1887

Abstract

While exploring previous findings that treatment of lymphoid cells from (HCV)-infected individuals with T cell-stimulating mitogens augments detection of the residing virus, an HCV replication system was established, in which mitogen-induced T cell-enriched cultures served as HCV targets and the derived T cells multiplied virus during repeated serial passage. HCV replication was ascertained by detecting HCV RNA positive and negative strands, HCV NS5a and E2 proteins, release of HCV virions and nucleocapsids (confirmed by immunoelectron microscopy) and infection of mitogen-induced T cells prepared from healthy donors. Further, affinity-purified normal human T lymphocytes were also susceptible to HCV infection and HCV replication was detected in pure T cells isolated from a patient with chronic hepatitis C. These results document that T cells can support propagation of HCV both and . The infection system established offers a valuable tool for studies on the entire cycle of HCV replication, virus cytopathogenicity and evaluation of antiviral agents against wild-type HCV in the natural host-cell milieu.

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2006-12-01
2019-11-19
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References

  1. Baré, P., Massud, I., Parodi, C. & 9 other authors ( 2005; ). Continuous release of hepatitis C virus (HCV) by peripheral blood mononuclear cells and B-lymphoblastoid cell-line cultures derived from HCV-infected patients. J Gen Virol 86, 1717–1727.[CrossRef]
    [Google Scholar]
  2. Bartenschlager, R. & Lohmann, V. ( 2000; ). Replication of hepatitis C virus. J Gen Virol 81, 1631–1648.
    [Google Scholar]
  3. Beld, M., Penning, M., Lukashov, V., McMorrow, M., Roos, M., Pakker, N., van den Hoek, A. & Goudsmit, J. ( 1998; ). Evidence that both HIV and HIV-induced immunodeficiency enhance HCV replication among HCV seroconverters. Virology 244, 504–512.[CrossRef]
    [Google Scholar]
  4. Braun, R. W. & Kirchner, H. ( 1986; ). T lymphocytes activated by interleukin 2 alone acquire permissiveness for replication of herpes simplex virus. Eur J Immunol 16, 709–711.[CrossRef]
    [Google Scholar]
  5. Castet, V., Fournier, C., Soulier, A., Brillet, T., Coste, J., Larrey, D., Dhumeaux, D., Maurel, P. & Pawlotsky, J.-M. ( 2002; ). Alpha interferon inhibits hepatitis C virus replication in primary human hepatocytes infected in vitro. J Virol 76, 8189–8199.[CrossRef]
    [Google Scholar]
  6. Chatterjee, R., Gupta, P., Kashmiri, S. V. S. & Ferrer, J. F. ( 1985; ). Phytohemagglutinin activation of the transcription of the bovine leukemia virus genome requires de novo protein synthesis. J Virol 54, 860–863.
    [Google Scholar]
  7. Fujita, N., Kaito, M., Ishida, S., Nakagawa, N., Ikoma, J., Adachi, Y. & Watanabe, S. ( 2001; ). Paraformaldehyde protects of hepatitis C virus particles during ultracentrifugation. J Med Virol 63, 108–116.[CrossRef]
    [Google Scholar]
  8. Goutagny, N., Fatmi, A., De Ledinghen, V., Penin, F., Couzigou, P., Inchauspé, G. & Bain, C. ( 2003; ). Evidence of viral replication in circulating dendritic cells during hepatitis C virus infection. J Infect Dis 187, 1951–1958.[CrossRef]
    [Google Scholar]
  9. Hijikata, M., Shimizu, Y. K., Kato, H., Iwamoto, A., Shih, J. W., Alter, H. J., Purcell, R. H. & Yoshikura, H. ( 1993; ). Equilibrium centrifugation studies of hepatitis C virus: evidence for circulating immune complexes. J Virol 67, 1953–1958.
    [Google Scholar]
  10. Hodgson, P. D. & Michalak, T. I. ( 2001; ). Augmented hepatic interferon gamma expression and T-cell influx characterize acute hepatitis progressing to recovery and residual lifelong virus persistence in experimental adult woodchuck hepatitis virus infection. Hepatology 34, 1049–1059.[CrossRef]
