1887

Abstract

It was observed recently that recombinant yeast-derived hepatitis B surface antigen (rHBsAg) particles, which contain the S protein only, bind almost exclusively to monocytes. It is shown here that binding requires the presence of the LPS receptor CD14. Furthermore, evidence is presented that a domain on CD14 that is identical to or largely overlaps with the LPS-binding pocket is instrumental for the attachment of rHBsAg. Additionally, it is shown that the heat-labile LPS-binding protein (LBP) catalyses the binding of rHBsAg to the cells. Remarkably, natural plasma-derived HBsAg (pHBsAg) does not have this property. pHBsAg devoid of its lipids and reconstituted with phosphatidylserine or phosphatidylglycerol acquires the characteristic of yeast-derived HBsAg. Clearly, the interaction of rHBsAg with the cell membrane is determined by the presence of charged phospholipids that are absent in pHBsAg. Although a lipid–receptor interaction is suggested, antibody-inhibition experiments suggest a possible involvement of the C-terminal region of the S protein in the interaction with monocytes. The possible implications of these observations for hepatitis B virus (HBV) infection and HBV vaccine efficiency are discussed.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-9-2279
2002-09-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/9/0832279a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-9-2279&mimeType=html&fmt=ahah

References

  1. Baijot M. 1991; Protein arrangement in the yeast-derived hepatitis B surface antigen particles . PhD thesis Université Catholique de Louvain; Belgium:
  2. Bazil V., Strominger J. L. 1991; Shedding as a mechanism of down-modulation of CD14 on stimulated human monocytes. Journal of Immunology 147:1567–1574
    [Google Scholar]
  3. 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]
  4. Chen Y.-C., Delbrook K., Dealwis C., Mimms L., Mushawar I. K., Mandecki W. 1996; Discontinuous epitopes of hepatitis B surface antigen derived from a filamentous phage peptide library. Proceedings of the National Academy of Sciences, USA 93:1997–2001
    [Google Scholar]
  5. Chisari F. V. 2000; Rous-Whipple Award Lecture. Viruses, immunity, and cancer: lessons from hepatitis B. American Journal of Pathology 156:1118–1132
    [Google Scholar]
  6. De Falco S., Ruvoletto M. G., Verdoliva A., Ruvo M., Raucci A., Marino M., Senatore S., Cassani G., Alberti A., Pontisso P., Fassina G. 2001; Cloning and expression of a novel hepatitis B virus-binding protein from HepG2 cells. Journal of Biological Chemistry 276:36613–36623
    [Google Scholar]
  7. De Meyer S., Gong Z., Depla E., Maertens G., Yap S. H. 1999; Involvement of phosphatidylserine and non-phospholipid components of the hepatitis B virus envelope in human Annexin V binding and in HBV infection in vitro . Journal of Hepatology 31:783–790
    [Google Scholar]
  8. Diminsky D., Schrimbeck R., Reimann J., Barenholz Y. 1997; Comparison between hepatitis B surface antigen (HBsAg) particles derived from mammalian cells (CHO) and yeast cells ( Hansenula polymorpha ): composition, structure and immunogenicity. Vaccine 15:637–647
    [Google Scholar]
  9. Diminsky D., Moav N., Gorecki M., Barenholz Y. 2000; Physical, chemical and immunological stability of CHO-derived hepatitis B surface antigen (HBsAg) particles. Vaccine 18:3–17
    [Google Scholar]
  10. Franco A., Paroli M., Testa U., Benvenuto R., Peschle C., Balsano F., Barnaba V. 1992; Transferrin receptor mediates uptake and presentation of hepatitis B envelope antigen by T lymphocytes. Journal of Experimental Medicine 175:1095–1105
    [Google Scholar]
  11. Ganem D. 1996; Hepadnaviridae and their replication. In Fields Virology pp 2703–2738 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  12. Gavilanes F., Gonzalez-Ros J. M., Peterson D. L. 1982; Structure of hepatitis B surface antigen. Characterization of the lipid components and their association with the viral proteins. Journal of Biological Chemistry 257:7770–7777
    [Google Scholar]
  13. Gavilanes F., Gomez-Gutierrez J., Aracil M., Gonzalez-Ros J. M., Ferragut J. A., Guerrero E., Peterson D. L. 1990; Hepatitis B surface antigen. Role of lipids in maintaining the structural and antigenic properties of protein components. Biochemical Journal 265:857–864
