1887

Abstract

Hepatitis C virus (HCV) is a hepatotropic virus that also infects cells of the immune system. HCV clones cultivated in human hepatoma Huh-7.5 cells have significantly advanced our understanding of HCV replication and candidate hepatocyte receptors. However, naturally occurring patient-derived HCV, in contrast to the HCV JFH-1 clone, is unable to infect Huh-7.5 cells, while it can replicate in human primary T-cells and selected T-cell lines. To better understand this incongruity, we examined the susceptibility of primary T-cells, PBMCs and T-cell lines to infection with patient-derived HCV, the classical HCV JFH-1 and a cell culture-adapted JFH1 known to be highly infectious to Huh-7.5 cells. We also tested whether Huh-7.5 cells are prone to virus readily infecting T-lymphocytes. The results revealed that while primary T-cells and Molt4 and Jurkat T-cell lines were susceptible to patient-derived HCV, they were resistant to infection with either JFH1 or JFH-1. However, the JFH1 clone interacted more firmly, although non-productively, with the cells than JFH-1. Further, Huh-7.5 cells robustly supported replication of JFH1 but not patient-derived, wild-type virus, despite using highly sensitive detection assays. In conclusion, JFH-1 and JFH1 clones were unable to establish productive infection in human primary T-cells, PBMCs and T-cell lines known to be prone to infection by patient-derived HCV, while Huh-7.5 cells were resistant to infection with naturally occurring virus infecting immune cells. The data showed that the ability to infect lymphocytes is a characteristic of native virus but not laboratory HCV clones.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.045393-0
2012-11-01
2020-07-07
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/11/2399.html?itemId=/content/journal/jgv/10.1099/vir.0.045393-0&mimeType=html&fmt=ahah

References

  1. Anonymous. 1999; Global surveillance and control of hepatitis C. Report of a WHO Consultation organized in collaboration with the Viral Hepatitis Prevention Board, Antwerp, Belgium. J Viral Hepat 6:35–47[PubMed] [CrossRef]
    [Google Scholar]
  2. Blackard J. T., Kemmer N., Sherman K. E. 2006; Extrahepatic replication of HCV: insights into clinical manifestations and biological consequences. Hepatology 44:15–22 [CrossRef][PubMed]
    [Google Scholar]
  3. Buck M., Chojkier M. 1996; Muscle wasting and dedifferentiation induced by oxidative stress in a murine model of cachexia is prevented by inhibitors of nitric oxide synthesis and antioxidants. EMBO J 15:1753–1765[PubMed]
    [Google Scholar]
  4. Castillo I., Rodríguez-Iñigo E., López-Alcorocho J. M., Pardo M., Bartolomé J., Carreño V. 2006; Hepatitis C virus replicates in the liver of patients who have a sustained response to antiviral treatment. Clin Infect Dis 43:1277–1283 [CrossRef][PubMed]
    [Google Scholar]
  5. Choo Q. L., Kuo G., Weiner A. J., Overby L. R., Bradley D. W., Houghton M. 1989; Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359–362 [CrossRef][PubMed]
    [Google Scholar]
  6. Cormier E. G., Tsamis F., Kajumo F., Durso R. J., Gardner J. P., Dragic T. 2004; CD81 is an entry coreceptor for hepatitis C virus. Proc Natl Acad Sci U S A 101:7270–7274 [CrossRef][PubMed]
    [Google Scholar]
  7. Damm E. M., Pelkmans L., Kartenbeck J., Mezzacasa A., Kurzchalia T., Helenius A. 2005; Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168:477–488 [CrossRef][PubMed]
    [Google Scholar]
  8. Di Liberto G., Roque-Afonso A. M., Kara R., Ducoulombier D., Fallot G., Samuel D., F�ray C. 2006; Clinical and therapeutic implications of hepatitis C virus compartmentalization. Gastroenterology 131:76–84 [CrossRef][PubMed]
    [Google Scholar]
  9. Durand T., Di Liberto G., Colman H., Cammas A., Boni S., Marcellin P., Cahour A., Vagner S., Féray C. 2010; Occult infection of peripheral B cells by hepatitis C variants which have low translational efficiency in cultured hepatocytes. Gut 59:934–942 [CrossRef][PubMed]
