OCCLUDIN; RIBAVIRIN; SOFOSBUVIR; TUMOR NECROSIS FACTOR; VIRUS RNA;

ADULT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; HEPATITIS C; HEPATITIS C VIRUS; HEPATITIS C VIRUS GENOTYPE 1A; HEPATITIS C VIRUS GENOTYPE 1B; HEPATITIS C VIRUS GENOTYPE 3A; HEPATITIS C VIRUS GENOTYPE 3B; HEPATITIS C VIRUS GENOTYPE 6F; HEPATITIS C VIRUS GENOTYPE 6N; HOST CELL; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; LIFE CYCLE; LIVER CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION; VIRUS LOAD; VIRUS PARTICLE; VIRUS RELEASE; VIRUS REPLICATION; BIOLOGICAL MODEL; CELL DIFFERENTIATION; GROWTH, DEVELOPMENT AND AGING; HEPACIVIRUS; HOST PATHOGEN INTERACTION; PATHOLOGY; PROCEDURES; VIROLOGY; VIRUS CULTURE;

ADULT; CELL DIFFERENTIATION; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MODELS, BIOLOGICAL; VIRUS CULTIVATION;

EID: 85007583151     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/s12985-016-0519-1     Document Type: Article

References (67)

1. Pawlotsky JM, Chevaliez S, McHutchison JG. The hepatitis C virus life cycle as a target for new antiviral therapies. Gastroenterology. 2007; 132: 1979-98.
2. Simmonds P, Bukh J, Combet C, Deleage G, Enomoto N, Feinstone S, Halfon P, Inchauspe G, Kuiken C, Maertens G, et al. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology. 2005; 42: 962-73.
3. Chisari FV. Unscrambling hepatitis C virus-host interactions. Nature. 2005; 436: 930-2.
4. Yu Y, Fisher JE, Lillegard JB, Rodysill B, Amiot B, Nyberg SL. Cell therapies for liver diseases. Liver Transpl. 2012; 18: 9-21.
5. Joshi D, Pinzani M, Carey I, Agarwal K. Recurrent HCV after liver transplantationmechanisms, assessment and therapy. Nat Rev Gastroenterol Hepatol. 2014; 11: 710-21.
6. Xiao F, Fofana I, Heydmann L, Barth H, Soulier E, Habersetzer F, Doffoel M, Bukh J, Patel AH, Zeisel MB, Baumert TF. Hepatitis C virus cell-cell transmission and resistance to direct-acting antiviral agents. PLoS Pathog. 2014; 10: e1004128.
7. Soltys KA, Soto-Gutierrez A, Nagaya M, Baskin KM, Deutsch M, Ito R, Shneider BL, Squires R, Vockley J, Guha C. Barriers to the successful treatment of liver disease by hepatocyte transplantation. J Hepatol. 2010; 53: 769-74.
8. Jazwinski AB, Muir AJ. Direct-acting antiviral medications for chronic hepatitis C virus infection. Gastroenterol Hepatol (N Y). 2011; 7: 154-62.
9. Halfon P, Locarnini S. Hepatitis C virus resistance to protease inhibitors. J Hepatol. 2011; 55: 192-206.
10. Vinaixa C, Rubin A, Aguilera V, Berenguer M. Recurrence of hepatitis C after liver transplantation. Ann Gastroenterol. 2013; 26: 304-13.
11. Wakita T, Kato T. Development of an Infectious HCV Cell Culture System. In Hepatitis C Viruses: Genomes and Molecular Biology. Edited by Tan SL. Norfolk (UK): Horizon Bioscience; 2006.
12. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, Murthy K, Habermann A, Krausslich HG, Mizokami M, et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med. 2005; 11: 791-6.
13. Catanese MT, Dorner M. Advances in experimental systems to study hepatitis C virus in vitro and in vivo. Virology. 2015; 479-480: 221-33.
14. Bartenschlager R, Pietschmann T. Efficient hepatitis C virus cell culture system: what a difference the host cell makes. Proc Natl Acad Sci U S A. 2005; 102: 9739-40.
15. Blight KJ, McKeating JA, Marcotrigiano J, Rice CM. Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture. J Virol. 2003; 77: 3181-90.
