HBV life cycle: Entry and morphogenesis

Viruses

Volumn 1, Issue 2, 2009, Pages 185-209

  Schädler, Stephanie ^a,b   Hildt, Eberhard ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Entry; Hepatitis B virus; Liver disease; Morphogenesis

Indexed keywords

EID: 84855463651     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v1020185     Document Type: Review

References (157)

1. Locarnini, S. Molecular virology of hepatitis B virus. Semin. Liver Dis. 2004, 24, 3-10.
2. Lupberger, J.; Hildt, E. Hepatitis B virus-induced oncogenesis. World J. Gastroenterol. 2007, 13, 74-81.
3. Cougot, D.; Neuveut, C.; Buendia, M.A. HBV induced carcinogenesis. J. Clin. Virol. 2005, 34, S75-78.
4. Ganem, D.; Schneider, R.J. Hepadnaviridae: the viruses and their replication. In Fields Virology, 4th ed.; Knipe, D.M., Howley, P.M., Eds.; Lippincott Williams: Wilkins, Philadelphia, USA, 2001; Volume 2, pp. 2923-2969.
5. Gerlich, W.H.; Heermann, K.H.; Lu, X. Functions of hepatitis B surface proteins. Arch. Virol. Suppl. 1992, 4, 129-132.
6. Lu, X.; Mehta, A.; Dwek, R.; Butters, T.; Block, T. Evidence that N-linked glycosylation is necessary for hepatitis B virus secretion. Virology 1995, 213, 660-665.
7. Schmitt, S.; Glebe, D.; Tolle, T.K.; Lochnit, G.; Linder, D.; Geyer, R.; Gerlich, W.H. Structure of pre-S2 N-and O-linked glycans in surface proteins from different genotypes of hepatitis B virus. J. Gen. Virol. 2004, 85, 2045-2053.
8. Eble, B.E.; Lingappa, V.R.; Ganem, D. The N-terminal (pre-S2) domain of a hepatitis B virus surface glycoprotein is translocated across membranes by downstream signal sequences. J. Virol. 1990, 64, 1414-1419.
9. Eble, B.E.; MacRae, D.R.; Lingappa, V.R.; Ganem, D. Multiple topogenic sequences determine the transmembrane orientation of the hepatitis B surface antigen. Mol. Cell. Biol. 1987, 7, 3591-3601.
10. Short, J.M.; Chen, S.; Roseman, A.M.; Butler, G.; Crowther, R.A. Structure of Hepatitis B Surface Antigen from Subviral Tubes Determined by Electron Cryomicroscopy. J. Mol. Biol. 2009, in press, May 3. [Epub ahead of print.
11. Bruss, V.; Ganem, D. The role of envelope proteins in hepatitis B virus assembly. Proc. Natl. Acad. Sci. U S A 1991, 88, 1059-1063.
12. Dryden, K.A.; Wieland, S.F.; Whitten-Bauer, C.; Gerin, J.L.; Chisari, F.V.; Yeager, M. Native hepatitis B virions and capsids visualized by electron cryomicroscopy. Mol. Cell 2006, 22, 843-850.
13. Seitz, S.; Urban, S.; Antoni, C.; Bottcher, B. Cryo-electron microscopy of hepatitis B virions reveals variability in envelope capsid interactions. EMBO J. 2007, 26, 4160-4167.
14. Bruss, V.; Lu, X.; Thomssen, R.; Gerlich, W.H. Post-translational alterations in transmembrane topology of the hepatitis B virus large envelope protein. EMBO J. 1994, 13, 2273-2279.
15. Ostapchuk, P.; Hearing, P.; Ganem, D. A dramatic shift in the transmembrane topology of a viral envelope glycoprotein accompanies hepatitis B viral morphogenesis. EMBO J. 1994, 13, 1048-1057.
16. Prange, R.; Streeck, R.E. Novel transmembrane topology of the hepatitis B virus envelope proteins. EMBO J. 1995, 14, 247-256.
17. Hildt, E.; Urban, S.; Hofschneider, P.H. Characterization of essential domains for the functionality of the MHBst transcriptional activator and identification of a minimal MHBst activator. Oncogene 1995, 11, 2055-2066.
18. Bruss, V.; Hagelstein, J.; Gerhardt, E.; Galle, P.R. Myristylation of the large surface protein is required for hepatitis B virus in vitro infectivity. Virology 1996, 218, 396-399.
19. Gripon, P.; Le Seyec, J.; Rumin, S.; Guguen-Guillouzo, C. Myristylation of the hepatitis B virus large surface protein is essential for viral infectivity. Virology 1995, 213, 292-299.
20. Rapoport, T.A.; Matlack, K.E.; Plath, K.; Misselwitz, B.; Staeck, O. Posttranslational protein translocation across the membrane of the endoplasmic reticulum. Biol. Chem. 1999, 380, 1143-1150.
