1887

Abstract

Since the widespread use of the highly active antiretroviral therapy, the incidence of liver disease has increased to become a leading cause of death among human immunodeficiency virus type 1 (HIV-1)-infected individuals. It can be proposed that the ability of HIV-1 to infect hepatocytes could influence liver diseases. Although the presence of HIV-1 was identified in hepatocytes from HIV-1 seropositive patients, the susceptibility of hepatocytes to HIV-1 infection remains controversial. We present evidence here that human hepatoma cells are not productively infected with CD4-dependent HIV-1 strains because of inefficient fusion related to an absence of cell surface CD4 and CXCR4. However, these cells display an increased susceptibility to infection with a CD4-independent viral isolate through an interaction with galactosyl ceramide, an alternate receptor for HIV-1. This study provides further understanding of the susceptibility of human hepatocytes to HIV-1 infection. However, investigations are recommended to consolidate these data.

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2011-03-01
2020-01-28
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References

  1. Adachi, A., Gendelman, H. E., Koenig, S., Folks, T., Willey, R., Rabson, A. & Martin, M. A. ( 1986; ). Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol 59, 284–291.
    [Google Scholar]
  2. Baba, M., Nishimura, O., Kanzaki, N., Okamoto, M., Sawada, H., Iizawa, Y., Shiraishi, M., Aramaki, Y., Okonogi, K. & other authors ( 1999; ). A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc Natl Acad Sci U S A 96, 5698–5703.[CrossRef]
    [Google Scholar]
  3. Babu, C. K., Suwansrinon, K., Bren, G. D., Badley, A. D. & Rizza, S. A. ( 2009; ). HIV induces TRAIL sensitivity in hepatocytes. PLoS ONE 4, e4623.[CrossRef]
    [Google Scholar]
  4. Balasubramanian, A., Koziel, M., Groopman, J. E. & Ganju, R. K. ( 2005; ). Molecular mechanism of hepatic injury in coinfection with hepatitis C virus and HIV. Clin Infect Dis 41 ((Suppl 1), ), S32–S37.[CrossRef]
    [Google Scholar]
  5. Banerjee, R., Sperber, K., Pizzella, T. & Mayer, L. ( 1992; ). Inhibition of HIV-1 productive infection in hepatoblastoma HepG2 cells by recombinant tumor necrosis factor-alpha. AIDS 6, 1127–1131.[CrossRef]
    [Google Scholar]
  6. Blight, K. J., McKeating, J. A. & Rice, C. M. ( 2002; ). Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 76, 13001–13014.[CrossRef]
    [Google Scholar]
  7. Bounou, S., Leclerc, J. E. & Tremblay, M. J. ( 2002; ). Presence of host ICAM-1 in laboratory and clinical strains of human immunodeficiency virus type 1 increases virus infectivity and CD4+-T-cell depletion in human lymphoid tissue, a major site of replication in vivo. J Virol 76, 1004–1014.[CrossRef]
    [Google Scholar]
  8. Bridger, G. J., Skerlj, R. T., Thornton, D., Padmanabhan, S., Martellucci, S. A., Henson, G. W., Abrams, M. J., Yamamoto, N., De Vreese, K. & other authors ( 1995; ). Synthesis and structure-activity relationships of phenylenebis(methylene)-linked bis-tetraazamacrocycles that inhibit HIV replication. Effects of macrocyclic ring size and substituents on the aromatic linker. J Med Chem 38, 366–378.[CrossRef]
    [Google Scholar]
  9. Cao, Y. Z., Friedman-Kien, A. E., Huang, Y. X., Li, X. L., Mirabile, M., Moudgil, T., Zucker-Franklin, D. & Ho, D. D. ( 1990; ). CD4-independent, productive human immunodeficiency virus type 1 infection of hepatoma cell lines in vitro. J Virol 64, 2553–2559.
    [Google Scholar]
  10. Cao, Y. Z., Dieterich, D., Thomas, P. A., Huang, Y. X., Mirabile, M. & Ho, D. D. ( 1992; ). Identification and quantitation of HIV-1 in the liver of patients with AIDS. AIDS 6, 65–70.[CrossRef]
    [Google Scholar]
  11. Cavrois, M., De Noronha, C. & Greene, W. C. ( 2002; ). A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat Biotechnol 20, 1151–1154.[CrossRef]
    [Google Scholar]
  12. Clapham, P. R. & McKnight, A. ( 2002; ). Cell surface receptors, virus entry and tropism of primate lentiviruses. J Gen Virol 83, 1809–1829.