16. Sa-ngiamsuntorn K, Wongkajornsilp A, Kasetsinsombat K, Duangsa-ard S, Nuntakarn L, Borwornpinyo S, Akarasereenont P, Limsrichamrern S, Hongeng S. Upregulation of CYP 450 s expression of immortalized hepatocyte-like cells derived from mesenchymal stem cells by enzyme inducers. BMC Biotechnol. 2011; 11: 89.
17. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, Wieland SF, Uprichard SL, Wakita T, Chisari FV. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A. 2005; 102: 9294-9.
18. Blight KJ, McKeating JA, Rice CM. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol. 2002; 76: 13001-14.
19. Breiman A, Grandvaux N, Lin R, Ottone C, Akira S, Yoneyama M, Fujita T, Hiscott J, Meurs EF. Inhibition of RIG-I-dependent signaling to the interferon pathway during hepatitis C virus expression and restoration of signaling by IKKepsilon. J Virol. 2005; 79: 3969-78.
20. Helle F, Brochot E, Fournier C, Descamps V, Izquierdo L, Hoffmann TW, Morel V, Herpe YE, Bengrine A, Belouzard S, et al. Permissivity of primary human hepatocytes and different hepatoma cell lines to cell culture adapted hepatitis C virus. PLoS One. 2013; 8: e70809.
21. Podevin P, Carpentier A, Pene V, Aoudjehane L, Carriere M, Zaidi S, Hernandez C, Calle V, Meritet JF, Scatton O, et al. Production of infectious hepatitis C virus in primary cultures of human adult hepatocytes. Gastroenterology. 2010; 139: 1355-64.
22. Gondeau C, Briolotti P, Razafy F, Duret C, Rubbo PA, Helle F, Reme T, Ripault MP, Ducos J, Fabre JM, et al. In vitro infection of primary human hepatocytes by HCV-positive sera: insights on a highly relevant model. Gut. 2014; 63: 1490-500.
23. Yu Y, Wang X, Nyberg SL. Potential and Challenges of Induced Pluripotent Stem Cells in Liver Diseases Treatment. J Clin Med. 2014; 3: 997-1017.
24. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126: 663-76.
25. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007; 131: 861-72.
26. Chun YS, Byun K, Lee B. Induced pluripotent stem cells and personalized medicine: current progress and future perspectives. Anat Cell Biol. 2011; 44: 245-55.
27. Schwartz RE, Trehan K, Andrus L, Sheahan TP, Ploss A, Duncan SA, Rice CM, Bhatia SN. Modeling hepatitis C virus infection using human induced pluripotent stem cells. Proc Natl Acad Sci U S A. 2012; 109: 2544-8.
28. Roelandt P, Obeid S, Paeshuyse J, Vanhove J, Van Lommel A, Nahmias Y, Nevens F, Neyts J, Verfaillie CM. Human pluripotent stem cell-derived hepatocytes support complete replication of hepatitis C virus. J Hepatol. 2012; 57: 246-51.
29. Si-Tayeb K, Duclos-Vallee JC, Petit MA. Hepatocyte-like cells differentiated from human induced pluripotent stem cells (iHLCs) are permissive to hepatitis C virus (HCV) infection: HCV study gets personal. J Hepatol. 2012; 57: 689-91.
30. Wu X, Robotham JM, Lee E, Dalton S, Kneteman NM, Gilbert DM, Tang H. Productive hepatitis C virus infection of stem cell-derived hepatocytes reveals a critical transition to viral permissiveness during differentiation. PLoS Pathog. 2012; 8: e1002617.
31. Hannan NR, Segeritz CP, Touboul T, Vallier L. Production of hepatocyte-like cells from human pluripotent stem cells. Nat Protoc. 2013; 8: 430-7.
32. Warlich E, Kuehle J, Cantz T, Brugman MH, Maetzig T, Galla M, Filipczyk AA, Halle S, Klump H, Scholer HR, et al. Lentiviral vector design and imaging approaches to visualize the early stages of cellular reprogramming. Mol Ther. 2011; 19: 782-9.
