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Volume 75, Issue 11

The Asialoglycoprotein Receptor Mediates Hepatic Binding and Uptake of Natural Hepatitis B Virus Particles Derived From Viraemic Carriers Free

Abstract

As a putative mechanism of hepatitis B virus (HBV) uptake into hepatocytes the interaction between HBV and the hepatic, human-derived asialoglycoprotein receptor (ASGPR) was investigated. Sera from patients with different variations of hepatitis B surface antigen-(HBsAg) positive chronic hepatitis, HBV particles isolated from HBV carriers with high-titre viraemia and commercial HBsAg served as sources of HBV. ASGPR was affinity-purified from human liver. HBV that had bound to isolated ASGPR was either detected by radio-immunoassay using solid-phase bound ASGPR or enzyme immunoassay with biotin-ASGPR bound to immobilized HBV. Furthermore, binding and uptake of purified, I-labelled HBV particles into human hepatoma cell lines (HepG2 and HuH7), which constitutively express functional ASGPR molecules, were compared to that of ASGPR-negative COS cells. As a result HBV was found to bind to purified human ASGPR in two different assays. Circulating virus particles from sera with high titre viraemia showed the highest attachment activity to ASGPR. HBV binding to purified ASGPR was saturable and inhibitable by an excess of -galactose-bearing ligands, by EDTA and anti-receptor immunoglobulin. Lysis of particles by adding detergent abolished immunodetectable HBV binding to purified ASGPR. Commercial HBsAg did not adhere to solid phase-immobilized ASGPR. Monoclonal anti-preS1 antibody (MA18/7) but not anti-preS2 antibody (Q19/10) inhibited virus attachment. Purified and radiolabelled HBV particles showed binding to HepG2 and HuH7 cells but to much lesser degree to COS cells. Cellular binding of HBV was significantly inhibited by blocking of ASGPR function. Both ASGPR ligands and rabbit anti-ASGPR immunoglobulin but not non-immune rabbit serum inhibited uptake of radiolabelled HBV particles into HepG2 cells or HuH7 cells, respectively. This study suggests that HBV virions may enter human hepatocytes via ASGPR molecules by attachment of viral preS1-related envelope binding sites to this receptor.

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© The Journal of General Virology 1994
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1994-11-01
2024-05-06
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References