    [Google Scholar]
  13. Curtis, B. M., Scharnowske, S. & Watson, A. J. ( 1992; ). Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc Natl Acad Sci U S A 89, 8356–8360.[CrossRef]
    [Google Scholar]
  14. Daar, E. S., Lynn, H., Donfield, S., Gomperts, E., Hilgartner, M. W., Hoots, W. K., Chernoff, D., Arkin, S., Wong, W. Y. & other authors ( 2001; ). Relation between HIV-1 and hepatitis C viral load in patients with hemophilia. J Acquir Immune Defic Syndr 26, 466–472.[CrossRef]
    [Google Scholar]
  15. De Clercq, E., Yamamoto, N., Pauwels, R., Balzarini, J., Witvrouw, M., De Vreese, K., Debyser, Z., Rosenwirth, B., Peichl, P. & other authors ( 1994; ). Highly potent and selective inhibition of human immunodeficiency virus by the bicyclam derivative JM3100. Antimicrob Agents Chemother 38, 668–674.[CrossRef]
    [Google Scholar]
  16. Derdeyn, C. A., Decker, J. M., Sfakianos, J. N., Wu, X., O'Brien, W. A., Ratner, L., Kappes, J. C., Shaw, G. M. & Hunter, E. ( 2000; ). Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J Virol 74, 8358–8367.[CrossRef]
    [Google Scholar]
  17. Dornadula, G., Zhang, H., Shetty, S. & Pomerantz, R. J. ( 1999; ). HIV-1 virions produced from replicating peripheral blood lymphocytes are more infectious than those from nonproliferating macrophages due to higher levels of intravirion reverse transcripts: implications for pathogenesis and transmission. Virology 253, 10–16.[CrossRef]
    [Google Scholar]
  18. Dumonceaux, J., Nisole, S., Chanel, C., Quivet, L., Amara, A., Baleux, F., Briand, P. & Hazan, U. ( 1998; ). Spontaneous mutations in the env gene of the human immunodeficiency virus type 1 NDK isolate are associated with a CD4-independent entry phenotype. J Virol 72, 512–519.
    [Google Scholar]
  19. Eyster, M. E., Fried, M. W., Di Bisceglie, A. M. & Goedert, J. J. ( 1994; ). Increasing hepatitis C virus RNA levels in hemophiliacs: relationship to human immunodeficiency virus infection and liver disease. Multicenter Hemophilia Cohort Study. Blood 84, 1020–1023.
    [Google Scholar]
  20. Fantini, J., Yahi, N. & Chermann, J. C. ( 1991; ). Human immunodeficiency virus can infect the apical and basolateral surfaces of human colonic epithelial cells. Proc Natl Acad Sci U S A 88, 9297–9301.[CrossRef]
    [Google Scholar]
  21. Fantini, J., Cook, D. G., Nathanson, N., Spitalnik, S. L. & Gonzalez-Scarano, F. ( 1993; ). Infection of colonic epithelial cell lines by type 1 human immunodeficiency virus is associated with cell surface expression of galactosylceramide, a potential alternative gp120 receptor. Proc Natl Acad Sci U S A 90, 2700–2704.[CrossRef]
    [Google Scholar]
  22. Fortin, J. F., Cantin, R., Lamontagne, G. & Tremblay, M. ( 1997; ). Host-derived ICAM-1 glycoproteins incorporated on human immunodeficiency virus type 1 are biologically active and enhance viral infectivity. J Virol 71, 3588–3596.
    [Google Scholar]
  23. Fromentin, R., Tardif, M. R. & Tremblay, M. J. ( 2010; ). Human hepatoma cells transmit surface bound HIV-1 to CD4+ T cells through an ICAM-1/LFA-1-dependent mechanism. Virology 398, 168–175.[CrossRef]
    [Google Scholar]
  24. Hammache, D., Piéroni, G., Yahi, N., Delézay, O., Koch, N., Lafont, H., Tamalet, C. & Fantini, J. ( 1998; ). Specific interaction of HIV-1 and HIV-2 surface envelope glycoproteins with monolayers of galactosylceramide and ganglioside GM3. J Biol Chem 273, 7967–7971.[CrossRef]
    [Google Scholar]
  25. Harouse, J. M. & González-Scarano, F. ( 1996; ). Infection of SK-N-MC cells, a CD4-negative neuroblastoma cell line, with primary human immunodeficiency virus type 1 isolates. J Virol 70, 7290–7294.