    [Google Scholar]
  10. Forton D. M., Karayiannis P., Mahmud N., Taylor-Robinson S. D., Thomas H. C. 2004; Identification of unique hepatitis C virus quasispecies in the central nervous system and comparative analysis of internal translational efficiency of brain, liver, and serum variants. J Virol 78:5170–5183 [CrossRef][PubMed]
    [Google Scholar]
  11. Gisbert J. P., García-Buey L., Pajares J. M., Moreno-Otero R. 2003; Prevalence of hepatitis C virus infection in B-cell non-Hodgkin’s lymphoma: systematic review and meta-analysis. Gastroenterology 125:1723–1732 [CrossRef][PubMed]
    [Google Scholar]
  12. Jones S. M., Howell K. E., Henley J. R., Cao H., McNiven M. A. 1998; Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science 279:573–577 [CrossRef][PubMed]
    [Google Scholar]
  13. Jones D. M., Atoom A. M., Zhang X., Kottilil S., Russell R. S. 2011; A genetic interaction between the core and NS3 proteins of hepatitis C virus is essential for production of infectious virus. J Virol 85:12351–12361 [CrossRef][PubMed]
    [Google Scholar]
  14. Kato T., Furusaka A., Miyamoto M., Date T., Yasui K., Hiramoto J., Nagayama K., Tanaka T., Wakita T. 2001; Sequence analysis of hepatitis C virus isolated from a fulminant hepatitis patient. J Med Virol 64:334–339 [CrossRef][PubMed]
    [Google Scholar]
  15. Kato T., Choi Y., Elmowalid G., Sapp R. K., Barth H., Furusaka A., Mishiro S., Wakita T., Krawczynski K., Liang T. J. 2008; Hepatitis C virus JFH-1 strain infection in chimpanzees is associated with low pathogenicity and emergence of an adaptive mutation. Hepatology 48:732–740 [CrossRef][PubMed]
    [Google Scholar]
  16. Korenaga M., Okuda M., Otani K., Wang T., Li Y., Weinman S. A. 2005; Mitochondrial dysfunction in hepatitis C. J Clin Gastroenterol 39:Suppl. 2S162–S166 [CrossRef][PubMed]
    [Google Scholar]
  17. Kroemer G., Jäättelä M. 2005; Lysosomes and autophagy in cell death control. Nat Rev Cancer 5:886–897 [CrossRef][PubMed]
    [Google Scholar]
  18. Lerat H., Berby F., Trabaud M. A., Vidalin O., Major M., Trépo C., Inchauspé G. 1996; Specific detection of hepatitis C virus minus strand RNA in hematopoietic cells. J Clin Invest 97:845–851 [CrossRef][PubMed]
    [Google Scholar]
  19. Lindenbach B. D., Meuleman P., Ploss A., Vanwolleghem T., Syder A. J., McKeating J. A., Lanford R. E., Feinstone S. M., Major M. E. other authors 2006; Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro . Proc Natl Acad Sci U S A 103:3805–3809 [CrossRef][PubMed]
    [Google Scholar]
  20. MacParland S. A., Pham T. N. Q., Gujar S. A., Michalak T. I. 2006; De novo infection and propagation of wild-type hepatitis C virus in human T lymphocytes in vitro . J Gen Virol 87:3577–3586 [CrossRef][PubMed]
    [Google Scholar]
  21. MacParland S. A., Pham T. N. Q., Guy C. S., Michalak T. I. 2009; Hepatitis C virus persisting after clinically apparent sustained virological response to antiviral therapy retains infectivity in vitro . Hepatology 49:1431–1441 [CrossRef][PubMed]
    [Google Scholar]
  22. Marukian S., Jones C. T., Andrus L., Evans M. J., Ritola K. D., Charles E. D., Rice C. M., Dustin L. B. 2008; Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells. Hepatology 48:1843–1850 [CrossRef][PubMed]
    [Google Scholar]
  23. Meuleman P., Leroux-Roels G. 2009; HCV animal models: a journey of more than 30 years. Viruses 1:222–240 [CrossRef][PubMed]
    [Google Scholar]
  24. Murakami K., Kimura T., Osaki M., Ishii K., Miyamura T., Suzuki T., Wakita T., Shoji I. 2008; Virological characterization of the hepatitis C virus JFH-1 strain in lymphocytic cell lines. J Gen Virol 89:1587–1592 [CrossRef][PubMed]
    [Google Scholar]