21. Awe, K.; Lambert, C.; Prange, R. Mammalian BiP controls posttranslational ER translocation of the hepatitis B virus large envelope protein. FEBS Lett. 2008, 582, 3179-3184.
22. Lambert, C.; Prange, R. Chaperone action in the posttranslational topological reorientation of the hepatitis B virus large envelope protein: Implications for translocational regulation. Proc. Natl. Acad. Sci. U S A 2003, 100, 5199-5204.
23. Matlack, K.E.; Misselwitz, B.; Plath, K.; Rapoport, T.A. BiP acts as a molecular ratchet during posttranslational transport of prepro-alpha factor across the ER membrane. Cell 1999, 97, 553-564.
24. Bruss, V. A short linear sequence in the pre-S domain of the large hepatitis B virus envelope protein required for virion formation. J. Virol. 1997, 71, 9350-9357.
25. Hildt, E.; Saher, G.; Bruss, V.; Hofschneider, P.H. The hepatitis B virus large surface protein (LHBs) is a transcriptional activator. Virology 1996, 225, 235-239.
26. Hildt, E.; Urban, S.; Eckerskorn, C.; Hofschneider, P.H. Isolation of highly purified, functional carboxy-terminally truncated hepatitis B virus middle surface protein activators from eucaryotic expression systems. Hepatology 1996, 24, 502-507.
27. Hildt, E.; Urban, S.; Lauer, U.; Hofschneider, P.H.; Kekule, A.S. ER-localization and functional expression of the HBV transactivator MHBst. Oncogene 1993, 8, 3359-3367.
28. Hildt, E.; Munz, B.; Saher, G.; Reifenberg, K.; Hofschneider, P.H. The PreS2 activator MHBs(t) of hepatitis B virus activates c-raf-1/Erk2 signaling in transgenic mice. EMBO J. 2002, 21, 525-535.
29. Stockl, L.; Berting, A.; Malkowski, B.; Foerste, R.; Hofschneider, P.H.; Hildt, E. Integrity of c-Raf-1/MEK signal transduction cascade is essential for hepatitis B virus gene expression. Oncogene 2003, 22, 2604-2610.
30. Hafner, A.; Brandenburg, B.; Hildt, E. Reconstitution of gene expression from a regulatoryprotein-deficient hepatitis B virus genome by cell-permeable HBx protein. EMBO Rep. 2003, 4, 767-773.
31. Huovila, A.P.; Eder, A.M.; Fuller, S.D. Hepatitis B surface antigen assembles in a post-ER, pre-Golgi compartment. J. Cell. Biol. 1992, 118, 1305-1320.
32. Gilbert, R.J.; Beales, L.; Blond, D.; Simon, M.N.; Lin, B.Y.; Chisari, F.V.; Stuart, D.I.; Rowlands, D.J. Hepatitis B small surface antigen particles are octahedral. Proc. Natl. Acad. Sci. U S A 2005, 102, 14783-14788.
33. Bruns, M.; Miska, S.; Chassot, S.; Will, H. Enhancement of hepatitis B virus infection by noninfectious subviral particles. J. Virol. 1998, 72, 1462-1468.
34. Patient, R.; Hourioux, C.; Sizaret, P.Y.; Trassard, S.; Sureau, C.; Roingeard, P. Hepatitis B virus subviral envelope particle morphogenesis and intracellular trafficking. J. Virol. 2007, 81, 3842-3851.
35. Chain, B.M.; Myers, R. Variability and conservation in hepatitis B virus core protein. BMC Microbiol. 2005, 5, 33.
36. Gallina, A.; Bonelli, F.; Zentilin, L.; Rindi, G.; Muttini, M.; Milanesi, G. A recombinant hepatitis B core antigen polypeptide with the protamine-like domain deleted self-assembles into capsid particles but fails to bind nucleic acids. J. Virol. 1989, 63, 4645-4652.
37. Zlotnick, A.; Cheng, N.; Stahl, S.J.; Conway, J.F.; Steven, A.C.; Wingfield, P.T. Localization of the C terminus of the assembly domain of hepatitis B virus capsid protein: implications for morphogenesis and organization of encapsidated RNA. Proc. Natl. Acad. Sci. U S A 1997, 94, 9556-9561.
38. Zlotnick, A.; Cheng, N.; Conway, J.F.; Booy, F.P.; Steven, A.C.; Stahl, S.J.; Wingfield, P.T. Dimorphism of hepatitis B virus capsids is strongly influenced by the C-terminus of the capsid protein. Biochemistry 1996, 35, 7412-7421.
39. Nassal, M. The arginine-rich domain of the hepatitis B virus core protein is required for pregenome encapsidation and productive viral positive-strand DNA synthesis but not for virus assembly. J. Virol. 1992, 66, 4107-4116.