    [Google Scholar]
  14. Gerlich W. H., Lu X., Heermann K. H. 1993; Studies on the attachment and penetration of hepatitis B virus. Journal of Hepatology 17 (Suppl. 3):S10–S14
    [Google Scholar]
  15. Gomez-Gutierrez J., Rodriguez-Crespo I., Peterson D. L., Gavilanes F. 1994; Reconstitution of hepatitis B surface antigen proteins into phospholipid vesicles. Biochimica et Biophysica Acta 1192:45–52
    [Google Scholar]
  16. Gomez-Gutierrez J., Rodriguez-Crespo I., Peterson D. L., Gavilanes F. 1995; Antigenicity of hepatitis B surface antigen proteins reconstituted with phospholipids. Biochimica et Biophysica Acta 1233:205–212
    [Google Scholar]
  17. Haziot A., Chen S., Ferrero E., Low M. G., Silber R., Goyert S. M. 1988; The monocyte differentiation antigen, CD14, is anchored to the cell membrane by a phosphatidylinositol linkage. Journal of Immunology 141:547–552
    [Google Scholar]
  18. Heijtink R. A., Kruining J., Bakker M., Schalm S. W. 1985; Immune response after vaccination with recombinant hepatitis B vaccine as compared to that after plasma-derived vaccine. Antiviral Research 8 (Suppl. 1):273–279
    [Google Scholar]
  19. Heijtink R. A., van Bergen P., Paulij W. P., de Man R. A., Osterhaus A. D. M. E. 2000; Anti-HBs characteristics after hepatitis B immunisation with plasma-derived and recombinant DNA-derived vaccines. Vaccine 18:1531–1538
    [Google Scholar]
  20. Hertogs K., Leenders W. P. J., Depla E., De Bruin W. C. 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]
  21. Imai M., Yanase Y., Nojiri T., Miyakawa Y., Mayumi M. 1979; A receptor for polymerized human and chimpanzee albumins on hepatitis B virus particles co-occurring with HBeAg. Gastroenterology 76:242–247
    [Google Scholar]
  22. Jack R. S., Grunwald U., Stelter F., Workalemahu G., Schutt C. 1995; Both membrane-bound and soluble forms of CD14 bind to gram-negative bacteria. European Journal of Immunology 25:1436–1441
    [Google Scholar]
  23. Jilg W., Lorbeer B., Schmidt M., Wilske B., Zoulek G., Deinhardt F. 1984; Clinical evaluation of a recombinant hepatitis B vaccine. Lancet ii:1174–1175
    [Google Scholar]
  24. Jolivet-Reynaud C., Lésenéchal M., O’Donnell B., Becquart L., Foussadier A., Forge F., Battail-Poirot N., Lacoux X., Carman W., Jolivet M. 2001; Localization of hepatitis B surface antigen epitopes present on variants and specifically recognised by anti-hepatitis B surface antigen monoclonal antibodies. Journal of Medical Virology 65:241–249
    [Google Scholar]
  25. Kim C. Y., Bissell D. M. 1971; Stability of the lipid and protein of hepatitis-associated (Australia) antigen. Journal of Infectious Diseases 123:470–476
    [Google Scholar]
  26. Leroux-Roels G., Cao T., De Knibber A., Meuleman P., Roobrouck A., Farhoudi A., Vanlandschoot P., Desombere I. 2001; Prevention of hepatitis B infections: vaccination and its limitation. Acta Clinica Belgica 56:209–219
    [Google Scholar]
  27. Manesis E. K., Cameron C. H., Gregoriadis G. 1979; Hepatitis B surface antigen-containing liposomes enhance humoral and cell-mediated immunity to the antigen. FEBS Letters 102:107–111
    [Google Scholar]
  28. 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]
  29. Meszaros K., Aberle S., White M., Parent J. B. 1995; Immunoreactivity and bioactivity of lipopolysaccharide-binding protein in normal and heat-inactivated sera. Infection and Immunity 63:363–365
    [Google Scholar]
  30. Neurath A. R., Strick N. 1994; The putative cell receptors for hepatitis B virus (HBV), annexin V, and apolipoprotein H, bind to lipid components of HBV. Virology 204:475–477
    [Google Scholar]
  31. Neurath A. R., 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 175:461–469
    [Google Scholar]
  32. Paulij W. P., de Wit P. L. M., Sünnen C. M. G., van Roosmalen M. H., Petersen-van Ettekoven A., Cooreman M. P., Heijtink R. A. 1999; Localization of a unique hepatitis B virus epitope sheds new light on the structure of hepatitis B virus surface antigen. Journal of General Virology 80:2121–2126
    [Google Scholar]
  33. Pedron T., Girard R., Chaby R. 1995; Variation of LPS-binding capacity, epitope expression, and shedding of membrane-bound CD14 during differentiation of human monocytes. Journal of Immunology 155:1460–1471
