Hepatitis B virus morphogenesis

World Journal of Gastroenterology

Volumn 13, Issue 1, 2007, Pages 65-73

  Bruss, Volker ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

HBsAG; Hepatitis B virus capsid; Hepatitis B virus morphogenesis; Virus envelopment

Indexed keywords

DNA POLYMERASE; HETERODIMER; HOMODIMER; LIPID; LIPOPROTEIN; MEMBRANE PROTEIN; PROTEIN C; PROTEIN S; VIRUS DNA; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

AMINO TERMINAL SEQUENCE; BINDING SITE; CYTOSOL; DISULFIDE BOND; DNA SYNTHESIS; ENDOPLASMIC RETICULUM; HEPATITIS B VIRUS; MEMBRANE STRUCTURE; MORPHOGENESIS; NONHUMAN; PARTICLE SIZE; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION; REVIEW; VIRION; VIROGENESIS; VIRUS CAPSID; VIRUS ENVELOPE; VIRUS GENOME; VIRUS NUCLEOCAPSID; VIRUS PARTICLE; VIRUS REPLICATION;

EID: 33846502163     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v13.i1.65     Document Type: Review

References (139)

1. Acs G, Sells MA, Purcell RH, Price P, Engle R, Shapiro M, Popper H. Hepatitis B virus produced by transfected Hep G2 cells causes hepatitis in chimpanzees. Proc Natl Acad Sci USA 1987; 84: 4641-4644
2. Yaginuma K, Shirakata Y, Kobayashi M, Koike K. Hepatitis B virus (HBV) particles are produced in a cell culture system by transient expression of transfected HBV DNA. Proc Natl Acad Sci USA 1987; 84: 2678-2682
3. 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 USA 2002; 99: 15655-15660
4. Nowak MA, Bonhoeffer S, Hill AM, Boehme R, Thomas HC, McDade H. Viral dynamics in hepatitis B virus infection. Proc Natl Acad Sci USA 1996; 93: 4398-4402
5. Roingeard P, Sureau C. Ultrastructural analysis of hepatitis B virus in HepG2-transfected cells with special emphasis on subviral filament morphogenesis. Hepatology 1998; 28: 1128-1133
6. Funk A, Hohenberg H, Mhamdi M, Will H, Sirma H. Spread of hepatitis B viruses in vitro requires extracellular progeny and may be codetermined by polarized egress. J Virol 2004; 78: 3977-3983
7. Chain BM, Myers R. Variability and conservation in hepatitis B virus core protein. BMC Microbiol 2005; 5: 33
8. Zhou S, Standring DN. Hepatitis B virus capsid particles are assembled from core-protein dimer precursors. Proc Natl Acad Sci USA 1992; 89: 10046-10050
9. Nassal M, Rieger A, Steinau O. Topological analysis of the hepatitis B virus core particle by cysteine-cysteine cross-linking. J Mol Biol 1992; 225: 1013-1025
10. Zheng J, Schodel F, Peterson DL. The structure of hepadnaviral core antigens. Identification of free thiols and determination of the disulfide bonding pattern. J Biol Chem 1992; 267: 9422-9429
11. Lingappa JR, Martin RL, Wong ML, Ganem D, Welch WJ, Lingappa VR. A eukaryotic cytosolic chaperonin is associated with a high molecular weight intermediate in the assembly of hepatitis B virus capsid, a multimeric particle. J Cell Biol 1994; 125: 99-111
12. Ceres P, Zlotnick A. Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids. Biochemistry 2002; 41: 11525-11531
13. Crowther RA, Kiselev NA, Bottcher B, Berriman JA, Borisova GP, Ose V, Pumpens P. Three-dimensional structure of hepatitis B virus core particles detern-dned by electron cryomicroscopy. Cell 1994; 77: 943-950
14. Kenney JM, von Bonsdorff CH, Nassal M, Fuller SD. Evolutionary conservation in the hepatitis B virus core structure: comparison of human and duck cores. Structure 1995; 3: 1009-1019
15. Roseman AM, Berriman JA, Wynne SA, Butler PJ, Crowther RA. A structural model for maturation of the hepatitis B virus core. Proc Natl Acad Sci USA 2005; 102: 15821-15826
16. 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
17. Zlotnick A, Cheng N, Conway JF, Booy FP, Steven AC, Stahl SJ, Wingfield PT. Dimorphism of hepatitis B virus capsids is strongly influenced by the C-terminus of the capsid protein. Biochemistry 1996; 35: 7412-7421
18. Conway JF, Cheng N, Zlotnick A, Wingfield PT, Stahl SJ, Steven AC. Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy. Nature 1997; 386: 91-94
