1887

Journal of General Virology header logo

Volume 80, Issue 3

A cellular protein which binds hepatitis B virus but not hepatitis B surface antigen. Free

Abstract

The envelope of hepatitis B virus (HBV) consists of three related proteins known as the large (L), middle (M) and small (S) hepatitis B surface antigens (HBsAg). L-HBsAg has a 108-119 amino acid extension at the N terminus compared with M-HBsAg and contains the preS1 sequence of the HBV envelope. Previous research has identified this region as the likely virus attachment protein which is thought to interact with the cellular receptor for the virus. However, as the receptor has still not been identified unequivocally, we used the preS1 region of L-HBsAg to screen a human liver cDNA library by the yeast two-hybrid system. Several positive clones were isolated which encoded cellular proteins that interacted with the HBV preS1 protein. The specificity was examined in an independent manner in experiments in which baculovirus-derived glutathione S-transferase (GST)-preS1 was incubated with 35S-labelled protein expressed by in vitro translation from the positive clones. The intensity of the interactions using this alternative approach mirrored those observed in the yeast two-hybrid system and two proteins (an unidentified protein and a mitochondrial protein) were selected for further study. The specificity of the binding reaction between the preS1 protein and these two proteins was further confirmed in a competition assay; HBV purified from serum, but not purified HBsAg, was able to compete with preS1 and thus block GST-preS1 binding to the unidentified protein but not to the mitochondrial protein. The unidentified protein was then expressed as a fusion protein with GST and this was able to bind HBV virions in a direct manner.

  • Received:
  • Accepted:
  • Published Online:
© Journal of General Virology 1999
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-80-3-607
1999-03-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/jgv/80/3/0800607a.html?itemId=/content/journal/jgv/10.1099/0022-1317-80-3-607&mimeType=html&fmt=ahah