40. Nassal, M.; Rieger, A. An intramolecular disulfide bridge between Cys-7 and Cys61 determines the structure of the secretory core gene product (e antigen) of hepatitis B virus. J. Virol. 1993, 67, 4307-4315.
41. Zhou, S.; Standring, D.N. Hepatitis B virus capsid particles are assembled from core-protein dimer precursors. Proc. Natl. Acad. Sci. U S A 1992, 89, 10046-10050.
42. Ceres, P.; Zlotnick, A. Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids. Biochemistry 2002, 41, 11525-11531.
43. Zlotnick, A.; Johnson, J.M.; Wingfield, P.W.; Stahl, S.J.; Endres, D. A theoretical model successfully identifies features of hepatitis B virus capsid assembly. Biochemistry 1999, 38, 14644-14652.
44. Bartenschlager, R.; Schaller, H. Hepadnaviral assembly is initiated by polymerase binding to the encapsidation signal in the viral RNA genome. EMBO J. 1992, 11, 3413-3420.
45. Beck, J.; Nassal, M. Efficient Hsp90-independent in vitro activation by Hsc70 and Hsp40 of duck hepatitis B virus reverse transcriptase, an assumed Hsp90 client protein. J. Biol. Chem. 2003, 278, 36128-36138.
46. Hirsch, R.C.; Lavine, J.E.; Chang, L.J.; Varmus, H.E.; Ganem, D. Polymerase gene products of hepatitis B viruses are required for genomic RNA packaging as wel as for reverse transcription. Nature 1990, 344, 552-555.
47. Junker-Niepmann, M.; Bartenschlager, R.; Schaller, H. A short cis-acting sequence is required for hepatitis B virus pregenome encapsidation and sufficient for packaging of foreign RNA. EMBO J. 1990, 9, 3389-3396.
48. Lott, L.; Beames, B.; Notvall, L.; Lanford, R.E. Interaction between hepatitis B virus core protein and reverse transcriptase. J. Virol. 2000, 74, 11479-11489.
49. Stahl, M.; Retzlaff, M.; Nassal, M.; Beck, J. Chaperone activation of the hepadnaviral reverse transcriptase for template RNA binding is established by the Hsp70 and stimulated by the Hsp90 system. Nucleic Acids Res. 2007, 35, 6124-6136.
50. Kann, M.; Thomssen, R.; Kochel, H.G.; Gerlich, W.H. Characterization of the endogenous protein kinase activity of the hepatitis B virus. Arch. Virol. Suppl. 1993, 8, 53-62.
51. Kang, H.; Yu, J.; Jung, G. Phosphorylation of hepatitis B virus core C-terminally truncated protein (Cp149) by PKC increases capsid assembly and stability. Biochem. J. 2008, 416, 47-54.
52. Crowther, R.A.; Kiselev, N.A.; Bottcher, B.; Berriman, J.A.; Borisova, G.P.; Ose, V.; Pumpens, P. Three-dimensional structure of hepatitis B virus core particles determined by electron cryomicroscopy. Cell 1994, 77, 943-950.
53. Bottcher, B.; Wynne, S.A.; Crowther, R.A. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 1997, 386, 88-91.
54. Conway, J.F.; Cheng, N.; Zlotnick, A.; Wingfield, P.T.; Stahl, S.J.; Steven, A.C. Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy. Nature 1997, 386, 91-94.
55. Wynne, S.A.; Crowther, R.A.; Leslie, A.G. The crystal structure of the human hepatitis B virus capsid. Mol. Cell 1999, 3, 771-780.
56. Bottcher, B.; Vogel, M.; Ploss, M.; Nassal, M. High plasticity of the hepatitis B virus capsid revealed by conformational stress. J. Mol. Biol. 2006, 356, 812-822.
57. Perlman, D.H.; Berg, E.A.; O'Connor P.B.; Costello, C.E.; Hu, J. Reverse transcription-associated dephosphorylation of hepadnavirus nucleocapsids. Proc. Natl. Acad. Sci. U S A 2005, 102, 9020-9025.
58. Roseman, A.M.; Berriman, J.A.; Wynne, S.A.; Butler, P.J.; Crowther, R.A. A structural model for maturation of the hepatitis B virus core. Proc. Natl. Acad. Sci. U S A 2005, 102, 15821-15826.
59. Beterams, G.; Bottcher, B.; Nassal, M. Packaging of up to 240 subunits of a 17 kDa nuclease into the interior of recombinant hepatitis B virus capsids. FEBS Lett. 2000, 481, 169-176.
60. Kratz, P.A.; Bottcher, B.; Nassal, M. Native display of complete foreign protein domains on the surface of hepatitis B virus capsids. Proc. Natl. Acad. Sci. U S A 1999, 96, 1915-1920.