19. Bottcher B, Wynne SA, Crowther RA. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 1997; 386: 88-91
20. Zlotnick A, Palmer I, Kaufman JD, Stahl SJ, Steven AC, Wingfield PT. Separation and crystallization of T = 3 and T = 4 icosahedral complexes of the hepatitis B virus core protein. Acta Crystallogr D Biol Crystallogr 1999; 55: 717-720
21. Wynne SA, Crowther RA, Leslie AG. The crystal structure of the human hepatitis B virus capsid. Mol Cell 1999; 3: 771-780
22. 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
23. Zlotnick A, Cheng N, Stahl SJ, Conway JF, Steven AC, Wingfield PT. 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 USA 1997; 94: 9556-9561
24. Machida A, Ohnuma H, Tsuda F, Yoshikawa A, Hoshi Y, Tanaka T, Kishimoto S, Akahane Y, Miyakawa Y, Mayumi M. Phosphorylation in the carboxyl-terminal domain of the capsid protein of hepatitis B virus: evaluation with a monoclonal antibody. J Virol 1991; 65: 6024-6030
25. Watts NR, Conway JF, Cheng N, Stahl SJ, Belnap DM, Steven AC, Wingfield PT. The morphogenic linker peptide of HBV capsid protein forms a mobile array on the interior surface. EMBO J 2002; 21: 876-884
26. Seifer M, Zhou S, Standring DN. A micromolar pool of anti-genically distinct precursors is required to initiate cooperative assembly of hepatitis B virus capsids in Xenopus oocytes. J Virol 1993; 67: 249-257
27. Hirsch RC, Lavine JE, Chang LJ, Varmus HE, 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
28. 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
29. Lott L, Notvall L, Lanford RE. Transcomplementation of core and polymerase functions of the woolly monkey and human hepatitis B viruses. Virology 2003; 308: 330-339
30. Lott L, Beames B, Notvall L, Lanford RE. Interaction between hepatitis B virus core protein and reverse transcriptase. J Virol 2000; 74: 11479-11489
31. 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
32. Wang X, Grammatikakis N, Hu J. Role of p50/CDC37 in hepadnavirus assembly and replication. J Biol Chem 2002; 277: 24361-24367
33. Hu J, Flores D, Toft D, Wang X, Nguyen D. Requirement of heat shock protein 90 for human hepatitis B virus reverse transcriptase function. J Virol 2004; 78: 13122-13131
34. Kann M, Gerlich WH. Effect of core protein phosphorylation by protein kinase C on encapsidation of RNA within core particles of hepatitis B virus. J Virol 1994; 68: 7993-8000
35. Kau JH, Ting LP. Phosphorylation of the core protein of hepatitis B virus by a 46-kilodalton serine kinase. J Virol 1998; 72: 3796-3803
36. 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
37. Enomoto M, Sawano Y, Kosuge S, Yamano Y, Kuroki K, Ohtsuki K. High phosphorylation of HBV core protein by two alpha-type CK2-activated cAMP-dependent protein kinases in vitro. FEBS Lett 2006; 580: 894-899
38. Chang C, Zhou S, Ganem D, Standring DN. Phenotypic mixing between different hepadnavirus nucleocapsid proteins reveals C protein dimerization to be cis preferential. J Virol 1994; 68: 5225-5231
39. Ulrich R, Nassal M, Meisel H, Kruger DH. Core particles of hepatitis B virus as carrier for foreign epitopes. Adv Virus Res 1998; 50: 141-182
40. Skamel C, Ploss M, Bottcher B, Stehle T, Wallich R, Simon MM, Nassal M. Hepatitis B virus capsid-like particles can display the complete, dimeric outer surface protein C and stimulate production of protective antibody responses against Borrelia burgdorferi infection. J Biol Chem 2006; 281: 17474-17481
41. Nassal M, Skamel C, Kratz PA, Wallich R, Stehle T, Simon MM. A fusion product of the complete Borrelia burgdorferi outer surface protein A (OspA) and the hepatitis B virus capsid protein is highly immunogenic and induces protective immunity similar to that seen with an effective lipidated OspA vaccine formula. Eur J Immunol 2005; 35: 655-665
42. Geldmacher A, Skrastina D, Borisova G, Petrovskis I, Kruger DH, Pumpens P, Ulrich R. A hantavirus nucleocapsid protein segment exposed on hepatitis B virus core particles is highly immunogenic in mice when applied without adjuvants or in the presence of pre-existing anti-core antibodies. Vaccine 2005; 23: 3973-3983
