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International Journal of Hepatology
Volume 2012 (2012), Article ID 292591, 8 pages
http://dx.doi.org/10.1155/2012/292591
Review Article

In Vitro Systems for the Study of Hepatitis C Virus Infection

NIHR Biomedical Research Unit and Centre for Liver Research, School of Immunity and Infection, College of Medical and Dental Sciences, University of Birmingham, Birmingham B15 2TT, UK

Received 26 April 2012; Revised 3 July 2012; Accepted 17 July 2012

Academic Editor: Fredric D. Gordon

Copyright © 2012 Garrick K. Wilson and Zania Stamataki. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. J. Alter, “Epidemiology of hepatitis C virus infection,” World Journal of Gastroenterology, vol. 13, no. 17, pp. 2436–2441, 2007. View at Google Scholar · View at Scopus
  2. A. D. Kwong, R. S. Kauffman, P. Hurter, and P. Mueller, “Discovery and development of telaprevir: an NS3-4A protease inhibitor for treating genotype 1 chronic hepatitis C virus,” Nature Biotechnology, vol. 29, no. 11, pp. 993–1003, 2011. View at Google Scholar
  3. F. Poordad, J. McCone, B. R. Bacon et al., “Boceprevir for untreated chronic HCV genotype 1 infection,” The New England Journal of Medicine, vol. 364, no. 13, pp. 1195–1206, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. A. J. Thompson, S. A. Locarnini, and M. R. Beard, “Resistance to anti-HCV protease inhibitors,” Current Opinion in Virology, vol. 1, no. 6, pp. 599–606, 2011. View at Publisher · View at Google Scholar
  5. S. Ciesek and H. Wedemeyer, “Immunosuppression, liver injury and post-transplant HCV recurrence,” Journal of Viral Hepatitis, vol. 19, no. 1, pp. 1–8, 2012. View at Publisher · View at Google Scholar
  6. P. G. Northup, T. L. Pruett, D. M. Kashmer, C. K. Argo, C. L. Berg, and T. M. Schmitt, “Donor factors predicting recipient survival after liver retransplantation: the retransplant donor risk index,” American Journal of Transplantation, vol. 7, no. 8, pp. 1984–1988, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. J. M. Timpe and J. A. McKeating, “Hepatitis C virus entry: possible targets for therapy,” Gut, vol. 57, no. 12, pp. 1728–1737, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. M. B. Zeisel, I. Fofana, S. Fafi-Kremer, and T. F. Baumert, “Hepatitis C virus entry into hepatocytes: molecular mechanisms and targets for antiviral therapies,” Journal of Hepatology, vol. 54, no. 3, pp. 566–576, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Pileri, Y. Uematsu, S. Campagnoli et al., “Binding of hepatitis C virus to CD81,” Science, vol. 282, no. 5390, pp. 938–941, 1998. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Scarselli, H. Ansuini, R. Cerino et al., “The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus,” EMBO Journal, vol. 21, no. 19, pp. 5017–5025, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. M. J. Evans, T. von Hahn, D. M. Tscherne et al., “Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry,” Nature, vol. 446, no. 7137, pp. 801–805, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Ploss, M. J. Evans, V. A. Gaysinskaya et al., “Human occludin is a hepatitis C virus entry factor required for infection of mouse cells,” Nature, vol. 457, no. 7231, pp. 882–886, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. V. Lohmann, F. Körner, J. O. Koch, U. Herian, L. Theilmann, and R. Bartenschlager, “Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line,” Science, vol. 285, no. 5424, pp. 110–113, 1999. View at Publisher · View at Google Scholar · View at Scopus