    [Google Scholar]
  26. Harouse, J. M., Bhat, S., Spitalnik, S. L., Laughlin, M., Stefano, K., Silberberg, D. H. & Gonzalez-Scarano, F. ( 1991; ). Inhibition of entry of HIV-1 in neural cell lines by antibodies against galactosyl ceramide. Science 253, 320–323.[CrossRef]
    [Google Scholar]
  27. Hendrix, C. W., Flexner, C., MacFarland, R. T., Giandomenico, C., Fuchs, E. J., Redpath, E., Bridger, G. & Henson, G. W. ( 2000; ). Pharmacokinetics and safety of AMD-3100, a novel antagonist of the CXCR-4 chemokine receptor, in human volunteers. Antimicrob Agents Chemother 44, 1667–1673.[CrossRef]
    [Google Scholar]
  28. Housset, C., Boucher, O., Girard, P. M., Leibowitch, J., Saimot, A. G., Bréchot, C. & Marche, C. ( 1990; ). Immunohistochemical evidence for human immunodeficiency virus-1 infection of liver Kupffer cells. Hum Pathol 21, 404–408.[CrossRef]
    [Google Scholar]
  29. Housset, C., Lamas, E., Courgnaud, V., Boucher, O., Girard, P. M., Marche, C. & Brechot, C. ( 1993; ). Presence of HIV-1 in human parenchymal and non-parenchymal liver cells in vivo. J Hepatol 19, 252–258.[CrossRef]
    [Google Scholar]
  30. Iser, D. M., Warner, N., Revill, P. A., Solomon, A., Wightman, F., Saleh, S., Crane, M., Cameron, P. U., Bowden, S. & other authors ( 2010; ). Coinfection of hepatic cell lines with human immunodeficiency virus and hepatitis B virus leads to an increase in intracellular hepatitis B surface antigen. J Virol 84, 5860–5867.[CrossRef]
    [Google Scholar]
  31. Johansen, T. E., Schøller, M. S., Tolstoy, S. & Schwartz, T. W. ( 1990; ). Biosynthesis of peptide precursors and protease inhibitors using new constitutive and inducible eukaryotic expression vectors. FEBS Lett 267, 289–294.[CrossRef]
    [Google Scholar]
  32. Joly, E. & Hudrisier, D. ( 2003; ). What is trogocytosis and what is its purpose? Nat Immunol 4, 815.[CrossRef]
    [Google Scholar]
  33. Kobessho, H., Matsushita, A., Takahashi, K., Shimodaira, M., Ishihara, T., Oita, T. & Takahashi, T. ( 2002; ). Hepatic encephalopathy in primary human immunodeficiency virus type 1 (HIV-1) infection. Intern Med 41, 1069–1072.[CrossRef]
    [Google Scholar]
  34. Lambert, A. A., Gilbert, C., Richard, M., Beaulieu, A. D. & Tremblay, M. J. ( 2008; ). The C-type lectin surface receptor DCIR acts as a new attachment factor for HIV-1 in dendritic cells and contributes to trans- and cis-infection pathways. Blood 112, 1299–1307.[CrossRef]
    [Google Scholar]
  35. Larkin, M., Childs, R. A., Matthews, T. J., Thiel, S., Mizuochi, T., Lawson, A. M., Savill, J. S., Haslett, C., Diaz, R. & Feizi, T. ( 1989; ). Oligosaccharide-mediated interactions of the envelope glycoprotein gp120 of HIV-1 that are independent of CD4 recognition. AIDS 3, 793–798.[CrossRef]
    [Google Scholar]
  36. Lin, W., Weinberg, E. M., Tai, A. W., Peng, L. F., Brockman, M. A., Kim, K. A., Kim, S. S., Borges, C. B., Shao, R. X. & Chung, R. T. ( 2008; ). HIV increases HCV replication in a TGF-β1-dependent manner. Gastroenterology 134, 803–811.[CrossRef]
    [Google Scholar]
  37. Lindenbach, B. D., Evans, M. J., Syder, A. J., Wölk, B., Tellinghuisen, T. L., Liu, C. C., Maruyama, T., Hynes, R. O., Burton, D. R. & other authors ( 2005; ). Complete replication of hepatitis C virus in cell culture. Science 309, 623–626.[CrossRef]
    [Google Scholar]
  38. Lusso, P., Cocchi, F., Balotta, C., Markham, P. D., Louie, A., Farci, P., Pal, R., Gallo, R. C. & Reitz, M. S., Jr ( 1995; ). Growth of macrophage-tropic and primary human immunodeficiency virus type 1 (HIV-1) isolates in a unique CD4+ T-cell clone (PM1): failure to downregulate CD4 and to interfere with cell-line-tropic HIV-1. J Virol 69, 3712–3720.