43. Ulrich R, Koletzki D, Lachmamm S, Lundkvist A, Zankl A, Kazaks A, Kurth A, Gelderblom HR, Borisova G, Meisel H, Kruger DH. New chimaeric hepatitis B virus core particles carrying hantavirus (serotype Puumala) epitopes: inummogenicity and protection against virus challenge. J Biotechnol 1999; 73: 141-153
44. Kratz PA, Bottcher B, Nassal M. Native display of complete foreign protein domains on the surface of hepatitis B virus capsids. Proc Natl Acad Sci USA 1999; 96: 1915-1920
45. Deres K, Schroder CH, Paessens A, Goldmann S, Hacker HJ, Weber O, Kramer T, Niewohner U, Pleiss U, Stoltefuss J, Graef E, Koletzki D, Masantschek RN, Reimarm A, Jaeger R, Gross R, Beckermann B, Schlemmer KH, Haebich D, Rubsamen-Waigmann H. Inhibition of hepatitis B virus replication by drug-induced depletion of nucleocapsids. Science 2003; 299: 893-896
46. Stray SJ, Bourne CR, Punna S, Lewis WG, Finn MG, Zlotnick A. A heteroaryldihydropyrimidine activates and can misdirect hepatitis B virus capsid assembly. Proc Natl Acad Sci USA 2005; 102: 8138-8143
47. Stray SJ, Johnson JM, Kopek BG, Zlotnick A. An in vitro fluorescence screen to identify antivirals that disrupt hepatitis B virus capsid assembly. Nat Biotechnol 2006; 24: 358-362
48. Asif-Ullah M, Choi KJ, Choi KI, Jeong YJ, Yu YG. Identification of compounds that inhibit the interaction between core and surface protein of hepatitis B virus. Antiviral Res 2006; 70: 85-90
49. Heermann KH, Goldmann U, Schwartz W, Seyffarth T, Baumgarten H, Gerlich WH. Large surface proteins of hepatitis B virus containing the pre-s sequence. J Virol 1984; 52: 396-402
50. Cattaneo R, Will H, Hernandez N, Schaller H. Signals regulating hepatitis B surface antigen transcription. Nature 1983; 305: 336-338
51. Sheu SY, Lo SJ. Preferential ribosomal scanning is involved in the differential synthesis of the hepatitis B viral surface antigens from subgenomic transcripts. Virology 1992; 188: 353-357
52. Eble BE, MacRae DR, Lingappa VR, Ganem D. Multiple topogenic sequences determine the transmembrane orientation of the hepatitis B surface antigen. Mol Cell Biol 1987; 7: 3591-3601
53. Peterson DL, Nath N, Gavilanes F. Structure of hepatitis B surface antigen. Correlation of subtype with amino acid sequence and location of the carbohydrate moiety. J Biol Chem 1982; 257: 10414-10420
54. Eble BE, Lingappa VR, 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
55. Stibbe W, Gerlich WH. Structural relationships between minor and major proteins of hepatitis B surface antigen. J Virol 1983; 46: 626-628
56. Schmitt S, Glebe D, Tolle TK, Lochnit G, Linder D, Geyer R, Gerlich WH. 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
57. Persing DH, Varmus HE, Ganem D. The preS1 protein of hepatitis B virus is acylated at its amino terminus with myristic acid. J Virol 1987; 61: 1672-1677
58. 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
59. Bruss V, Lu X, Thomssen R, Gerlich WH. Post-translational alterations in transmembrane topology of the hepatitis B virus large envelope protein. EMBO J 1994; 13: 2273-2279
60. Prange R, Streeck RE. Novel transmembrane topology of the hepatitis B virus envelope proteins. EMBO J 1995; 14: 247-256
61. 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
62. Swameye I, Schaller H. Dual topology of the large envelope protein of duck hepatitis B virus: determinants preventing pre-S translocation and glycosylation. J Virol 1997; 71: 9434-9441
63. Guo JT, Pugh JC. Topology of the large envelope protein of duck hepatitis B virus suggests a mechanism for membrane translocation during particle morphogenesis. J Virol 1997; 71: 1107-1114
64. 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 USA 2003; 100: 5199-5204
65. Loffler-Mary H, Werr M, Prange R. Sequence-specific repression of cotranslational translocation of the hepatitis B virus envelope proteins coincides with binding of heat shock protein Hsc7O. Virology 1997; 235: 144-152