  14. K. J. Blight, J. A. McKeating, and C. M. Rice, “Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication,” Journal of Virology, vol. 76, no. 24, pp. 13001–13014, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. K. J. Blight, A. A. Kolykhalov, and C. M. Rice, “Efficient initiation of HCV RNA replication in cell culture,” Science, vol. 290, no. 5498, pp. 1972–1974, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Krieger, V. Lohmann, and R. Bartenschlager, “Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations,” Journal of Virology, vol. 75, no. 10, pp. 4614–4624, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Cocquerel, C. Wychowski, F. Minner, F. Penin, and J. Dubuisson, “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,” Journal of Virology, vol. 74, no. 8, pp. 3623–3633, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. T. von Hahn and C. M. Rice, “Hepatitis C virus entry,” Journal of Biological Chemistry, vol. 283, no. 7, pp. 3689–3693, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. J. P. Michalak, C. Wychowski, A. Choukhi et al., “Characterization of truncated forms of hepatitis C virus glycoproteins,” Journal of General Virology, vol. 78, no. 9, pp. 2299–2306, 1997. View at Google Scholar · View at Scopus
  20. M. Hsu, J. Zhang, M. Flint et al., “Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 12, pp. 7271–7276, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. L. M. Lagging, K. Meyer, R. J. Owens, and R. Ray, “Functional role of hepatitis C virus chimeric glycoproteins in the infectivity of pseudotyped virus,” Journal of Virology, vol. 72, no. 5, pp. 3539–3546, 1998. View at Google Scholar · View at Scopus
  22. B. Bartosch, J. Dubuisson, and F. L. Cosset, “Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes,” Journal of Experimental Medicine, vol. 197, no. 5, pp. 633–642, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Wakita, T. Pietschmann, T. Kato et al., “Production of infectious hepatitis C virus in tissue culture from a cloned viral genome,” Nature Medicine, vol. 11, no. 7, pp. 791–796, 2005. View at Google Scholar · View at Scopus
  24. B. D. Lindenbach, M. J. Evans, A. J. Syder et al., “Virology: complete replication of hepatitis C virus in cell culture,” Science, vol. 309, no. 5734, pp. 623–626, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Zhong, P. Gastaminza, G. Cheng et al., “Robust hepatitis C virus infection in vitro,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 26, pp. 9294–9299, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. B. D. Lindenbach, P. Meuleman, A. Ploss et al., “Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 10, pp. 3805–3809, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. J. M. Gottwein, T. K. H. Scheel, T. B. Jensen et al., “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, vol. 49, no. 2, pp. 364–377, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. T. K. H. Scheel, J. M. Gottwein, T. B. Jensen et al., “Development of JFH1-based cell culture systems for hepatitis C virus genotype 4a and evidence for cross-genotype neutralization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 3, pp. 997–1002, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. J. M. Gottwein, T. K. H. Scheel, A. M. Hoegh et al., “Robust hepatitis C genotype 3a cell culture releasing adapted intergenotypic 3a/2a (S52/JFH1) viruses,” Gastroenterology, vol. 133, no. 5, pp. 1614–1626, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Yi, R. A. Villanueva, D. L. Thomas, T. Wakita, and S. M. Lemon, “Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 7, pp. 2310–2315, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. Q. L. Choo, G. Kuo, A. J. Weiner et al., “Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome,” Science, vol. 244, no. 4902, pp. 359–362, 1989. View at Google Scholar
  32. C. Gondeau, L. Pichard-Garcia, and P. Maurel, “Cellular models for the screening and development of anti-hepatitis C virus agents,” Pharmacology and Therapeutics, vol. 124, no. 1, pp. 1–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. R. Bartenschlager and V. Lohmann, “Novel cell culture systems for the hepatitis C virus,” Antiviral Research, vol. 52, no. 1, pp. 1–17, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. D. V. Sangar and A. R. Carroll, “A tale of two strands: reverse-transcriptase polymerase chain reaction detection of hepatitis C virus replication,” Hepatology, vol. 28, no. 5, pp. 1173–1176, 1998. View at Publisher · View at Google Scholar · View at Scopus