    [Google Scholar]
  39. Mack, M., Kleinschmidt, A., Brühl, H., Klier, C., Nelson, P. J., Cihak, J., Plachý, J., Stangassinger, M., Erfle, V. & Schlöndorff, D. ( 2000; ). Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med 6, 769–775.[CrossRef]
    [Google Scholar]
  40. Moir, S., Boissinot, M., Tremblay, M. & Poulin, L. ( 1997; ). CD4 deletion mutants evaluated for human immunodeficiency virus type 1 infectivity in a highly efficient system of expression and detection based on LTR-dependent reporter gene activation. J Virol Methods 65, 209–217.[CrossRef]
    [Google Scholar]
  41. Molina, J. M., Welker, Y., Ferchal, F., Decazes, J. M., Shenmetzler, C. & Modaï, J. ( 1992; ). Hepatitis associated with primary HIV infection. Gastroenterology 102, 739.
    [Google Scholar]
  42. Mondor, I., Ugolini, S. & Sattentau, Q. J. ( 1998; ). Human immunodeficiency virus type 1 attachment to HeLa CD4 cells is CD4 independent and gp120 dependent and requires cell surface heparans. J Virol 72, 3623–3634.
    [Google Scholar]
  43. Moore, J. S., Hall, S. D. & Jackson, S. ( 2002; ). Cell-associated HIV-1 infection of salivary gland epithelial cell lines. Virology 297, 89–97.[CrossRef]
    [Google Scholar]
  44. Niu, M. T., Stein, D. S. & Schnittman, S. M. ( 1993; ). Primary human immunodeficiency virus type 1 infection: review of pathogenesis and early treatment intervention in humans and animal retrovirus infections. J Infect Dis 168, 1490–1501.[CrossRef]
    [Google Scholar]
  45. Niu, X., Gupta, K., Yang, J. T., Shamblott, M. J. & Levchenko, A. ( 2009; ). Physical transfer of membrane and cytoplasmic components as a general mechanism of cell-cell communication. J Cell Sci 122, 600–610.[CrossRef]
    [Google Scholar]
  46. Platt, E. J., Wehrly, K., Kuhmann, S. E., Chesebro, B. & Kabat, D. ( 1998; ). Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 72, 2855–2864.
    [Google Scholar]
  47. Pöhlmann, S., Soilleux, E. J., Baribaud, F., Leslie, G. J., Morris, L. S., Trowsdale, J., Lee, B., Coleman, N. & Doms, R. W. ( 2001; ). DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans. Proc Natl Acad Sci U S A 98, 2670–2675.[CrossRef]
    [Google Scholar]
  48. Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A. & Ratajczak, M. Z. ( 2006; ). Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487–1495.[CrossRef]
    [Google Scholar]
  49. Rozmyslowicz, T., Majka, M., Kijowski, J., Murphy, S. L., Conover, D. O., Poncz, M., Ratajczak, J., Gaulton, G. N. & Ratajczak, M. Z. ( 2003; ). Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS 17, 33–42.[CrossRef]
    [Google Scholar]
  50. Schmitt, M. P., Gendrault, J. L., Schweitzer, C., Steffan, A. M., Beyer, C., Royer, C., Jaeck, D., Pasquali, J. L., Kirn, A. & Aubertin, A. M. ( 1990; ). Permissivity of primary cultures of human Kupffer cells for HIV-1. AIDS Res Hum Retroviruses 6, 987–991.
    [Google Scholar]
  51. Seddiki, N., Ramdani, A., Saffar, L., Portoukalian, J., Gluckman, J. C. & Gattegno, L. ( 1994; ). A monoclonal antibody directed to sulfatide inhibits the binding of human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein to macrophages but not their infection by the virus. Biochim Biophys Acta 1225, 289–296.[CrossRef]
    [Google Scholar]
  52. Soto, B., Sánchez-Quijano, A., Rodrigo, L., del Olmo, J. A., García-Bengoechea, M., Hernández-Quero, J., Rey, C., Abad, M. A., Rodríguez, M. & other authors ( 1997; ). Human immunodeficiency virus infection modifies the natural history of chronic parenterally-acquired hepatitis C with an unusually rapid progression to cirrhosis. J Hepatol 26, 1–5.