33. Ulvestad M, Nordell P, Asplund A, Rehnstrom M, Jacobsson S, Holmgren G, Davidson L, Brolen G, Edsbagge J, Bjorquist P, et al. Drug metabolizing enzyme and transporter protein profiles of hepatocytes derived from human embryonic and induced pluripotent stem cells. Biochem Pharmacol. 2013; 86: 691-702.
34. Vieyres G, Pietschmann T. Entry and replication of recombinant hepatitis C viruses in cell culture. Methods. 2013; 59: 233-48.
35. Yu X, Uprichard SL: Cell-based hepatitis C virus infection fluorescence resonance energy transfer (FRET) assay for antiviral compound screening. Curr Protoc Microbiol 2010, Chapter 17: Unit 17 15.
36. Raymond VA, Selliah S, Ethier C, Houle R, Jouan L, Maniere T, Lamarre D, Willems B, Bilodeau M. Primary cultures of human hepatocytes isolated from hepatitis C virus-infected cirrhotic livers as a model to study hepatitis C infection. Liver Int. 2009; 29: 942-9.
37. Zorn AM. Liver development. In StemBook. Cambridge (MA): The Stem Cell Research Community; 2008.
38. Hu A, Shang C, Li Q, Sun N, Wu L, Ma Y, Jiao X, Min J, Zeng G, He X. Epithelial-mesenchymal transition delayed by E-cad to promote tissue formation in hepatic differentiation of mouse embryonic stem cells in vitro. Stem Cells Dev. 2014; 23: 877-87.
39. Touboul T, Hannan NR, Corbineau S, Martinez A, Martinet C, Branchereau S, Mainot S, Strick-Marchand H, Pedersen R, Di Santo J, et al. Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology. 2010; 51: 1754-65.
40. Song Z, Cai J, Liu Y, Zhao D, Yong J, Duo S, Song X, Guo Y, Zhao Y, Qin H, et al. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res. 2009; 19: 1233-42.
41. Chen YF, Tseng CY, Wang HW, Kuo HC, Yang VW, Lee OK. Rapid generation of mature hepatocyte-like cells from human induced pluripotent stem cells by an efficient three-step protocol. Hepatology. 2012; 55: 1193-203.
42. Si-Tayeb K, Noto FK, Nagaoka M, Li J, Battle MA, Duris C, North PE, Dalton S, Duncan SA. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology. 2010; 51: 297-305.
43. Wongkajornsilp A, Sa-Ngiamsuntorn K, Hongeng S. Development of immortalized hepatocyte-like cells from hMSCs. Methods Mol Biol. 2012; 826: 73-87.
44. Zhao D, Chen S, Duo S, Xiang C, Jia J, Guo M, Lai W, Lu S, Deng H. Promotion of the efficient metabolic maturation of human pluripotent stem cell-derived hepatocytes by correcting specification defects. Cell Res. 2013; 23: 157-61.
45. Chistiakov DA, Chistiakov PA. Strategies to produce hepatocytes and hepatocyte-like cells from pluripotent stem cells. Hepatol Res. 2012; 42: 111-9.
46. Du Y, Wang J, Jia J, Song N, Xiang C, Xu J, Hou Z, Su X, Liu B, Jiang T, et al. Human hepatocytes with drug metabolic function induced from fibroblasts by lineage reprogramming. Cell Stem Cell. 2014; 14: 394-403.
47. Sainz Jr B, TenCate V, Uprichard SL. Three-dimensional Huh7 cell culture system for the study of Hepatitis C virus infection. Virol J. 2009; 6: 103.
48. Farquhar MJ, Hu K, Harris HJ, Davis C, Brimacombe CL, Fletcher SJ, Baumert TF, Rappoport JZ, Balfe P, McKeating JA. Hepatitis C virus induces CD81 and claudin-1 endocytosis. J Virol. 2012; 86: 4305-16.
49. Meertens L, Bertaux C, Dragic T. Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles. J Virol. 2006; 80: 11571-8.
50. Blanchard E, Belouzard S, Goueslain L, Wakita T, Dubuisson J, Wychowski C, Rouille Y. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol. 2006; 80: 6964-72.