  35. S. T. Takyar, D. S. Li, Y. H. Wang, R. Trowbridge, and E. J. Gowans, “Specific detection of minus-strand hepatitis C virus RNA by reverse- transcription polymerase chain reaction on polyA(+)-purified RNA,” Hepatology, vol. 32, no. 2, pp. 382–387, 2000. View at Google Scholar · View at Scopus
  36. R. E. Lanford, C. Sureau, J. R. Jacob, R. White, and T. R. Fuerst, “Demonstration of in vitro infection of chimpanzee hepatocytes with hepatitis C virus using strand-specific RT/PCR,” Virology, vol. 202, no. 2, pp. 606–614, 1994. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Codran, C. Royer, D. Jaeck et al., “Entry of hepatitis C virus pseudotypes into primary human hepatocytes by clathrin-dependent endocytosis,” Journal of General Virology, vol. 87, no. 9, pp. 2583–2593, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Podevin, A. Carpentier, V. Pne et al., “Production of infectious hepatitis C virus in primary cultures of human adult hepatocytes,” Gastroenterology, vol. 139, no. 4, pp. 1355–1364, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Sivaraman, J. K. Leach, S. Townsend et al., “A microscale in vitro physiological model of the liver: predictive screens for drug metabolism and enzyme induction,” Current Drug Metabolism, vol. 6, no. 6, pp. 569–591, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. S. N. Bhatia, U. J. Balis, M. L. Yarmush, and M. Toner, “Effect of cell-cell interactions in preservation of cellular phenotype: cocultivation of hepatocytes and nonparenchymal cells,” FASEB Journal, vol. 13, no. 14, pp. 1883–1900, 1999. View at Google Scholar · View at Scopus
  41. S. R. Khetani and S. N. Bhatia, “Microscale culture of human liver cells for drug development,” Nature Biotechnology, vol. 26, no. 1, pp. 120–126, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Ploss, S. R. Khetani, C. T. Jones et al., “Persistent hepatitis C virus infection in microscale primary human hepatocyte cultures,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 7, pp. 3141–3145, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. X. Wu, J. M. Robotham, E. Lee et al., “Productive hepatitis C virus infection of stem cell-derived hepatocytes reveals a critical transition to viral permissiveness during differentiation,” PLoS Pathogens, vol. 8, no. 4, Article ID e1002617, 2012. View at Publisher · View at Google Scholar
  44. T. Yoshida, K. Takayama, M. Kondoh et al., “Use of human hepatocyte-like cells derived from induced pluripotent stem cells as a model for hepatocytes in hepatitis C virus infection,” Biochemical and biophysical research communications, vol. 416, no. 1-2, pp. 119–124, 2011. View at Google Scholar
  45. K. Si-Tayeb, J. C. Duclos-Vallee, and M. A. Petit, “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, vol. 57, no. 3, pp. 689–691, 2012. View at Google Scholar
  46. P. Roelandt, S. Obeid, J. Paeshuyse et al., “Human pluripotent stem cell-derived hepatocytes support complete replication of hepatitis C virus,” Journal of Hepatology, vol. 57, no. 2, pp. 246–251, 2012. View at Google Scholar
  47. S. Marukian, L. Andrus, T. P. Sheahan et al., “Hepatitis C virus induces interferon-lambda and interferon-stimulated genes in primary liver cultures,” Hepatology, vol. 54, no. 6, pp. 1913–1923, 2011. View at Publisher · View at Google Scholar
  48. C. A. Lázaro, M. Chang, W. Tang et al., “Hepatitis C virus replication in transfected and serum-infected cultured human fetal hepatocytes,” American Journal of Pathology, vol. 170, no. 2, pp. 478–489, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. L. Andrus, S. Marukian, C. T. Jones et al., “Expression of paramyxovirus V proteins promotes replication and spread of hepatitis C virus in cultures of primary human fetal liver cells,” Hepatology, vol. 54, no. 6, pp. 1901–1912, 2011. View at Publisher · View at Google Scholar
