Duck hepatitis B virus requires cholesterol for endosomal escape during virus entry

Journal of Virology

Volumn 82, Issue 21, 2008, Pages 10532-10542

  Funk, Anneke ^a,d   Mhamdi, Mouna ^a   Hohenberg, Heinz ^a   Heeren, Jörg ^b   Reimer, Rudolph ^a   Lambert, Carsten ^c   Prange, Reinhild ^c   Sirma, Hüseyin ^a  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOSOME; HEPATITIS B VIRUS; LIPID RAFT; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS INFECTIVITY; CHEMISTRY; HUMAN; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY;

DUCK HEPATITIS B VIRUS; HEPATITIS B VIRUS;

CELL LINE, TUMOR; CHOLESTEROL; ENDOSOMES; HEPATITIS B VIRUS, DUCK; HEPATOCYTES; HUMANS; VIRUS INTERNALIZATION;

EID: 55249088566     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00422-08     Document Type: Article

References (40)

1. Alberts, A. W., J. Chen, G. Kuron, V. Hunt, J. Huff, C. Hoffman, J. Rothrock, M. Lopez, H. Joshua, E. Harris, A. Patchett, R. Monaghan, S. Currie, E. Stapley, G. Albers-Schonberg, O. Hensens, J. Hirshfield, K. Hoogsteen, J. Liesch, and J. Springer. 1980. Mevinolin: a highly potent competitive inhibitor of hydroxymethylglutaryl-coenzyme A reductase and a cholesterol-lowering agent. Proc. Natl. Acad. Sci. USA 77:3957-3961.
2. Anderson, H. A., Y. Chen, and L. C. Norkin. 1996. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol. Biol. Cell 7:1825-1834.
3. Bender, F. C., J. C. Whitbeck, M. Ponce de Leon, H. Lou, R. J. Eisenberg, and G. H. Cohen. 2003. Specific association of glycoprotein B with lipid rafts during herpes simplex virus entry. J. Virol. 77:9542-9552.
4. Campbell, S. M., S. M. Crowe, and J. Mak. 2002. Virion-associated cholesterol is critical for the maintenance of HIV-1 structure and infectivity. AIDS 16:2253-2261.
5. Chojnacki, J., D. A. Anderson, and E. V. L. Grgacic. 2005. A hydrophobic domain in the large envelope protein is essential for fusion of duck hepatitis B virus at the late endosome. J. Virol. 79:14945-14955.
6. Danthi, P., and M. Chow. 2004. Cholesterol removal by methyl-β-cyclodextrin inhibits poliovirus entry. J. Virol. 78:33-41.
7. Diminsky, D., R. Schirmbeck, J. Reimann, and Y. Barenholz. 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.
8. Funk, A., H. Hohenberg, M. Mhamdi, H. Will, and H. Sirma. 2004. Spread of hepatitis B viruses in vitro requires extracellular progeny and may be codetermined by polarized egress. J. Virol. 78:3977-3983.
9. Funk, A., M. Mhamdi, H. Hohenberg, H. Will, and H. Sirma. 2006. pH-independent entry and sequential endosomal sorting are major determinants of hepadnaviral infection in primary hepatocytes. Hepatology 44:685-693.
10. Funk, A., M. Mhamdi, L. Lin, H. Will, and H. Sirma. 2004. Itinerary of hepatitis B viruses: delineation of restriction points critical for infectious entry. J. Virol. 78:8289-8300.
11. Funk, A., M. Mhamdi, H. Will, and H. Sirma. 2007. Avian hepatitis B viruses: molecular and cellular biology, phylogenesis, and host tropism. World J. Gastroenterol. 13:91-103.
12. Ganem, D., and R. J. Schneider. 2001. Hepadnaviridae: the viruses and their replication, p. 2923-2969. In D. M. Knipe and P. M. Howley (ed.), Fields virology, vol. 2. Lippincott, Williams & Wilkins, Philadelphia, PA.
13. Gavilanes, F., J. M. Gonzalez-Ros, and D. L. Peterson. 1982. Structure of hepatitis B surface antigen. Characterization of the lipid components and their association with the viral proteins. J. Biol. Chem. 257:7770-7777.
14. Glebe, D., and S. Urban. 2007. Viral and cellular determinants involved in hepadnaviral entry. World J. Gastroenterol. 13:22-38.
15. Gripon, P., S. Rumin, S. Urban, J. Le Seyec, D. Glaise, I. Cannie, C. Guyomard, J. Lucas, C. Trepo, and C. Guguen-Guillouzo. 2002. Infection of a human hepatoma cell line by hepatitis B virus. Proc. Natl. Acad. Sci. USA 99:15655-15660.
16. Haque, M. E., and B. R. Lentz. 2002. Influence of gp41 fusion peptide on the kinetics of poly(ethylene glycol)-mediated model membrane fusion. Biochemistry 41:10866-10876.
17. Hernandez, L. D., L. R. Hoffman, T. G. Wolfsberg, and J. M. White. 1996. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12:627-661.