51. Coller KE, Berger KL, Heaton NS, Cooper JD, Yoon R, Randall G. RNA interference and single particle tracking analysis of hepatitis C virus endocytosis. PLoS Pathog. 2009; 5: e1000702.
52. Shiokawa M, Fukuhara T, Ono C, Yamamoto S, Okamoto T, Watanabe N, Wakita T, Matsuura Y. Novel permissive cell lines for complete propagation of hepatitis C virus. J Virol. 2014; 88: 5578-94.
53. Owen DM, Huang H, Ye J, Gale Jr M. Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor. Virology. 2009; 394: 99-108.
54. Gastaminza P, Cheng G, Wieland S, Zhong J, Liao W, Chisari FV. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J Virol. 2008; 82: 2120-9.
55. Gottwein JM, Scheel TK, Jensen TB, Lademann JB, Prentoe JC, Knudsen ML, Hoegh AM, Bukh J. Development and characterization of hepatitis C virus genotype 1-7 cell culture systems: role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology. 2009; 49: 364-77.
56. Scheel TK, Gottwein JM, Mikkelsen LS, Jensen TB, Bukh J. Recombinant HCV variants with NS5A from genotypes 1-7 have different sensitivities to an NS5A inhibitor but not interferon-alpha. Gastroenterology. 2011; 140: 1032-42.
57. Tariq H, Manzoor S, Parvaiz F, Javed F, Fatima K, Qadri I. An overview: in vitro models of HCV replication in different cell cultures. Infect Genet Evol. 2012; 12: 13-20.
58. Li YP, Ramirez S, Jensen SB, Purcell RH, Gottwein JM, Bukh J. Highly efficient full-length hepatitis C virus genotype 1 (strain TN) infectious culture system. Proc Natl Acad Sci U S A. 2012; 109: 19757-62.
59. Yi M, Villanueva RA, Thomas DL, Wakita T, Lemon SM. Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. Proc Natl Acad Sci U S A. 2006; 103: 2310-5.
60. Saeed M, Gondeau C, Hmwe S, Yokokawa H, Date T, Suzuki T, Kato T, Maurel P, Wakita T. Replication of hepatitis C virus genotype 3a in cultured cells. Gastroenterology. 2013; 144: 56-8. e57.
61. Narbus CM, Israelow B, Sourisseau M, Michta ML, Hopcraft SE, Zeiner GM, Evans MJ. HepG2 cells expressing microRNA miR-122 support the entire hepatitis C virus life cycle. J Virol. 2011; 85: 12087-92.
62. Kambara H, Fukuhara T, Shiokawa M, Ono C, Ohara Y, Kamitani W, Matsuura Y. Establishment of a novel permissive cell line for the propagation of hepatitis C virus by expression of microRNA miR122. J Virol. 2012; 86: 1382-93.
63. Da Costa D, Turek M, Felmlee DJ, Girardi E, Pfeffer S, Long G, Bartenschlager R, Zeisel MB, Baumert TF. Reconstitution of the entire hepatitis C virus life cycle in nonhepatic cells. J Virol. 2012; 86: 11919-25.
64. Saeed M, Andreo U, Chung HY, Espiritu C, Branch AD, Silva JM, Rice CM. SEC14L2 enables pan-genotype HCV replication in cell culture. Nature. 2015; 524: 471-5.
65. Schoggins JW, Rice CM. Innate immune responses to hepatitis C virus. Curr Top Microbiol Immunol. 2013; 369: 219-42.
66. Fukuhara T, Taketomi A, Motomura T, Okano S, Ninomiya A, Abe T, Uchiyama H, Soejima Y, Shirabe K, Matsuura Y, Maehara Y. Variants in IL28B in liver recipients and donors correlate with response to peg-interferon and ribavirin therapy for recurrent hepatitis C. Gastroenterology. 2010; 139: 1577-85. 1585 e1571-1573.
67. Suppiah V, Moldovan M, Ahlenstiel G, Berg T, Weltman M, Abate ML, Bassendine M, Spengler U, Dore GJ, Powell E, et al. IL28B is associated with response to chronic hepatitis C interferon-alpha and ribavirin therapy. Nat Genet. 2009; 41: 1100-4.