  50. M. Ikeda, K. Sugiyama, T. Mizutani et al., “Human hepatocyte clonal cell lines that support persistent replication of hepatitis C virus,” Virus Research, vol. 56, no. 2, pp. 157–167, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. H. H. Aly, K. Watashi, M. Hijikata et al., “Serum-derived hepatitis C virus infectivity in interferon regulatory factor-7-suppressed human primary hepatocytes,” Journal of Hepatology, vol. 46, no. 1, pp. 26–36, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. R. E. Lanford, B. Guerra, H. Lee et al., “Antiviral effect and virus-host interactions in response to alpha interferon, gamma interferon, poly(I)-poly(C), tumor necrosis factor alpha, and ribavirin in hepatitis C virus subgenomic replicons,” Journal of Virology, vol. 77, no. 2, pp. 1092–1104, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Sumpter, Y. M. Loo, E. Foy et al., “Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I,” Journal of Virology, vol. 79, no. 5, pp. 2689–2699, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. D. Durantel and F. Zoulim, “Going towards more relevant cell culture models to study the in vitro replication of serum-derived hepatitis C virus and virus/host cell interactions?” Journal of Hepatology, vol. 46, no. 1, pp. 1–5, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. B. Sainz Jr. and F. V. Chisari, “Production of infectious hepatitis C virus by well-differentiated, growth-arrested human hepatoma-derived cells,” Journal of Virology, vol. 80, no. 20, pp. 10253–10257, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. O. Bauhofer, A. Ruggieri, B. Schmid, P. Schirmacher, and R. Bartenschlager, “Persistance of HCV in quiescent hepatic cells during an interferon-induced antiviral response,” Gastroenterology, vol. 143, no. 2, pp. 429.e8–438.e8, 2012. View at Google Scholar
  57. B. Sainz Jr., N. Barretto, X. Yu, P. Corcoran, and S. L. Uprichard, “Permissiveness of human hepatoma cell lines for HCV infection,” Virology Journal, vol. 9, article 30, 2012. View at Publisher · View at Google Scholar
  58. S. Haid, M. P. Windisch, R. Bartenschlager, and T. Pietschmann, “Mouse-specific residues of claudin-1 limit hepatitis C virus genotype 2a infection in a human hepatocyte cell line,” Journal of Virology, vol. 84, no. 2, pp. 964–975, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. M. P. Windisch, M. Frese, A. Kaul, M. Trippier, V. Lohmann, and R. Bartenschlager, “Dissecting the interferon-induced inhibition of hepatitis C virus replication by using a novel host cell line,” Journal of Virology, vol. 79, no. 21, pp. 13778–13793, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. E. Blanchard, S. Belouzard, L. Goueslain et al., “Hepatitis C virus entry depends on clathrin-mediated endocytosis,” Journal of Virology, vol. 80, no. 14, pp. 6964–6972, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. I. Benedicto, F. Molina-Jiménez, B. Bartosch et al., “The tight junction-associated protein occludin is required for a postbinding step in hepatitis C virus entry and infection,” Journal of Virology, vol. 83, no. 16, pp. 8012–8020, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. C. L. Jopling, M. Yi, A. M. Lancaster, S. M. Lemon, and P. Sarnow, “Molecular biology: modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA,” Science, vol. 309, no. 5740, pp. 1577–1581, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. J. A. McKeating, L. Q. Zhang, C. Logvinoff et al., “Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner,” Journal of Virology, vol. 78, no. 16, pp. 8496–8505, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. C. J. Mee, H. J. Harris, M. J. Farquhar et al., “Polarization restricts hepatitis C virus entry into HepG2 hepatoma cells,” Journal of Virology, vol. 83, no. 12, pp. 6211–6221, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. C. J. Mee, M. J. Farquhar, H. J. Harris et al., “Hepatitis C virus infection reduces hepatocellular polarity in a vascular endothelial growth factor-dependent manner,” Gastroenterology, vol. 138, no. 3, pp. 1134–1142, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. G. K. Wilson, C. L. Brimacombe et al., “A dual role for hypoxia inducible factor-1alpha in the hepatitis C virus lifecycle and hepatoma migration,” Journal of hepatology, vol. 56, no. 4, pp. 803–809, 2012. View at Publisher · View at Google Scholar