66. Prange R, Werr M, Loffler-Mary H. Chaperones involved in hepatitis B virus morphogenesis. Biol Chem 1999; 380: 305-314
67. Cho DY, Yang GH, Ryu CJ, Hong HJ. Molecular chaperone GRP78/BiP interacts with the large surface protein of hepatitis B virus in vitro and in vivo. J Virol 2003; 77: 2784-2788
68. Berting A, Hahnen J, Kroger M, Gerlich WH. Computer-aided studies on the spatial structure of the small hepatitis B surface protein. Intervirology 1995; 38: 8-15
69. Lambert C, Prange R. Dual topology of the hepatitis B virus large envelope protein: determinants influencing post-translational pre-S translocation. J Biol Chem 2001; 276: 22265-22272
70. Grgacic EV. Identification of structural determinants of the first transmembrane domain of the small envelope protein of duck hepatitis B virus essential for particle morphogenesis. J Gen Virol 2002; 83: 1635-1644
71. Grgacic EV, Kuhn C, Schaller H. Hepadnavirus envelope topology: insertion of a loop region in the membrane and role of S in L protein translocation. J Virol 2000; 74: 2455-2458
72. Grgacic EV, Anderson DA. St, a truncated envelope protein derived from the S protein of duck hepatitis B virus, acts as a chaperone for the folding of the large envelope protein. J Virol 2005; 79: 5346-5352
73. Lambert C, Mann S, Prange R. Assessment of determinants affecting the dual topology of hepadnaviral large envelope proteins. J Gen Virol 2004; 85: 1221-1225
74. 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
75. 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
76. Hildt E, Saher G, Bruss V, Hofschneider PH. The hepatitis B virus large surface protein (LHBs) is a transcriptional activator. Virology 1996; 225: 235-239
77. Wounderlich G, Bruss V. Characterization of early hepatitis B virus surface protein oligomers. Arch Virol 1996; 141: 1191-1205
78. Mangold CM, Unckell F, Werr M, Streeck RE. Secretion and antigenicity of hepatitis B virus small envelope proteins lacking cysteines in the major antigenic region. Virology 1995; 211: 535-543
79. Mangold CM, Streeck RE. Mutational analysis of the cysteine residues in the hepatitis B virus small envelope protein. J Virol 1993; 67: 4588-4597
80. Grgacic EV, Anderson DA. The large surface protein of duck hepatitis B virus is phosphorylated in the pre-S domain. J Virol 1994; 68: 7344-7350
81. Rothmann K, Schnolzer M, Radziwill G, Hildt E, Moelling K, Schaller H. Host cell-virus cross talk: phosphorylation of a hepatitis B virus envelope protein mediates intracellular signaling. J Virol 1998; 72: 10138-10147
82. Borel C, Sunyach C, Hantz O, Trepo C, Kay A. Phosphorylation of DHBV pre-S: identification of the major site of phosphorylation and effects of mutations on the virus life cycle. Virology 1998; 242: 90-98
83. Grgacic EV, Lin B, Gazina EV, Snooks MJ, Anderson DA. Normal phosphorylation of duck hepatitis B virus L protein is dispensable for infectivity. J Gen Virol 1998; 79 (Pt 11): 2743-2751
84. Huovila AP, Eder AM, Fuller SD. Hepatitis B surface antigen assembles in a post-ER, pre-Golgi compartment. J Cell Biol 1992; 118: 1305-1320
85. Patzer EJ, Nakamura GR, Simonsen CC, Levinson AD, Brands R. Intracellular assembly and packaging of hepatitis B surface antigen particles occur in the endoplasmic reticulum. J Virol 1986; 58: 884-892
86. Gilbert RJ, Beales L, Blond D, Simon MN, Lin BY, Chisari FV, Stuart DI, Rowlands DJ. Hepatitis B small surface antigen particles are octahedral. Proc Natl Acad Sci USA 2005; 102: 14783-14788
87. McAleer WJ, Buynak EB, Maigetter RZ, Wampler DE, Miller WJ, Hilleman MR. Human hepatitis B vaccine from recombinant yeast. Nature 1984; 307: 178-180
88. Xu Z, Bruss V, Yen TS. Formation of intracellular particles by hepatitis B virus large surface protein. J Virol 1997; 71: 5487-5494
89. Gavilanes F, Gonzalez-Ros JM, Peterson DL. Structure of hepatitis B surface antigen. Characterization of the lipid components and their association with the viral proteins. J Biol Chem 1982; 257: 7770-7777