  1. Abdullah M., Kierszenbaum A. L. 1989; Identification of rat testis galactosyl receptor using antibodies to liver asialoglycoprotein receptor: purification and localization on surfaces of spermatogenic cells and sperm. Journal of Biological Chemistry 108:367–375
     [Google Scholar]
  2. Alberti A., Gerlich W. H., Heermann K. H., Pontisso P. 1990; Nature and display of hepatitis B virus envelope proteins and the humoral immune response. Springer Seminars in Immunopathology 12:5–23
     [Google Scholar]
  3. Bchini F., Capel F., Dauhuet C., Dubanchet S., Petit M. A. 1990; In vitro infection of human hepatoma (HepG2) cells with hepatitis B virus. Journal of Virology 64:3025–3032
     [Google Scholar]
  4. Dash S., Das K. V. S., Panda S. K. 1992; Receptor for preSl(21–47) component of hepatitis B virus on the liver cell: role in virus-cell interaction. Journal of Medical Virology 37:116–121
     [Google Scholar]
  5. Fogarty International Center Proceedings22DHEW Publication (NIH) 76–725 pp 9–11 1976; Disease of the liver and biliary tract: standardization of nomenclature, diagnostic criteria and diagnostic methodology. Washington DC: US Government Printing Office;
  6. Franco A., Paroli M., Testa U, Peschle C., Balsano V., Barnaba V. 1992; Transferrin receptor mediates uptake and presentation of hepatitis B envelope antigen by T- lymphocytes. Journal of Experimental Medicine 175:1195–1205
     [Google Scholar]
  7. Gerken G., Manns M., Gerlich W. H., Hess G., Meyer Zum Büschenfelde K. -H. 1987; Pre-S encoded surface proteins in relation to the major viral surface antigen in acute hepatitis B virus infection. Gastroenterology 92:1864–1868
     [Google Scholar]
  8. Gerken G., Manns M., Gerlich W. H., Hess G., Meyer Zum Büschenfelde K. -H. 1989; Immune blot analysis of viral surface proteins in serum and liver of patients with chronic hepatitis B virus infection. Journal of Medical Virology 29:261–265
     [Google Scholar]
  9. Gerken G., Kremsdorf G., Capel G., Petit M. A., Dauguet C., Manns M. P., Meyer Zum BÜschenfelde K. -H., Brechot C. 1991; Hepatitis B defective virus with rearrangements in the PreS gene during chronic HBV infection. Virology 183:555–565
     [Google Scholar]
  10. Gripon P., Diot C., Guguen-Guillouzo C. 1993; Reproducible high level infection of cultured adult hepatocytes by hepatitis B virus: effect of polyethylene glycol on absorption and penetration. Virology 192:534–540
     [Google Scholar]
  11. Harford J., Ashwell G. 1982; The hepatic receptor for asialoglycoproteins. In The Glycoconjugates 4 pp 27–55 Horowitz M. Edited by New York: Academic Press;
     [Google Scholar]
  12. Heermann K. H., Goldmann U., Schwartz W., Seyffahrt T., Baumgarten H., Gerlich W. H. 1984; Large surface protein of hepatitis B virus containing the pre-S sequence. Journal of Virology 52:396–402
     [Google Scholar]
  13. Hertogs K., Leenders W. P., Depla E., De-Bruin W. C., Meheus L., Raymackers J., Moshage H., Yap S. H. 1993; Endonexin II, present on human liver plasma membranes, is a specific binding protein of small hepatitis B virus (HBV) envelope protein. Virology 197:549–557
     [Google Scholar]
  14. Hoofnagle J. H., Seef L. B. 1982; Natural history of chronic type B hepatitis. In Progress in Liver Diseases 5 pp 469–477 Popper H., Schaffner F. Edited by New York: Grune & Stratton;
     [Google Scholar]
  15. Hu C., Lee E. Y., Hewitt J. E., Baenziger J. U., Mu J. Z., Deschryver-Kecskemeti D., Alpers D. H. 1991; The minor components of the rat asiaglycoprotein receptor are apically located in neonatal enterocytes. Gastroenterology 101:1477–1487
     [Google Scholar]
  16. Hubbard A. L., Wall D. A., Ma A. 1983; Isolation of rat hepatocyte plasma membranes. 1. Presence of the three major domains. Journal of Cell Biology 96:217–229
     [Google Scholar]
  17. Kaiser J., Stockert R. J., Schein P. S., Wolkoff A. W. 1986; Recognition of hepatitis B surface antigen by the human hepatoma cell line HepG2. Transactions of the Association of American Physicians 69:86–91
     [Google Scholar]
  18. Kolb-Bachofen V. 1991; A membrane-bound form of the acute- phase protein C-reactive protein is the galactose-specific particle receptor on rat liver macrophages. Pathobiology 59:272–275
     [Google Scholar]
  19. Kuroda S., Otaka S., Miyazaki T., Nakao M., Fujisawa Y. 1992; Hepatitis B virus envelope L protein particles. Journal of Biological Chemistry 267:1953–1961
     [Google Scholar]
  20. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. 1951; Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193:265–275
     [Google Scholar]
  21. Meijer D. K. F., Jansen R. W., Molema G. 1992; Drug targeting systems for antiviral agents: options and limitations. Antiviral Research 18:215–258
     [Google Scholar]
  22. Morell A. G., Irving R. A., Sternlieb I., Scheinberg I. H., Ashwell G. 1968; Physical and chemical studies on ceruloplasmin. V. Metabolic studies on sialic acid-free ceruloplasmin in vivo. Journal of Biological Chemistry 243:155–159