61. Uetrecht, C.; Versluis, C.; Watts, N.R.; Roos, W.H.; Wuite, G.J.; Wingfield, P.T.; Steven, A.C.; Heck, A.J. High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids. Proc. Natl. Acad. Sci. U S A 2008, 105, 9216-9220.
62. Melegari, M.; Wolf, S.K.; Schneider, R.J. Hepatitis B virus DNA replication is coordinated by core protein serine phosphorylation and HBx expression. J. Virol. 2005, 79, 9810-9820.
63. Deres, K.; Schroder, C.H.; Paessens, A.; Goldmann, S.; Hacker, H.J.; Weber, O.; Kramer, T.; Niewohner, U.; Pleiss, U.; Stoltefuss, J.; Graef, E.; Koletzki, D.; Masantschek, R.N.; Reimann, A.; Jaeger, R.; Gross, R.; Beckermann, B.; Schlemmer, K.H.; Haebich, D.; Rubsamen-Waigmann, H. Inhibition of hepatitis B virus replication by drug-induced depletion of nucleocapsids. Science 2003, 299, 893-896.
64. Stray, S.J.; Zlotnick, A. BAY 41-4109 has multiple effects on Hepatitis B virus capsid assembly. J. Mol. Recognit. 2006, 19, 542-548.
65. Bourne, C.; Lee, S.; Venkataiah, B.; Lee, A.; Korba, B.; Finn, M.G.; Zlotnick, A. Small-molecule effectors of hepatitis B virus capsid assembly give insight into virus life cycle. J. Virol. 2008, 82, 10262-10270.
66. Stray, S.J.; Bourne, C.R.; Punna, S.; Lewis, W.G.; Finn, M.G.; Zlotnick, A. A heteroaryldihydropyrimidine activates and can misdirect hepatitis B virus capsid assembly. Proc. Natl. Acad. Sci. U S A 2005, 102, 8138-8143.
67. Marsh, M.; Helenius, A. Virus entry: open sesame. Cell 2006, 124, 729-740.
68. Gripon, P.; Diot, C.; Theze, N.; Fourel, I.; Loreal, O.; Brechot, C.; Guguen-Guillouzo, C. Hepatitis B virus infection of adult human hepatocytes cultured in the presence of dimethyl sulfoxide. J. Virol. 1988, 62, 4136-4143.
69. Rijntjes, P.J.; Moshage, H.J.; Yap, S.H. In vitro infection of primary cultures of cryopreserved adult human hepatocytes with hepatitis B virus. Virus Res. 1988, 10, 95-109.
70. Galle, P.R.; Hagelstein, J.; Kommerell, B.; Volkmann, M.; Schranz, P.; Zentgraf, H. In vitro experimental infection of primary human hepatocytes with hepatitis B virus. Gastroenterology 1994, 106, 664-673.
71. Gripon, P.; Diot, C.; Guguen-Guillouzo, C. Reproducible high level infection of cultured adult human hepatocytes by hepatitis B virus: effect of polyethylene glycol on adsorption and penetration. Virology 1993, 192, 534-540.
72. Walter, E.; Keist, R.; Niederost, B.; Pult, I.; Blum, H.E. Hepatitis B virus infection of tupaia hepatocytes in vitro and in vivo. Hepatology 1996, 24, 1-5.
73. Kock, J.; Nassal, M.; MacNelly, S.; Baumert, T.F.; Blum, H.E.; von Weizsacker, F. Efficient infection of primary tupaia hepatocytes with purified human and woolly monkey hepatitis B virus. J. Virol. 2001, 75, 5084-5089.
74. von Weizsacker, F.; Kock, J.; MacNelly, S.; Ren, S.; Blum, H.E.; Nassal, M. The tupaia model for the study of hepatitis B virus: direct infection and HBV genome transduction of primary tupaia hepatocytes. Methods Mol. Med. 2004, 96, 153-161.
75. Neurath, A.R.; Kent, S.B.; Strick, N.; Parker, K. Identification and chemical synthesis of a host cell receptor binding site on hepatitis B virus. Cell 1986, 46, 429-436.
76. Paran, N.; Geiger, B.; Shaul, Y. HBV infection of cell culture: evidence for multivalent and cooperative attachment. EMBO J. 2001, 20, 4443-4453.
77. Treichel, U.; Meyer zum Buschenfelde, K.H.; Dienes, H.P.; Gerken, G. Receptor-mediated entry of hepatitis B virus particles into liver cells. Arch. Virol. 1997, 142, 493-498.
78. Treichel, U.; Schreiter, T.; Meyer zum Buschenfelde, K.H.; Stockert, R.J. High-yield purification and characterization of human asialoglycoprotein receptor. Protein Expr. Purif. 1995, 6, 251-255.