90. Persing DH, Varmus HE, Ganem D. Inhibition of secretion of hepatitis B surface antigen by a related presurface polypeptide. Science 1986; 234: 1388-1391
91. Ou JH, Rutter WJ. Regulation of secretion of the hepatitis B virus major surface antigen by the preS-1 protein. J Virol 1987; 61: 782-786
92. Xu Z, Jensen G, Yen TS. Activation of hepatitis B virus S promoter by the viral large surface protein via induction of stress in the endoplasmic reticulum. J Virol 1997; 71: 7387-7392
93. Chisari FV, Ferrari C. Hepatitis B virus immunopathogenesis. Annu Rev Immunol 1995; 13: 29-60
94. Gazina E, Gallina A, Milanesi G. Common localization of retention determinants in hepatitis B virus L protein from different strains. J Gen Virol 1996; 77 (Pt 12): 3069-3075
95. Kuroki K, Russnak R, Ganem D. Novel N-terminal amino acid sequence required for retention of a hepatitis B virus glycoprotein in the endoplasmic reticulum. Mol Cell Biol 1989; 9: 4459-4466
96. Prange R, Clemen A, Streeck RE. Myristylation is involved in intracellular retention of hepatitis B virus envelope proteins. J Virol 1991; 65: 3919-3923
97. Gazina EV, Lin B, Gallina A, Milanesi G, Anderson DA. Intracellular retention of duck hepatitis B virus large surface protein is independent of preS topology. Virology 1998; 242: 266-278
98. Gerhardt E, Bruss V. Phenotypic mixing of rodent but not avian hepadnavirus surface proteins into human hepatitis B virus particles. J Virol 1995; 69: 1201-1208
99. Lambert C, Thome N, Kluck CJ, Prange R. Functional incorporation of green fluorescent protein into hepatitis B virus envelope particles. Virology 2004; 330: 158-167
100. Bruss V, Ganem D. Mutational analysis of hepatitis B surface antigen particle assembly and secretion. J Virol 1991; 65: 3813-3820
101. Mason WS, Aldrich C, Summers J, Taylor JM. Asymmetric replication of duck hepatitis B virus DNA in liver cells: Free minus-strand DNA. Proc Natl Acad Sci USA 1982; 79: 3997-4001
102. Weiser B, Ganem D, Seeger C, Varmus HE. Closed circular viral DNA and asymmetrical heterogeneous forms in livers from animals infected with ground squirrel hepatitis virus. J Virol 1983; 48: 1-9
103. Summers J, Mason WS. Replication of the genome of a hepatitis B-like virus by reverse transcription of an RNA intermediate. Cell 1982; 29: 403-415
104. Yu M, Summers J. A domain of the hepadnavirus capsid protein is specifically required for DNA maturation and virus assembly. J Virol 1991; 65: 2511-2517
105. Gerelsaikhan T, Tavis JE, Bruss V. Hepatitis B virus nucleocapsid envelopment does not occur without genomic DNA synthesis. J Virol 1996; 70: 4269-4274
106. Wei Y, Tavis JE, Ganem D. Relationship between viral DNA synthesis and virion envelopment in hepatitis B viruses. J Virol 1996; 70: 6455-6458
107. Perlman D, Hu J. Duck hepatitis B virus virion secretion requires a double-stranded DNA genome. J Virol 2003; 77: 2287-2294
108. Yu M, Summers J. Multiple functions of capsid protein phosphorylation in duck hepatitis B virus replication. J Virol 1994; 68: 4341-4348
109. Yu M, Summers J. Phosphorylation of the duck hepatitis B virus capsid protein associated with conformational changes in the C terminus. J Virol 1994; 68: 2965-2969
110. Perlman DH, Berg EA, O'connor PB, Costello CE, Hu J. Reverse transcription-associated dephosphorylation of hepadnavirus nucleocapsids. Proc Natl Acad Sci USA 2005; 102: 9020-9025
111. Gazina EV, Fielding JE, Lin B, Anderson DA. Core protein phosphorylation modulates pregenomic RNA encapsidation to different extents in human and duck hepatitis B viruses. J Virol 2000; 74: 4721-4728
112. Yuan TT, Sahu GK, Whitehead WE, Greenberg R, Shih C. The mechanism of an immature secretion phenotype of a highly frequent naturally occurring missense mutation at codon 97 of human hepatitis B virus core antigen. J Virol 1999; 73: 5731-5740
113. Yuan TT, Shih C. A frequent, naturally occurring mutation (P130T) of human hepatitis B virus core antigen is compensatory for immature secretion phenotype of another frequent variant (I97L). J Virol 2000; 74: 4929-4932