    [Google Scholar]
  34. 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]
  35. 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]
  36. Ryu C. J., Cho D.-Y., Gripon P., Kim H. S., Guguen-Guillouzo C., Hong H. J. 2000; An 80-kilodalton protein that binds to the pre-S1 domain of hepatitis B virus. Journal of Virology 74:110–116
    [Google Scholar]
  37. Satoh O., Umeda M., Imai H., Tunoo H., Inoue K. 1990; Lipid composition of hepatitis B virus surface antigen particles and the particle-producing hepatoma cell lines. Journal of Lipid Research 31:1293–1300
    [Google Scholar]
  38. Satoh O., Imai H., Yoneyama T., Miyamura T., Utsumi H., Inoue K., Umeda M. 2000; Membrane structure of the hepatitis B virus surface antigen particle. Biochemical Journal 127:543–550
    [Google Scholar]
  39. Schromm A. B., Brandenburg K., Rietschel E. T., Flad H. D., Carroll S. F., Seydel U. 1996; Lipopolysaccharide-binding protein mediates CD14-independent intercalation of lipopolysaccharide into phospholipid membranes. FEBS Letters 309:267–271
    [Google Scholar]
  40. Seeger C., Mason W. S. 2000; Hepatitis B virus biology. Microbiology and Molecular Biology Reviews 64:51–68
    [Google Scholar]
  41. Skelly J., Howard C. R., Zuckerman A. J. 1981; Hepatitis B polypeptide vaccine preparation in micelle form. Nature 290:51–54
    [Google Scholar]
  42. Stefas I., Rucheton M., D’Angeac A. D., Morel-Baccard C., Seigneurin J. M., Zarski J. P., Martin M., Cerutti M., Bossy J. P., Missé D., Graafland H., Veas F. 2001; Hepatitis B virus Dane particles bind to human plasma apolipoprotein H. Hepatology 33:207–217
    [Google Scholar]
  43. Stelter F., Bernheiden M., Menzel R., Jack R. S., Witt S., Fan X., Pfister M., Schutt C. 1997; Mutation of amino acids 39–44 of human CD14 abrogates binding of lipopolysaccharide and Escherichia coli . European Journal of Biochemistry 243:100–109
    [Google Scholar]
  44. Stelter F., Loppnow H., Menzel R., Grunwald U., Bernheiden M., Jack R. S., Ulmer A. J., Schutt C. 1999; Differential impact of substitution of amino acids 9–13 and 91–101 of human CD14 on soluble CD14-dependent activation of cells by lipopolysaccharide. Journal of Immunology 163:6035–6044
    [Google Scholar]
  45. Stirk H. J., Thornton J. M., Howard C. R. 1992; A topological model for hepatitis B surface antigen. Intervirology 33:148–158
    [Google Scholar]
  46. 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]
  47. Van der Meeren P., Van Crieckinge W., Vanderdeelen J., Baert L. 1994; Phospholipid composition of r-DNA hepatitis B surface antigens. International Journal of Pharmaceutics 106:89–92
    [Google Scholar]
  48. Vanlandschoot P., Beirnaert E., Barrere B., Calder L., Millar B., Wharton S., Jou W. M., Fiers W. 1998; An antibody that binds to the membrane-proximal end of influenza virus haemagglutinin (H3 subtype) inhibits the low-pH-induced conformational change and cell–cell fusion but does not neutralize virus. Journal of General Virology 79:1781–1791
    [Google Scholar]
  49. Vanlandschoot P., Van Houtte F., Roobrouck A., Farhoudi A., Leroux-Roels G. 2002; Yeast-derived hepatitis B surface antigen suppresses the activation of monocytes through interaction with a serum protein and a monocyte-specific receptor. Journal of General Virology 83:1281–1289
    [Google Scholar]
  50. Wright S. D., Ramos R. A., Tobias P. S., Ulevitch R. J., Mathison J. C. 1990; CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249:1431–1433
    [Google Scholar]
  51. Wurfel M. M., Wright S. D. 1997; Lipopolysaccharide-binding protein and soluble CD14 transfer lipopolysaccharide to phospholipid bilayers: preferential interaction with particular classes of lipid. Journal of Immunology 158:3925–3934
    [Google Scholar]
  52. Yu B., Hailman E., Wright S. D. 1997; Lipopolysaccharide binding protein and soluble CD14 catalyze exchange of phospholipids. Journal of Clinical Investigation 99:315–324
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-9-2279
Loading
/content/journal/jgv/10.1099/0022-1317-83-9-2279
Loading

Data & Media loading...

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