79. Bchini, R.; Capel, F.; Dauguet, C.; Dubanchet, S.; Petit, M.A. In vitro infection of human hepatoma (HepG2) cells with hepatitis B virus. J. Virol. 1990, 64, 3025-3032.
80. Gripon, P.; Rumin, S.; Urban, S.; Le Seyec, J.; Glaise, D.; Cannie, I.; Guyomard, C.; Lucas, J.; Trepo, C.; Guguen-Guillouzo, C. Infection of a human hepatoma cell line by hepatitis B virus. Proc. Natl. Acad. Sci. U S A 2002, 99, 15655-15660.
81. Nassal, M. Hepatitis B viruses: reverse transcription a different way. Virus Res. 2008, 134, 235-249.
82. Singh, M.; Dicaire, A.; Wakil, A.E.; Luscombe, C.; Sacks, S.L. Quantitation of hepatitis B virus (HBV) covalently closed circular DNA (cccDNA) in the liver of HBV-infected patients by LightCycler real-time PCR. J. Virol. Methods 2004, 118, 159-167.
83. Lucifora, J.; Durantel, D.; Belloni, L.; Barraud, L.; Villet, S.; Vincent, I.E.; Margeridon-Thermet, S.; Hantz, O.; Kay, A.; Levrero, M.; Zoulim, F. Initiation of hepatitis B virus genome replication and production of infectious virus following delivery in HepG2 cells by novel recombinant baculovirus vector. J. Gen. Virol. 2008, 89, 1819-1828.
84. Lupberger, J.; Mund, A.; Kock, J.; Hildt, E. Cultivation of HepG2.2.15 on Cytodex-3: higher yield of hepatitis B virus and less subviral particles compared to conventional culture methods. J. Hepatol. 2006, 45, 547-552.
85. Offensperger, W.B.; Offensperger, S.; Walter, E.; Blum, H.E.; Gerok, W. Sulfated polyanions do not inhibit duck hepatitis B virus infection. Antimicrob. Agents Chemother. 1991, 35, 2431-2433.
86. Leistner, C.M.; Gruen-Bernhard, S.; Glebe, D. Role of glycosaminoglycans for binding and infection of hepatitis B virus. Cell Microbiol. 2008, 10, 122-133.
87. Schulze, A.; Gripon, P.; Urban, S. Hepatitis B virus infection initiates with a large surface proteindependent binding to heparan sulfate proteoglycans. Hepatology 2007, 46, 1759-1768.
88. Glebe, D.; Urban, S. Viral and cellular determinants involved in hepadnaviral entry. World J. Gastroenterol. 2007, 13, 22-38.
89. Le Seyec, J.; Chouteau, P.; Cannie, I.; Guguen-Guillouzo, C.; Gripon, P. Role of the pre-S2 domain of the large envelope protein in hepatitis B virus assembly and infectivity. J. Virol. 1998, 72, 5573-5578.
90. De Falco, S.; Ruvo, M.; Verdoliva, A.; Scarallo, A.; Raimondo, D.; Raucci, A.; Fassina, G. Nterminal myristylation of HBV preS1 domain enhances receptor recognition. J. Pept. Res. 2001, 57, 390-400.
91. Engelke, M.; Mills, K.; Seitz, S.; Simon, P.; Gripon, P.; Schnolzer, M.; Urban, S. Characterization of a hepatitis B and hepatitis delta virus receptor binding site. Hepatology 2006, 43, 750-760.
92. Glebe, D.; Urban, S.; Knoop, E.V.; Cag, N.; Krass, P.; Grun, S.; Bulavaite, A.; Sasnauskas, K.; Gerlich, W.H. Mapping of the hepatitis B virus attachment site by use of infection-inhibiting preS1 lipopeptides and tupaia hepatocytes. Gastroenterology 2005, 129, 234-245.
93. Gripon, P.; Cannie, I.; Urban, S. Efficient inhibition of hepatitis B virus infection by acylated peptides derived from the large viral surface protein. J. Virol. 2005, 79, 1613-1622.
94. Urban, S.; Gripon, P. Inhibition of duck hepatitis B virus infection by a myristoylated pre-S peptide of the large viral surface protein. J. Virol. 2002, 76, 1986-1990.
95. Petersen, J.; Dandri, M.; Mier, W.; Lutgehetmann, M.; Volz, T.; von Weizsacker, F.; Haberkorn, U.; Fischer, L.; Pollok, J.M.; Erbes, B.; Seitz, S.; Urban, S. Prevention of hepatitis B virus infection in vivo by entry inhibitors derived from the large envelope protein. Nat. Biotechnol. 2008, 26, 335-341.
96. Glebe, D.; Aliakbari, M.; Krass, P.; Knoop, E.V.; Valerius, K.P.; Gerlich, W.H. Pre-s1 antigendependent infection of Tupaia hepatocyte cultures with human hepatitis B virus. J. Virol. 2003, 77, 9511-9521.