References

  1. Barker L. F., Maynard J. E., Purcell R. H., Hoofnagle J. H., Berquist K. R., London W. T. 1975; Viral hepatitis, type B, in experimental animals. American Journal of Medical Sciences 270:189–196
     [Google Scholar]
  2. Brazas R., Ganem D. 1996; A cellular homolog of hepatitis delta antigen: implications for viral replication and evolution. Science 274:90–94
     [Google Scholar]
  3. Breiner K. M., Urban S., Schaller H. 1998; Carboxypeptidase D (gp180), a Golgi-resident protein, functions in the attachment and entry of avian hepatitis B viruses. Journal of Virology 72:8098–8104
     [Google Scholar]
  4. Budkowska A., Quan C., Groh F., Bedossa P., Dubreuil P., Bouvet J. P., Pillot J. 1993; Hepatitis B virus (HBV) binding factor in human serum: candidate for a soluble form of hepatocyte HBV receptor. Journal of Virology 67:4316–4322
     [Google Scholar]
  5. Budkowska A., Bedossa P., Groh F., Louise A., Pillot J. 1995; Fibronectin of human liver sinusoids binds hepatitis B virus: identification by an anti-idiotypic antibody bearing the internal image of the pre-S2 domain. Journal of Virology 69:840–848
     [Google Scholar]
  6. Chien C. T., Bartel P. L., Sternglanz R., Fields S. 1991; The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proceedings of the National Academy of Sciences, USA 88:9578–9582
     [Google Scholar]
  7. Dash S., Rao K., Panda S. 1992; Receptor for PreS1 (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]
  8. De Meyer S., Gong Z. J., Suwandhi W., van Pelt J., Soumillion A., Yap S. H. 1997; Organ and species specificity of hepatitis B virus (HBV) infection: a review of literature with a special reference to preferential attachment of HBV to human hepatocytes. Journal of Viral Hepatitis 4:145–153
     [Google Scholar]
  9. Fields S., Song O. 1989; A novel genetic system to detect protein-protein interactions. Nature 340:245–247
     [Google Scholar]
  10. Fowler K. J., Brown R. M., Cotton R. G. H. 1983; Elimination of Mycoplasma orale from the human hepatoma cell line PLC/PRF/5. Experimental Cell Research 149:303–306
     [Google Scholar]
  11. Franco A., Paroli M., Testa U., Benvenuto R., 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]
  12. Galibert F., Mandart E., Fitoussi F., Tiollais P., Charnay P. 1979; Nucleotide sequence of the hepatitis B virus genome (subtype ayw) cloned in E. coli . Nature 281:646–650
     [Google Scholar]
  13. Ganem D. 1996; Hepadnaviridae and their replication. In Fields Virology 3rd edn pp 2073–2737 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott-Raven;
     [Google Scholar]
  14. Gietz D., St Jean A., Woods R. A., Schiestl R. H. 1992; Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Research 20:1425
     [Google Scholar]
  15. Hansen H., Svensson U., Zhu J., Laviola L., Giorgino F., Wolf G., Smith R. J., Riedel H. 1996; Interaction between the Grb10 SH2 domain and the insulin receptor carboxyl terminus. Journal of Biological Chemistry 271:8882–8886
     [Google Scholar]
  16. Harvey T. J., Macnaughton T. B., Gowans E. J. 1997; The development and characterisation of a SV40 T-antigen positive cell line of human hepatic origin. Journal of Virological Methods 65:67–74
     [Google Scholar]
  17. Heermann K. H., Goldmann U., Schwartz W., Seyffarht T., Baumgarten H., Gerlich W. H. 1984; Large surface protein of hepatitis B virus containing the preS sequence. Journal of Virology 52:396–402
     [Google Scholar]
  18. Hertogs K., Leenders W. P. J., 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]
  19. Hong H., Kohli K., Trivedi A., Johnson D. L., Stallcup M. R. 1996; GRIP1, a novel mouse protein that serves as a transcriptional coactivator in yeast for the hormone binding domains of steroid receptors. Proceedings of the National Academy of Sciences, USA 93:4948–4952
     [Google Scholar]
  20. Ito H., Fukada Y., Murata K., Kimura A. 1983; Transformation of intact yeast cells treated with alkali cations. Journal of Bacteriology 153:163–168
     [Google Scholar]
  21. Klingmuller U., Schaller H. 1993; Hepadnavirus infection requires interaction between the viral pre-S domain and a specific hepatocellular receptor. Journal of Virology 67:7414–7422
     [Google Scholar]
  22. Komai K., Peeples M. 1990; Physiology and function of the Vero cell receptor for the hepatitis B virus small S protein. Virology 177:332–338
     [Google Scholar]
  23. Kuroki K., Cheung R., Marion P. L., Ganem D. 1994; A cell surface protein that binds avian hepatitis B virus particles. Journal of Virology 68:2091–2096
     [Google Scholar]
  24. Kuroki K., Eng F., Ishikawa T., Turck C., Harada F., Ganem D. 1995; gp180, a host cell glycoprotein that binds duck hepatitis B virus particles, is encoded by a member of the carboxypeptidase gene family. Journal of Biological Chemistry 270:15022–15028
     [Google Scholar]
  25. Lee T. H., Elledge S. J., Butel J. S. 1995; Hepatitis B virus X protein interacts with a probable cellular DNA repair protein. Journal of Virology 69:1107–1114
     [Google Scholar]
  26. Leenders W. P., Glansbeek H. L., De Bruin W. C., Yap S. H. 1990; Binding of the major and large HBsAg to human hepatocytes and liver plasma membranes; putative external and internal receptors for infection and secretion of hepatitis B virus. Hepatology 12:141–147
     [Google Scholar]
  27. Machida A., Kishimoto S., Ohnuma H., Miyamoto H., Baba K., Oda K., Nakamura T., Miyakawa Y., Mayuma M. 1983; A hepatitis B surface antigen polypeptide (p31) with the receptor for polymerized human as well as chimpanzee albumin. Gastroenterology 86:268–274
     [Google Scholar]