    [Google Scholar]
  11. Hyypiä, T., Korkiamäki, P. & Vainionpää, R. ( 1985; ). Replication of measles virus in human lymphocytes. J Exp Med 161, 1261–1271.[CrossRef]
    [Google Scholar]
  12. Kaito, M., Watanabe, S., Tsukiyama-Kohara, K. & 7 other authors ( 1994; ). Hepatitis C virus particle detected by immunoelectron microscopic study. J Gen Virol 75, 1755–1760.[CrossRef]
    [Google Scholar]
  13. Kanto, T., Hayashi, N., Takehara, T., Hagiwara, H., Mita, E., Naito, M., Kasahara, A., Fusamoto, H. & Kamada, T. ( 1994; ). Buoyant density of hepatitis C virus recovered from infected hosts: two different features in sucrose equilibrium density-gradient centrifugation related to degree of liver inflammation. Hepatology 19, 296–302.[CrossRef]
    [Google Scholar]
  14. Laskus, T., Radkowski, M., Wang, L. F., Vargas, H. & Rakela, J. ( 1998; ). The presence of active hepatitis C virus replication in lymphoid tissue in patients coinfected with human immunodeficiency virus type 1. J Infect Dis 178, 1189–1192.[CrossRef]
    [Google Scholar]
  15. Laskus, T., Radkowski, M., Piasek, A., Nowicki, M., Horban, A., Cianciara, J. & Rakela, J. ( 2000; ). Hepatitis C virus in lymphoid cells of patients coinfected with human immunodeficiency virus type 1: evidence of active replication in monocytes/macrophages and lymphocytes. J Infect Dis 181, 442–448.[CrossRef]
    [Google Scholar]
  16. Laskus, T., Radkowski, M., Jablonska, J., Kibler, K., Wilkinson, J., Adair, D. & Rakela, J. ( 2004; ). Human immunodeficiency virus facilitates infection/replication of hepatitis C virus in native human macrophages. Blood 103, 3854–3859.[CrossRef]
    [Google Scholar]
  17. 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]
    [Google Scholar]
  18. Lindenbach, B. D., Evans, M. J., Syder, A. J. & 8 other authors ( 2005; ). Complete replication of hepatitis C virus in cell culture. Science 309, 623–626.[CrossRef]
    [Google Scholar]
  19. Maillard, P., Krawczynski, K., Nitkiewicz, J. & 7 other authors ( 2001; ). Nonenveloped nucleocapsids of hepatitis C virus in the serum of infected patients. J Virol 75, 8240–8250.[CrossRef]
    [Google Scholar]
  20. Michalak, T. I., Hodgson, P. D. & Churchill, N. D. ( 2000; ). Posttranscriptional inhibition of class I major histocompatibility complex presentation on hepatocytes and lymphoid cells in chronic woodchuck hepatitis virus infection. J Virol 74, 4483–4494.[CrossRef]
    [Google Scholar]
  21. Morsica, G., Tambussi, G., Sitia, G., Novati, R., Lazzarin, A., Lopalco, L. & Mukenge, S. ( 1999; ). Replication of hepatitis C virus in B lymphocytes (CD19+). Blood 94, 1138–1139.
    [Google Scholar]
  22. Okuda, M., Hino, K., Korenaga, M., Yamaguchi, Y., Katoh, Y. & Okita, K. ( 1999; ). Differences in hypervariable region 1 quasispecies of hepatitis C virus in human serum, peripheral blood mononuclear cells, and liver. Hepatology 29, 217–222.[CrossRef]
    [Google Scholar]
  23. Owsianka, A., Clayton, R. F., Loomis-Price, L. D., McKeating, J. A. & Patel, A. H. ( 2001; ). Functional analysis of hepatitis C virus E2 glycoproteins and virus-like particles reveals structural dissimilarities between different forms of E2. J Gen Virol 82, 1877–1883.
    [Google Scholar]
  24. Pham, T. N. Q. & Michalak, T. I. ( 2006; ). Occult hepatitis C virus persistence: identification and characteristics. MLO Med Lab Obs 38, 20–22.
    [Google Scholar]
  25. 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]
    [Google Scholar]
  26. 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]
    [Google Scholar]