97. Offensperger, W.B.; Offensperger, S.; Walter, E.; Blum, H.E.; Gerok, W. Inhibition of duck hepatitis B virus infection by lysosomotropic agents. Virology 1991, 183, 415-418.
98. Offensperger, W.B.; Offensperger, S.; Walter, E.; Blum, H.E.; Gerok, W. Suramin prevents duck hepatitis B virus infection in vivo. Antimicrob. Agents Chemother. 1993, 37, 1539-1542.
99. Stoeckl, L.; Funk, A.; Kopitzki, A.; Brandenburg, B.; Oess, S.; Will, H.; Sirma, H.; Hildt, E. Identification of a structural motif crucial for infectivity of hepatitis B viruses. Proc. Natl. Acad. Sci. U S A 2006, 103, 6730-6734.
100. Chojnacki, J.; Anderson, D.A.; Grgacic, E.V. A hydrophobic domain in the large envelope protein is essential for fusion of duck hepatitis B virus at the late endosome. J. Virol. 2005, 79, 14945-14955.
101. Berting, A.; Fischer, C.; Schaefer, S.; Garten, W.; Klenk, H.D.; Gerlich, W.H. Hemifusion activity of a chimeric influenza virus hemagglutinin with a putative fusion peptide from hepatitis B virus. Virus Res. 2000, 68, 35-49.
102. Epand, R.M. Fusion peptides and the mechanism of viral fusion. Biochim. Biophys. Acta 2003, 1614, 116-121.
103. Nunez, E.; Yelamos, B.; Delgado, C.; Gomez-Gutierrez, J.; Peterson, D.L.; Gavilanes, F. Interaction of preS domains of hepatitis B virus with phospholipid vesicles. Biochim. Biophys. Acta 2009, 1788, 417-424.
104. Rodriguez-Crespo, I.; Nunez, E.; Yelamos, B.; Gomez-Gutierrez, J.; Albar, J.P.; Peterson, D.L.; Gavilanes, F. Fusogenic activity of hepadnavirus peptides corresponding to sequences downstream of the putative cleavage site. Virology 1999, 261, 133-142.
105. Grgacic, E.V.; Schaller, H. A metastable form of the large envelope protein of duck hepatitis B virus: low-pH release results in a transition to a hydrophobic, potentially fusogenic conformation. J. Virol. 2000, 74, 5116-5122.
106. Oess, S.; Hildt, E. Novel cell permeable motif derived from the PreS2-domain of hepatitis-B virus surface antigens. Gene Ther. 2000, 7, 750-758.
107. Bleifuss, E.; Kammertoens, T.; Hutloff, A.; Quarcoo, D.; Dorner, M.; Straub, P.; Uckert, W.; Hildt, E. The translocation motif of hepatitis B virus improves protein vaccination. Cell Mol. Life Sci. 2006, 63, 627-635.
108. Brandenburg, B.; Stockl, L.; Gutzeit, C.; Roos, M.; Lupberger, J.; Schwartlander, R.; Gelderblom, H.; Sauer, I.M.; Hofschneider, P.H.; Hildt, E. A novel system for efficient gene transfer into primary human hepatocytes via cell-permeable hepatitis B virus-like particle. Hepatology 2005, 42, 1300-1309.
109. Saher, G.; Hildt, E. Activation of c-Raf-1 kinase signal transduction pathway in alpha(7) integrindeficient mice. J. Biol. Chem. 1999, 274, 27651-27657.
110. Blanchet, M.; Sureau, C. Infectivity determinants of the hepatitis B virus pre-S domain are confined to the N-terminal 75 amino acid residues. J. Virol. 2007, 81, 5841-5849.
111. Gudima, S.; Meier, A.; Dunbrack, R.; Taylor, J.; Bruss, V. Two potentially important elements of the hepatitis B virus large envelope protein are dispensable for the infectivity of hepatitis delta virus. J. Virol. 2007, 81, 4343-4347.
112. Lepere, C.; Regeard, M.; Le Seyec, J.; Gripon, P. The translocation motif of hepatitis B virus envelope proteins is dispensable for infectivity. J. Virol. 2007, 81, 7816-7818.
113. Gudima, S.; He, Y.; Chai, N.; Bruss, V.; Urban, S.; Mason, W.; Taylor, J. Primary human hepatocytes are susceptible to infection by hepatitis delta virus assembled with envelope proteins of woodchuck hepatitis virus. J. Virol. 2008, 82, 7276-83.
114. Rabe, B.; Glebe, D.; Kann, M. Lipid-mediated introduction of hepatitis B virus capsids into nonsusceptible cells allows highly efficient replication and facilitates the study of early infection events. J. Virol. 2006, 80, 5465-5473.