114. Jilbert AR, Miller DS, Scougall CA, Turnbull H, Burrell CJ. Kinetics of duck hepatitis B virus infection following low dose virus inoculation: one virus DNA genome is infectious in neonatal ducks. Virology 1996; 226: 338-345
115. Barker LF, Murray R. Relationship of virus dose to incubation time of clinical hepatitis and time of appearance of hepatitis-associated antigen. Am J Med Sci 1972; 263: 27-33
116. 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 USA 2003; 100: 9849-9854
117. Biermer M, Puro R, Schneider RJ. Tumor necrosis factor alpha inhibition of hepatitis B virus replication involves disruption of capsid Integrity through activation of NF-kappaB. J Virol 2003; 77: 4033-4042
118. Mabit H, Schaller H. Intracellular hepadnavirus nucleocapsids are selected for secretion by envelope protein-independent membrane binding. J Virol 2000; 74: 11472-11478
119. von Schwedler UK, Stuchell M, Muller B, Ward DM, Chung HY, Morita E, Wang HE, Davis T, He GP, Cimbora DM, Scott A, Krausslich FIG, Kaplan J, Morham SG, Sundquist WI. The protein network of HIV budding. Cell 2003; 114: 701-713
120. Freed EO. Viral late domains. J Virol 2002; 76: 4679-4687
121. 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
122. Bruss V, Ganem D. The role of envelope proteins in hepatitis B virus assembly. Proc Natl Acad Sci USA 1991; 88: 1059-1063
123. 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
124. Summers J, Smith PM, Huang MJ, Yu MS. Morphogenetic and regulatory effects of mutations in the envelope proteins of an avian hepadnavirus. J Virol 1991; 65: 1310-1317
125. 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 Suppl 4: S102-S104
126. Prange R, Werr M, Birkner M, Hilfrich R, Streeck RE. Properties of modified hepatitis B virus surface antigen particles carrying preS epitopes. J Gen Virol 1995; 76 (Pt 9): 2131-2140
127. Summers J, Smith PM, Horwich AL. Hepadnavirus envelope proteins regulate covalently closed circular DNA amplification. J Virol 1990; 64: 2819-2824
128. Lenhoff RJ, Summers J. Coordinate regulation of replication and virus assembly by the large envelope protein of an avian hepadnavirus. J Virol 1994; 68: 4565-4571
129. 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
130. Cheng RH, Kuhn RJ, Olson NH, Rossmann MG, Choi HK, Smith TJ, Baker TS. Nucleocapsid and glycoprotein organization in an enveloped virus. Cell 1995; 80: 621-630
131. Le Pogam S, Shih C. Influence of a putative intermolecular interaction between core and the pre-S1 domain of the large envelope protein on hepatitis B virus secretion. J Virol 2002; 76: 6510-6517
132. 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
133. 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
134. Koschel M, Thomssen R, Bruss V. Extensive mutagenesis of the hepatitis B virus core gene and mapping of mutations that allow capsid formation. J Virol 1999; 73: 2153-2160
135. Koschel M, Oed D, Gerelsaikhan T, Thomssen R, Bruss V. Hepatitis B virus core gene mutations which block nucleocapsid envelopment. J Virol 2000; 74: 1-7
136. Le Pogam S, Yuan TT, Sahu GK, Chatterjee S, Shih C. Low-level secretion of human hepatitis B virus virions caused by two independent, naturally occurring mutations (P5T and L60V) in the capsid protein. J Virol 2000; 74: 9099-9105
137. Kluge B, Schlager M, Pairan A, Bruss V. Determination of the minimal distance between the matrix and transmembrane domains of the large hepatitis B virus envelope protein. J Virol 2005; 79: 7918-7921
138. Dyson MR, Murray K. Selection of peptide inhibitors of interactions involved in complex protein assemblies: association of the core and surface antigens of hepatitis B virus. Proc Natl Acad Sci USA 1995; 92: 2194-2198
139. Bottcher B, Tsuji N, Takahashi H, Dyson MR, Zhao S, Crowther RA, Murray K. Peptides that block hepatitis B virus assembly: analysis by cryomicroscopy, mutagenesis and transfection. EMBO J 1998; 17: 6839-6845