18. Imelli, N., O. Meier, K. Boucke, S. Hemmi, and U. F. Greber. 2004. Cholesterol is required for endocytosis and endosomal escape of adenovirus type 2. J. Virol. 78:3089-3098.
19. Kilsdonk, E. P., P. G. Yancey, G. W. Stoudt, F. W. Bangerter, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1995. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 270:17250-17256.
20. Klenk, H. D., and P. W. Choppin. 1970. Glycosphingolipids of plasma membranes of cultured cells and an enveloped virus (SV5) grown in these cells. Proc. Natl. Acad. Sci. USA 66:57-64.
21. Laine, R., M. L. Kettunen, C. G. Gahmberg, L. Kääriä inen, and O. Renkonen. 1972. Fatty chains of different lipid classes of Semliki Forest virus and host cell membranes. J. Virol. 10:433-438.
22. Lambert, C., S. Mann, and R. Prange. 2004. Assessment of determinants affecting the dual topology of hepadnaviral large envelope proteins. J. Gen. Virol. 85:1221-1225.
23. Lambert, C., and R. Prange. 2001. Dual topology of the hepatitis B virus large envelope protein: determinants influencing post-translational pre-S translocation. J. Biol. Chem. 276:22265-22272.
24. Lange, Y., and T. L. Steck. 1985. Cholesterol-rich intracellular membranes: a precursor to the plasma membrane. J. Biol. Chem. 260:15592-15597.
25. Leistner, C. M., S. Gruen-Bernhard, and D. Glebe. 2008. Role of glycosaminoglycans for binding and infection of hepatitis B virus. Cell. Microbiol. 10:122-133.
26. Lenard, J., and R. W. Compans. 1974. The membrane structure of lipid-containing viruses. Biochim. Biophys. Acta 344:51-94.
27. Manes, S., G. del Real, R. A. Lacalle, P. Lucas, C. Gomez-Mouton, S. Sanchez-Palomino, R. Delgado, J. Alcami, E. Mira, and A. C. Martinez. 2000. Membrane raft microdomains mediate lateral assemblies required for HIV-1 infection. EMBO Rep. 1:190-196.
28. Moffett, S., D. A. Brown, and M. E. Linder. 2000. Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 275:2191-2198.
29. Nichols, B. J., A. K. Kenworthy, R. S. Polishchuk, R. Lodge, T. H. Roberts, K. Hirschberg, R. D. Phair, and J. Lippincott-Schwartz. 2001. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153:529-541.
30. Pelkmans, L. 2005. Viruses as probes for systems analysis of cellular signalling, cytoskeleton reorganization and endocytosis. Curr. Opin. Microbiol. 8:331-337.
31. Pralle, A., P. Keller, E. L. Florin, K. Simons, and J. K. Horber. 2000. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148:997-1008.
32. Prassolov, A., H. Hohenberg, T. Kalinina, C. Schneider, L. Cova, O. Krone, K. Frolich, H. Will, and H. Sirma. 2003. New hepatitis B virus of cranes that has an unexpected broad host range. J. Virol. 77:1964-1976.
33. Renkonen, O., L. Kaarainen, K. Simons, and C. G. Gahmberg. 1971. The lipid class composition of Semliki Forest virus and plasma membranes of the host cells. Virology 46:318-326.
34. Saez-Cirion, A., S. Nir, M. Lorizate, A. Agirre, A. Cruz, J. Perez-Gil, and J. L. Nieva. 2002. Sphingomyelin and cholesterol promote HIV-1 gp41 pretransmembrane sequence surface aggregation and membrane restructuring. J. Biol. Chem. 277:21776-21785.
35. Satoh, O., H. Imai, T. Yoneyama, T. Miyamura, H. Utsumi, K. Inoue, and M. Umeda. 2000. Membrane structure of the hepatitis B virus surface antigen particle. J. Biochem. 127:543-550.
36. Schultz, U., E. Grgacic, and M. Nassal. 2004. Duck hepatitis B virus: an invaluable model system for HBV infection. Adv. Virus Res. 63:1-70.
37. Schulze, A., P. Gripon, and S. Urban. 2007. Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans. Hepatology 46:1759-1768.
38. Stoeckl, L., A. Funk, A. Kopitzki, B. Brandenburg, S. Oess, H. Will, H. Sirma, and E. Hildt. 2006. Identification of a structural motif crucial for infectivity of hepatitis B viruses. Proc. Natl. Acad. Sci. USA 103:6730-6734.
39. Teissier, E., and E. I. Pecheur. 2007. Lipids as modulators of membrane fusion mediated by viral fusion proteins. Eur. Biophys. J. 36:887-899.
40. Uekama, K., K. Arimori, A. Sakai, K. Masaki, T. Irie, and M. Otagiri. 1987. Improvement in percutaneous absorption of prednisolone by beta- and gamma-cyclodextrin complexations. Chem. Pharm. Bull. 35:2910-2913.