115. Dohner, K.; Sodeik, B. The role of the cytoskeleton during viral infection. Curr. Top Microbiol. Immunol. 2005, 285, 67-108.
116. Sodeik, B. Mechanisms of viral transport in the cytoplasm. Trends Microbiol. 2000, 8, 465-72.
117. Huang, C.J.; Chen, Y.H.; Ting, L.P. Hepatitis B virus core protein interacts with the C-terminal region of actin-binding protein. J. Biomed. Sci. 2000, 7, 160-168.
118. Kann, M.; Bischof, A.; Gerlich, W.H. In vitro model for the nuclear transport of the hepadnavirus genome. J. Virol. 1997, 71, 1310-1316.
119. Kann, M.; Sodeik, B.; Vlachou, A.; Gerlich, W.H.; Helenius, A. Phosphorylation-dependent binding of hepatitis B virus core particles to the nuclear pore complex. J. Cell Biol. 1999, 145, 45-55.
120. Rabe, B.; Vlachou, A.; Pante, N.; Helenius, A.; Kann, M. Nuclear import of hepatitis B virus capsids and release of the viral genome. Proc. Natl. Acad. Sci. U S A 2003, 100, 9849-9854.
121. Pante, N.; Kann, M. Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol. Biol. Cell 2002, 13, 425-434.
122. Hillemann, A.; Brandenburg, B.; Schmidt, U.; Roos, M.; Smirnow, I.; Lemken, M.L.; Lauer, U.M.; Hildt, E. Protein transduction with bacterial cytosine deaminase fused to the TLM intercellular transport motif induces profound chemosensitivity to 5-fluorocytosine in human hepatoma cells. J. Hepatol. 2005, 43, 442-450.
123. Conway, J.F.; Watts, N.R.; Belnap, D.M.; Cheng, N.; Stahl, S.J.; Wingfield, P.T.; Steven, A.C. Characterization of a conformational epitope on hepatitis B virus core antigen and quasiequivalent variations in antibody binding. J. Virol. 2003, 77, 6466-6473.
124. Lupberger, J.; Luckow, A.; Pairan, A.; Schmidt, M.; Schaedler, S.; Hildt, E. Nuclear import of Hepatitis B virus polymerase is mediated by a novel bipartite NLS and depends on CKII phosphorylation, submitted for publication, 2009.
125. Jun-Bin, S.; Zhi, C.; Wei-Qin, N.; Jun, F. A quantitative method to detect HBV cccDNA by chimeric primer and real-time polymerase chain reaction. J. Virol. Methods 2003, 112, 45-52.
126. Sun, D.; Nassal, M. Stable HepG2-and Huh7-based human hepatoma cell lines for efficient regulated expression of infectious hepatitis B virus. J. Hepatol. 2006, 45, 636-645.
127. Gao, W.; Hu, J. Formation of hepatitis B virus covalently closed circular DNA: removal of genome-linked protein. J. Virol. 2007, 81, 6164-6174.
128. Guo, H.; Jiang, D.; Zhou, T.; Cuconati, A.; Block, T.M.; Guo, J.T. Characterization of the intracellular deproteinized relaxed circular DNA of hepatitis B virus: an intermediate of covalently closed circular DNA formation. J. Virol. 2007, 81, 12472-12484.
129. Wang, H.; Kim, S.; Ryu, W.S. DDX3 DEAD-Box RNA helicase inhibits hepatitis B virus reverse transcription by incorporation into nucleocapsids. J. Virol. 2009, 83, 5815-5824.
130. Seeger, C.; Mason, W.S. Hepatitis B virus biology. Microbiol. Mol. Biol. Rev. 2000, 64, 51-68.
131. Lee, G.H.; Wasser, S.; Lim, S.G. Hepatitis B pregenomic RNA splicing--the products, the regulatory mechanisms and its biological significance. Virus Res. 2008, 136, 1-7.
132. Kock, J.; Nassal, M.; Deres, K.; Blum, H.E.; von Weizsacker, F. Hepatitis B virus nucleocapsids formed by carboxy-terminally mutated core proteins contain spliced viral genomes but lack fullsize DNA. J. Virol. 2004, 78, 13812-13818.
133. Le Pogam, S.; Chua, P.K.; Newman, M.; Shih, C. Exposure of RNA templates and encapsidation of spliced viral RNA are influenced by the arginine-rich domain of human hepatitis B virus core antigen (HBcAg 165-173). J. Virol. 2005, 79, 1871-1887.
134. Newman, M.; Suk, F.M.; Cajimat, M.; Chua, P.K.; Shih, C. Stability and morphology comparisons of self-assembled virus-like particles from wild-type and mutant human hepatitis B virus capsid proteins. J. Virol. 2003, 77, 12950-12960.
135. Lambert, C.; Doring, T.; Prange, R. Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and gamma 2-adaptin. J. Virol. 2007, 81, 9050-9060.