     [Google Scholar]
  23. Nakabayashi H., Taketa K., Myano K., Yamane T., Sato J. 1982; Growth of human hepatoma cell lines with differentiated functions in chemically defined medium. Cancer Research 42:3858–3862
     [Google Scholar]
  24. Neurath A., Strick N., Sproul P. 1992; Search for hepatitis B virus cell receptors reveals binding sites for interleukin 6 on the virus envelope protein. Journal of Experimental Medicine 175:461–459
     [Google Scholar]
  25. Paietta E., Stockert R. J., Racevskis J. 1992; Differences in the abundance of variably spliced receptor polypeptide, H2, in normal and transformed human liver. Hepatology 15:395–402
     [Google Scholar]
  26. Petit M. A., Dubanechet S., Capel F. 1989; A monoclonal antibody specific for the hepatocyte receptor binding site on hepatitis B virus. Molecular Immunology 26:531–537
     [Google Scholar]
  27. Petit M. A., Zoulim F., Capel F. 1990; Variable expression of preSl antigen in serum during chronic hepatitis B virus infection: an accurate marker for the level of hepatitis B virus replication. Hepatology 11:809–814
     [Google Scholar]
  28. Petit M. A., Duchanchet F., Capel F., Voet F., Dauguet C., Hauser P. 1991; HepG2 cell binding activities of different hepatitis B virus isolates: inhibitory effect of anti-HBs and anti-preSl(21–47). Virology 180:483–491
     [Google Scholar]
  29. Pontisso P., Petit M. A., Bankowski M. J., Peeples M. 1989; Human liver plasma membranes contain receptors for the hepatitis B virus preSl region and, via polymerized human serum albumin, for the preS2 region. Journal of Virology 63:1981–1988
     [Google Scholar]
  30. Pontisso P., Ruvoletto M. G., Gerlich W. H., Heermann K. H., Bardini F., Alberti A. 1990; Identification of an attachment site for human liver plasma membranes on hepatitis B virus particles. Virology 173:522–527
     [Google Scholar]
  31. Pontisso P., Morsica P., Ruvoletto M. G., Zambello R., Colletta R., Chemello L., Alberti A. 1991; Hepatitis B virus binds to peripheral blood mononuclear cells via the preSl protein. Journal of Hepatology 12:203–206
     [Google Scholar]
  32. Schwartz A. L., Fridovich S. E., Lodish H. F. 1982; Kinetics of internalization and recycling of the asialoglycoprotein receptor in two hepatoma cell lines. Journal of Biological Chemistry 257:4230–4237
     [Google Scholar]
  33. Shia M. A., Lodish FI. F. 1989; The two subunits of the human asialoglycoprotein receptor have different fates when expressed alone in fibroblasts. Proceedings of the National Academy of Sciences U.S.A: 861158–1162
     [Google Scholar]
  34. Spiess M. 1990; The asialoglycoprotein receptor: a model for endocytotic transport receptors. Biochemistry 29:10009–10018
     [Google Scholar]
  35. Stockert R. J., Morell A. G. 1990; Second messenger modulation of the asialoglycoprotein receptor. Journal of Biological Chemistry 265:1841–1846
     [Google Scholar]
  36. Treichel U., Roos P. H., Kolb H. 1989; The hepatic asialoglycoprotein receptor selectively binds to some endogenous tissue. European Journal of Cell Biology 48:116–120
     [Google Scholar]
  37. Treichel U., Poralla T., Hess G., Manns M., Meyer Zum Büschenfelde K. -H. 1990; Autoantibodies to human asialoglycoprotein receptor in autoimmune type chronic active hepatitis. Hepatology 11:606–612
     [Google Scholar]
  38. Treichel U., Paietta E., Poralla T., Meyer Zum Büschenfelde K. -H., Stockert R. J. 1994; Effects of cytokines on synthesis and function of the hepatic asialoglycoprotein receptor. Journal of Cellular Physiology 158:527–534
     [Google Scholar]
  39. Wong D. T., Nath N., Sninsky J. J. 1985; Identification of the hepatitis B virus polypeptides encoded by the entire pre-S open reading frame. Journal of Virology 55:223–231
     [Google Scholar]
  40. Williams R. K., Jiang G. S., Holmes K. V. 1991; Receptor for mouse hepatitis virus is a member of the carcinoembryonic antigen family of glycoproteins. Proceedings of the National Academy of Sciences U.S.A: 885533–5536
     [Google Scholar]
  41. Wu G. Y., Wu C. H. 1988; Receptor-mediated gene delivery and expression in vivo. Journal of Biological Chemistry 263:14621–14624
     [Google Scholar]
  42. Wu G. Y., Zhang P., Rowell R. J., Wu C. H. 1992; Modification of inactivated adenovirus with a targetable DNA carrier enhances foreign gene expression in vitro and in vivo. Hepatology 16:112
     [Google Scholar]
  43. Yu Ip C. C., Miller W. J., Kubek D. J. 1992; Structural characterisation of the N-glycans of a recombinant hepatitis B surface antigen derived from yeast. Biochemistry 31:285–295
     [Google Scholar]
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The Asialoglycoprotein Receptor Mediates Hepatic Binding and Uptake of Natural Hepatitis B Virus Particles Derived From Viraemic Carriers
J. Gen. Virol. 75, 3021 (1994); https://doi.org/10.1099/0022-1317-75-11-3021
/content/journal/jgv/10.1099/0022-1317-75-11-3021
/content/journal/jgv/10.1099/0022-1317-75-11-3021
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