  28. Matsumoto M., Hsieh T.-Y., Zhu N., VanArsdale T., Hwang S. B., Jeng K.-S., Gorbalenya A. E., Lo S.-Y., Ou J.-H., Ware C. F., Lai M. M. C. 1997; Hepatitis C virus core protein interacts with the cytoplasmic tail of lymphotoxin-β receptor. Journal of Virology 71:1301–1309
     [Google Scholar]
  29. Mehdi H., Kaplan M. J., Anlar F. Y., Yang X., Bayer R., Sutherland K., Peeples M. E. 1994; Hepatitis B virus surface antigen binds to apolipoprotein H. Journal of Virology 68:2415–2424
     [Google Scholar]
  30. Neurath A. R., Kent S. B. H., Parker K., Prince A. M., Strick N., Brotman B., Sproul P. 1986a; Antibodies to a synthetic peptide from the pre-S 120–145 region of the hepatitis B virus envelope are virus–neutralizing. Vaccine 4:35–37
     [Google Scholar]
  31. Neurath A. R., Kent S. B. H., Strick N., Parker K. 1986b; Identification and chemical synthesis of a host cell receptor binding site on hepatitis B virus. Cell 46:426–436
     [Google Scholar]
  32. Neurath A. R., Strick N., Li Y. Y. 1992; Cells transfected with human interleukin 6 cDNA acquire binding sites for the hepatitis B virus envelope protein. Journal of Experimental Medicine 176:1561–1569
     [Google Scholar]
  33. Niethammer M., Kim E., Sheng M. 1996; Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. Journal of Neuroscience 16:2157–2163
     [Google Scholar]
  34. Onate S. A., Tsai S. Y., Tsai M. J., O’Malley B. W. 1995; Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 270:1354–1357
     [Google Scholar]
  35. O’Neill T. J., Craparo A., Gustafson T. A. 1994; Characterization of an interaction between insulin receptor substrate 1 and the insulin receptor by using the two-hybrid system. Molecular and Cellular Biology 14:6433–6442
     [Google Scholar]
  36. Petit M. A., Capel F., Dubanchet S., Mabit H. 1992; PreS1-specific binding proteins as potential receptors for hepatitis B virus in human hepatocytes. Virology 187:211–222
     [Google Scholar]
  37. Pontisso P., Petit M. A., Bankowski M. J., Peeples M. E. 1989; Human liver plasma membranes contain receptors for the hepatitis B virus pre S1 region and, via polymerized human serum albumin, for the pre S2 region. Journal of Virology 63:1981–1988
     [Google Scholar]
  38. Pontisso P., Ruvoletto M. G., Tiribelli C., Gerlich W. H., Ruol A., Alberti A. 1992; The preS1 domain of hepatitis B virus and IgA cross-react in their binding to the hepatocyte surface. Journal of General Virology 73:2041–2045
     [Google Scholar]
  39. Qiao M., Macnaughton T. B., Gowans E. J. 1994; Adsorption and penetration of hepatitis B virus in a nonpermissive cell line. Virology 201:356–363
     [Google Scholar]
  40. Rice C. M., Grakuoi A., Galler R., Chambers T. J. 1989; Transcription of infectious yellow fever RNA from full-length cDNA templates produced by in vitro ligation. Nature New Biologist 1:285–296
     [Google Scholar]
  41. Rossi F., Gallina A., Milanesi G. 1996; Nef-CD4 physical interaction sensed with the yeast two-hybrid system. Virology 217:397–403
     [Google Scholar]
  42. Sells M. A., Chen M.-L., Acs G. 1987; Production of hepatitis B virus particles in HepG2 cells transfected with cloned hepatitis B virus DNA. Proceedings of the National Academy of Sciences, USA 84:1005–1009
     [Google Scholar]
  43. Shih C., Yu M. Y., Li L. S., Shih J. W. 1990; Hepatitis B virus propagated in a rat hepatoma cell line is infectious in a primate model. Virology 179:871–873
     [Google Scholar]
  44. Sureau C., Lanford R. 1993; Analysis of hepatitis B virus envelope proteins in assembly and infectivity of human hepatitis delta virus. Progress in Clinical and Biological Research 382:45–51
     [Google Scholar]
  45. Sureau C., Romet-Lemonne J. L., Mullins J. I., Essex M. 1986; Production of hepatitis B virus by a differentiated human hepatoma cell line after transfection with cloned circular HBV DNA. Cell 47:37–47
     [Google Scholar]
  46. Sureau C., Guerra B., Lanford R. E. 1993; Role of the large hepatitis B virus envelope protein in infectivity of the hepatitis delta virion. Journal of Virology 67:366–372
     [Google Scholar]
  47. Tong S., Li J., Wands J. R. 1995; Interaction between duck hepatitis B virus and a 170-kilodalton cellular protein is mediated through a neutralizing epitope of the pre-S region and occurs during viral infection. Journal of Virology 69:7106–7112
     [Google Scholar]
  48. Treichel U., Meyer zum Buschenfelde K.-H., Stockert R. J., Poralla T., Gerken G. 1994; The asialoglycoprotein receptor mediates hepatic binding and uptake of natural hepatitis B virus particles derived from viraemic carriers. Journal of General Virology 75:3021–3029
     [Google Scholar]
  49. Tsurimoto T., Fujiyama A., Matsubara K. 1987; Stable expression and replication of hepatitis B virus genome in an integrated state in a human hepatoma cell line transfected with the cloned viral DNA. Proceedings of the National Academy of Sciences, USA 84:444–448
     [Google Scholar]
  50. Wang Y.-H., Davies A. H., Jones I. M. 1995; Expression and purification of glutathione S-transferase-tagged HIV-1 gp120: no evidence of an interaction with CD26. Virology 208:142–146
     [Google Scholar]
  51. Yeh S., Chang C. 1996; Cloning and characterization of a specific coactivator, ARA70, for the androgen receptor in human prostate cells. Proceedings of the National Academy of Sciences, USA 93:5517–5521
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-80-3-607
Loading
A cellular protein which binds hepatitis B virus but not hepatitis B surface antigen.
J. Gen. Virol. 80, 607 (1999); https://doi.org/10.1099/0022-1317-80-3-607
/content/journal/jgv/10.1099/0022-1317-80-3-607
/content/journal/jgv/10.1099/0022-1317-80-3-607
Loading

Data & Media loading...

Most cited 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