136. Watanabe, T.; Sorensen, E.M.; Naito, A.; Schott, M.; Kim, S.; Ahlquist, P. Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Proc. Natl. Acad. Sci. U S A 2007, 104, 10205-10210.
137. Bruss, V. Hepatitis B virus morphogenesis. World J. Gastroenterol. 2007, 13, 65-73.
138. Zhang, Y.Y.; Zhang, B.H.; Theele, D.; Litwin, S.; Toll, E.; Summers, J. Single-cell analysis of covalently closed circular DNA copy numbers in a hepadnavirus-infected liver. Proc. Natl. Acad. Sci. U S A 2003, 100, 12372-12377.
139. Gerelsaikhan, T.; Tavis, J.E.; Bruss, V. Hepatitis B virus nucleocapsid envelopment does not occur without genomic DNA synthesis. J. Virol. 1996, 70, 4269-4274.
140. Perlman, D.; Hu, J. Duck hepatitis B virus virion secretion requires a double-stranded DNA genome. J. Virol. 2003, 77, 2287-2294.
141. Wei, Y.; Tavis, J.E.; Ganem, D. Relationship between viral DNA synthesis and virion envelopment in hepatitis B viruses. J. Virol. 1996, 70, 6455-6458.
142. Liao, W.; Ou, J.H. Phosphorylation and nuclear localization of the hepatitis B virus core protein: significance of serine in the three repeated SPRRR motifs. J. Virol. 1995, 69, 1025-1029.
143. Daub, H.; Blencke, S.; Habenberger, P.; Kurtenbach, A.; Dennenmoser, J.; Wissing, J.; Ullrich, A.; Cotten, M. Identification of SRPK1 and SRPK2 as the major cellular protein kinases phosphorylating hepatitis B virus core protein. J. Virol. 2002, 76, 8124-8137.
144. Basagoudanavar, S.H.; Perlman, D.H.; Hu, J. Regulation of hepadnavirus reverse transcription by dynamic nucleocapsid phosphorylation. J. Virol. 2007, 81, 1641-1649.
145. Bruss, V. Envelopment of the hepatitis B virus nucleocapsid. Virus Res. 2004, 106, 199-209.
146. Ponsel, D.; Bruss, V. Mapping of amino acid side chains on the surface of hepatitis B virus capsids required for envelopment and virion formation. J. Virol. 2003, 77, 416-422.
147. Fernholz, D.; Stemler, M.; Brunetto, M.; Bonino, F.; Will, H. Replicating and virion secreting hepatitis B mutant virus unable to produce preS2 protein. J. Hepatol. 1991, 13, S102-104.
148. Ueda, K.; Tsurimoto, T.; Matsubara, K. Three envelope proteins of hepatitis B virus: large S, middle S, and major S proteins needed for the formation of Dane particles. J. Virol. 1991, 65, 3521-3529.
149. Bruss, V.; Vieluf, K. Functions of the internal pre-S domain of the large surface protein in hepatitis B virus particle morphogenesis. J. Virol. 1995, 69, 6652-6657.
150. Summers, J.; Smith, P.M.; Horwich, A.L. Hepadnavirus envelope proteins regulate covalently closed circular DNA amplification. J. Virol. 1990, 64, 2819-2824.
151. Summers, J.; Smith, P.M.; Huang, M.J.; Yu, M.S. Morphogenetic and regulatory effects of mutations in the envelope proteins of an avian hepadnavirus. J. Virol. 1991, 65, 1310-1317.
152. Lenhoff, R.J.; Summers, J. Coordinate regulation of replication and virus assembly by the large envelope protein of an avian hepadnavirus. J. Virol. 1994, 68, 4565-4571.
153. Poisson, F.; Severac, A.; Hourioux, C.; Goudeau, A.; Roingeard, P. Both pre-S1 and S domains of hepatitis B virus envelope proteins interact with the core particle. Virology 1997, 228, 115-120.
154. Loffler-Mary, H.; Dumortier, J.; Klentsch-Zimmer, C.; Prange, R. Hepatitis B virus assembly is sensitive to changes in the cytosolic S loop of the envelope proteins. Virology 2000, 270, 358-367.
155. Bottcher, B.; Tsuji, N.; Takahashi, H.; Dyson, M.R.; Zhao, S.; Crowther, R.A.; Murray, K. Peptides that block hepatitis B virus assembly: analysis by cryomicroscopy, mutagenesis and transfection. EMBO J. 1998, 17, 6839-6845.
156. Mabit, H.; Schaller, H. Intracellular hepadnavirus nucleocapsids are selected for secretion by envelope protein-independent membrane binding. J. Virol. 2000, 74, 11472-11478.
157. Babst, M. A protein's final ESCRT. Traffic 2005, 6, 2-9.