  67. N. F. Fletcher, G. K. Wilson, J. Murray et al., “Hepatitis C virus infects the endothelial cells of the blood-brain barrier,” Gastroenterology, vol. 142, pp. 634.e6–643.e6, 2012. View at Google Scholar
  68. N. F. Fletcher, J. P. Yang, M. J. Farquhar et al., “Hepatitis C virus infection of neuroepithelioma cell lines,” Gastroenterology, vol. 139, no. 4, pp. 1365–1374, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. C. J. Mee, J. Grove, H. J. Harris, K. Hu, P. Balfe, and J. A. McKeating, “Effect of cell polarization on hepatitis C virus entry,” Journal of Virology, vol. 82, no. 1, pp. 461–470, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. I. Fofana, S. E. Krieger, F. Grunert et al., “Monoclonal anti-claudin 1 antibodies prevent hepatitis C virus infection of primary human hepatocytes,” Gastroenterology, vol. 139, no. 3, pp. 953.e4–964.e4, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Decaens, M. Durand, B. Grosse, and D. Cassio, “Which in vitro models could be best used to study hepatocyte polarity?” Biology of the Cell, vol. 100, no. 7, pp. 387–398, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. W. Yang, C. Qiu, N. Biswas et al., “Correlation of the tight junction-like distribution of claudin-1 to the cellular tropism of hepatitis C virus,” Journal of Biological Chemistry, vol. 283, no. 13, pp. 8643–8653, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. V. Lohmann, S. Hoffmann, U. Herian, F. Penin, and R. Bartenschlager, “Viral and cellular determinants of hepatitis C virus RNA replication in cell culture,” Journal of Virology, vol. 77, no. 5, pp. 3007–3019, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. F. Molina-Jimenez, I. Benedicto, V. L. Dao Thi et al., “Matrigel-embedded 3D culture of Huh-7 cells as a hepatocyte-like polarized system to study hepatitis C virus cycle,” Virology, vol. 425, no. 1, pp. 31–39, 2012. View at Google Scholar
  75. C. J. Mee, H. J. Harris, M. J. Farquhar et al., “Polarization restricts hepatitis C virus entry into HepG2 hepatoma cells,” Journal of Virology, vol. 83, no. 12, pp. 6211–6221, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. G. K. Wilson, C. L. Brimacombe, I. A. Rowe et al., “A dual role for hypoxia inducible factor-1alpha in the hepatitis C virus lifecycle and hepatoma migration,” Journal of Hepatology, vol. 56, no. 4, pp. 803–809, 2012. View at Publisher · View at Google Scholar
  77. S. Lagaye, H. Shen, B. Saunier et al., “Efficient replication of primary or culture hepatitis C virus isolates in human liver slices: a relevant ex vivo model of liver infection,” Hepatology. In press. View at Publisher · View at Google Scholar
  78. E. Liaskou, M. Karikoski, G. M. Reynolds et al., “Regulation of mucosal addressin cell adhesion molecule 1 expression in human and mice by vascular adhesion protein 1 amine oxidase activity,” Hepatology, vol. 53, no. 2, pp. 661–672, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. Z. Stamataki, C. Shannon-Lowe, J. Shaw et al., “Hepatitis C virus association with peripheral blood B lymphocytes potentiates viral infection of liver-derived hepatoma cells,” Blood, vol. 113, no. 3, pp. 585–593, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. T. B. H. Geijtenbeek, D. S. Kwon, R. Torensma et al., “DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells,” Cell, vol. 100, no. 5, pp. 587–597, 2000. View at Google Scholar · View at Scopus
  81. C. D. Shannon-Lowe, B. Neuhierl, G. Baldwin, A. B. Rickinson, and H. J. Delecluse, “Resting B cells as a transfer vehicle for Epstein-Barr virus infection of epithelial cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 18, pp. 7065–7070, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. C. Welsch, A. Jesudian, S. Zeuzem, and I. Jacobson, “New direct-acting antiviral agents for the treatment of hepatitis C virus infection and perspectives,” Gut, vol. 61, supplement 1, pp. i36–i46, 2012. View at Publisher · View at Google Scholar