  25. Pal S., Sullivan D. G., Kim S., Lai K. K., Kae J., Cotler S. J., Carithers R. L. Jr, Wood B. L., Perkins J. D., Gretch D. R. 2006; Productive replication of hepatitis C virus in perihepatic lymph nodes in vivo: implications of HCV lymphotropism. Gastroenterology 130:1107–1116 [CrossRef][PubMed]
    [Google Scholar]
  26. Pham T. N. Q., MacParland S. A., Mulrooney P. M., Cooksley H., Naoumov N. V., Michalak T. I. 2004; Hepatitis C virus persistence after spontaneous or treatment-induced resolution of hepatitis C. J Virol 78:5867–5874 [CrossRef][PubMed]
    [Google Scholar]
  27. Pham T. N. Q., MacParland S. A., Coffin C. S., Lee S. S., Bursey F. R., Michalak T. I. 2005; Mitogen-induced upregulation of hepatitis C virus expression in human lymphoid cells. J Gen Virol 86:657–666 [CrossRef][PubMed]
    [Google Scholar]
  28. Pham T. N. Q., King D., MacParland S. A., McGrath J. S., Reddy S. B., Bursey F. R., Michalak T. I. 2008; Hepatitis C virus replicates in the same immune cell subsets in chronic hepatitis C and occult infection. Gastroenterology 134:812–822 [CrossRef][PubMed]
    [Google Scholar]
  29. Pham T. N. Q., Mercer S. E., Michalak T. I. 2009; Chronic hepatitis C and persistent occult hepatitis C virus infection are characterized by distinct immune cell cytokine expression profiles. J Viral Hepat 16:547–556 [CrossRef][PubMed]
    [Google Scholar]
  30. Pham T. N. Q., Coffin C. S., Michalak T. I. 2010; Occult hepatitis C virus infection: what does it mean?. Liver Int 30:502–511 [CrossRef][PubMed]
    [Google Scholar]
  31. Pham T. N. Q., Coffin C. S., Churchill N. D., Urbanski S. J., Lee S. S., Michalak T. I. 2012; Hepatitis C virus persistence after sustained virological response to antiviral therapy in patients with or without past exposure to hepatitis B virus. J Viral Hepat 19:103–111 [CrossRef][PubMed]
    [Google Scholar]
  32. Radkowski M., Gallegos-Orozco J. F., Jablonska J., Colby T. V., Walewska-Zielecka B., Kubicka J., Wilkinson J., Adair D., Rakela J., Laskus T. 2005; Persistence of hepatitis C virus in patients successfully treated for chronic hepatitis C. Hepatology 41:106–114 [CrossRef][PubMed]
    [Google Scholar]
  33. Roque-Afonso A. M., Ducoulombier D., Di Liberto G., Kara R., Gigou M., Dussaix E., Samuel D., Féray C. 2005; Compartmentalization of hepatitis C virus genotypes between plasma and peripheral blood mononuclear cells. J Virol 79:6349–6357 [CrossRef][PubMed]
    [Google Scholar]
  34. Russell R. S., Meunier J. C., Takikawa S., Faulk K., Engle R. E., Bukh J., Purcell R. H., Emerson S. U. 2008; Advantages of a single-cycle production assay to study cell culture-adaptive mutations of hepatitis C virus. Proc Natl Acad Sci U S A 105:4370–4375 [CrossRef][PubMed]
    [Google Scholar]
  35. Sarhan M. A., Pham T. N. Q., Chen A. Y., Michalak T. I. 2012; Hepatitis C virus infection of human T lymphocytes is mediated by CD5. J Virol 86:3723–3735 [CrossRef][PubMed]
    [Google Scholar]
  36. Shimizu Y. K., Igarashi H., Kanematu T., Fujiwara K., Wong D. C., Purcell R. H., Yoshikura H. 1997; Sequence analysis of the hepatitis C virus genome recovered from serum, liver, and peripheral blood mononuclear cells of infected chimpanzees. J Virol 71:5769–5773[PubMed]
    [Google Scholar]
  37. Shimizu Y. K., Igarashi H., Kiyohara T., Shapiro M., Wong D. C., Purcell R. H., Yoshikura H. 1998; Infection of a chimpanzee with hepatitis C virus grown in cell culture. J Gen Virol 79:1383–1386[PubMed]
    [Google Scholar]
  38. Tong M. J., el-Farra N. S., Reikes A. R., Co R. L. 1995; Clinical outcomes after transfusion-associated hepatitis C. N Engl J Med 332:1463–1466 [CrossRef][PubMed]
    [Google Scholar]
  39. Wakita T., Pietschmann T., Kato T., Date T., Miyamoto M., Zhao Z., Murthy K., Habermann A., Kräusslich H. G. other authors 2005; Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11:791–796 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.045393-0
Loading
/content/journal/jgv/10.1099/vir.0.045393-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error