  27. Pumeechockchai, W., Bevitt, D., Agarwal, K., Petropoulou, T., Langer, B. C. A., Belohradsky, B., Bassendine, M. F. & Toms, G. L. ( 2002; ). Hepatitis C virus particles of different density in the blood of chronically infected immunocompetent and immunodeficient patients: implications for virus clearance by antibody. J Med Virol 68, 335–342.[CrossRef]
    [Google Scholar]
  28. Radkowski, M., Kubicka, J., Kisiel, E., Cianciara, J., Nowicki, M., Rakela, J. & Laskus, T. ( 2000; ). Detection of active hepatitis C virus and hepatitis G virus/GB virus C replication in bone marrow in human subjects. Blood 95, 3986–3989.
    [Google Scholar]
  29. Radkowski, M., Bednarska, A., Horban, A., Stanczak, J., Wilkinson, J., Adair, D. M., Nowicki, M., Rakela, J. & Laskus, T. ( 2004; ). Infection of primary human macrophages with hepatitis C virus in vitro: induction of tumour necrosis factor-α and interleukin 8. J Gen Virol 85, 47–59.[CrossRef]
    [Google Scholar]
  30. Radkowski, M., Gallegos-Orozco, J. F., Jablonska, J. & 7 other authors ( 2005a; ). Persistence of hepatitis C virus in patients successfully treated for chronic hepatitis C. Hepatology 41, 106–114.[CrossRef]
    [Google Scholar]
  31. Radkowski, M., Horban, A., Gallegos-Orozco, J. F., Pawelczyk, A., Jablonska, J., Wilkinson, J., Adair, D. & Laskus, T. ( 2005b; ). Evidence for viral persistence in patients who test positive for anti-hepatitis C virus antibodies and have normal alanine aminotransferase levels. J Infect Dis 191, 1730–1733.[CrossRef]
    [Google Scholar]
  32. Shimizu, Y. K., Iwamoto, A., Hijikata, M., Purcell, R. H. & Yoshikura, H. ( 1992; ). Evidence for in vitro replication of hepatitis C virus genome in a human T-cell line. Proc Natl Acad Sci U S A 89, 5477–5481.[CrossRef]
    [Google Scholar]
  33. 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.
    [Google Scholar]
  34. Sung, V. M.-H., Shimodaira, S., Doughty, A. L., Picchio, G. R., Can, H., Yen, T. S. B., Lindsay, K. L., Levine, A. M. & Lai, M. M. C. ( 2003; ). Establishment of B-cell lymphoma cell lines persistently infected with hepatitis C virus in vivo and in vitro: the apoptotic effects of virus infection. J Virol 77, 2134–2146.[CrossRef]
    [Google Scholar]
  35. van der Meulen, K. M., Nauwynck, H. J. & Pensaert, M. B. ( 2002; ). Increased susceptibility of peripheral blood mononuclear cells to equine herpes virus type 1 infection upon mitogen stimulation: a role of the cell cycle and of cell-to-cell transmission of the virus. Vet Microbiol 86, 157–163.[CrossRef]
    [Google Scholar]
  36. Wakita, T., Pietschmann, T., Kato, T. & 9 other authors ( 2005; ). Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11, 791–796.[CrossRef]
    [Google Scholar]
  37. Willems, M., Peerlinck, K., Moshage, H., Deleu, I., Van den Eynde, C., Vermylen, J. & Yap, S. H. ( 1994; ). Hepatitis C virus-RNAs in plasma and in peripheral blood mononuclear cells of hemophiliacs with chronic hepatitis C: evidence for viral replication in peripheral blood mononuclear cells. J Med Virol 42, 272–278.[CrossRef]
    [Google Scholar]
  38. Zhong, J., Gastaminza, P., Cheng, G. & 7 other authors ( 2005; ). Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102, 9294–9299.[CrossRef]
    [Google Scholar]
  39. Zignego, A. L., Macchia, D., Monti, M. & 7 other authors ( 1992; ). Infection of peripheral mononuclear blood cells by hepatitis C virus. J Hepatol 15, 382–386.
    [Google Scholar]
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vol. , part 12, pp. 3577 – 3586

Examination of HCV RNA variants in T cell-enriched culture after the direct infection with HCV N07/M inoculum and in cultured T cells collected during serial passage of the virus by nucleotide sequencing [ PDF] (715 KB)



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