    [Google Scholar]
  53. Speck, R. F., Esser, U., Penn, M. L., Eckstein, D. A., Pulliam, L., Chan, S. Y. & Goldsmith, M. A. ( 1999; ). A trans-receptor mechanism for infection of CD4-negative cells by human immunodeficiency virus type 1. Curr Biol 9, 547–550.
    [Google Scholar]
  54. Steffan, A. M., Lafon, M. E., Gendrault, J. L., Schweitzer, C., Royer, C., Jaeck, D., Arnaud, J. P., Schmitt, M. P., Aubertin, A. M. & Kirn, A. ( 1992; ). Primary cultures of endothelial cells from the human liver sinusoid are permissive for human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 89, 1582–1586.[CrossRef]
    [Google Scholar]
  55. Suzuki, Y., Misawa, N., Sato, C., Ebina, H., Masuda, T., Yamamoto, N. & Koyanagi, Y. ( 2003; ). Quantitative analysis of human immunodeficiency virus type 1 DNA dynamics by real-time PCR: integration efficiency in stimulated and unstimulated peripheral blood mononuclear cells. Virus Genes 27, 177–188.[CrossRef]
    [Google Scholar]
  56. Svarovskaia, E. S., Barr, R., Zhang, X., Pais, G. C., Marchand, C., Pommier, Y., Burke, T. R., Jr & Pathak, V. K. ( 2004; ). Azido-containing diketo acid derivatives inhibit human immunodeficiency virus type 1 integrase in vivo and influence the frequency of deletions at two-long-terminal-repeat-circle junctions. J Virol 78, 3210–3222.[CrossRef]
    [Google Scholar]
  57. Takeuchi, Y., McClure, M. O. & Pizzato, M. ( 2008; ). Identification of gammaretroviruses constitutively released from cell lines used for human immunodeficiency virus research. J Virol 82, 12585–12588.[CrossRef]
    [Google Scholar]
  58. Tuyama, A. C., Hong, F. & Schecter, A. D. ( 2007; ). HIV entry and replication in stellate cells promotes cellular activation and fibrogenesis: implications for hepatic fibrosis in HIV/HCV coinfection. In 58th Annual Meeting of the American Association for the Study of Liver Diseases (AASLD), abstract LB3, p. 2–6. Boston: John Wiley & Son.
  59. Vlahakis, S. R., Villasis-Keever, A., Gomez, T. S., Bren, G. D. & Paya, C. V. ( 2003; ). Human immunodeficiency virus-induced apoptosis of human hepatocytes via CXCR4. J Infect Dis 188, 1455–1460.[CrossRef]
    [Google Scholar]
  60. Warren, A., Le Couteur, D. G., Fraser, R., Bowen, D. G., McCaughan, G. W. & Bertolino, P. ( 2006; ). T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells. Hepatology 44, 1182–1190.[CrossRef]
    [Google Scholar]
  61. Weber, R., Sabin, C. A., Friis-Møller, N., Reiss, P., El-Sadr, W. M., Kirk, O., Dabis, F., Law, M. G., Pradier, C. & other authors ( 2006; ). Liver-related deaths in persons infected with the human immunodeficiency virus: the D:A:D study. Arch Intern Med 166, 1632–1641.[CrossRef]
    [Google Scholar]
  62. Wei, X., Decker, J. M., Liu, H., Zhang, Z., Arani, R. B., Kilby, J. M., Saag, M. S., Wu, X., Shaw, G. M. & Kappes, J. C. ( 2002; ). Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46, 1896–1905.[CrossRef]
    [Google Scholar]
  63. Xiao, P., Usami, O., Suzuki, Y., Ling, H., Shimizu, N., Hoshino, H., Zhuang, M., Ashino, Y., Gu, H. & Hattori, T. ( 2008; ). Characterization of a CD4-independent clinical HIV-1 that can efficiently infect human hepatocytes through chemokine (C-X-C motif) receptor 4. AIDS 22, 1749–1757.[CrossRef]
    [Google Scholar]
  64. Yahi, N., Baghdiguian, S., Moreau, H. & Fantini, J. ( 1992; ). Galactosyl ceramide (or a closely related molecule) is the receptor for human immunodeficiency virus type 1 on human colon epithelial HT29 cells. J Virol 66, 4848–4854.
    [Google Scholar]
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