Structural Organization of Pregenomic RNA and the Carboxy-Terminal Domain of the Capsid Protein of Hepatitis B Virus

PLoS Pathogens

Volumn 8, Issue 9, 2012, Pages

  Wang, Joseph C Y ^a   Dhason, Mary S ^a   Zlotnick, Adam ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CHAPERONE; GENOMIC RNA; SINGLE STRANDED RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; HEPATITIS B VIRUS; IN VITRO STUDY; NONHUMAN; POROSITY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA STRUCTURE; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

CAPSID; CAPSID PROTEINS; DNA, VIRAL; GENOME, VIRAL; HEPATITIS B VIRUS; MOLECULAR CHAPERONES; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RNA, VIRAL; VIRUS ASSEMBLY;

HEPATITIS B VIRUS; MIRIDAE;

EID: 84866941201     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002919     Document Type: Article

References (58)

1. World Health Organization [WHO] (2004) Hepatitis B vaccines. Weekly epidemiological record 79 9 Jul 2004. WHO. pp. 255-263.
2. Webster T, (2011) Ambivalence and Activism: Employment Discrimination in China. Vand J Transnat'l L 44: 643-709.
3. Lu J, (2009) Employment Discrimination in China: The Current Situation and Principle Challenges. Hamline L Rev 32: 133-190.
4. Summers J, Mason WS, (1982) Replication of the genome of a hepatitis B-like virus by reverse transcription of an RNA intermediate. Cell 29: 403-415.
5. Heermann KH, Goldmann U, Schwartz W, Seyffarth T, Baumgarten H, et al. (1984) Large surface proteins of hepatitis B virus containing the pre-s sequence. J Virol 52: 396-402.
6. Kenney JM, von Bonsdorff CH, Nassal M, Fuller SD, (1995) Evolutionary conservation in the hepatitis B virus core structure: comparison of human and duck cores. Structure 3: 1009-1019.
7. Stannard LM, Hodgkiss M, (1979) Morphological irregularities in Dane particle cores. J Gen Virol 45: 509-514.
8. Crowther RA, Kiselev NA, Bottcher B, Berriman JA, Borisova GP, et al. (1994) Three-dimensional structure of hepatitis B virus core particles determined by electron cryomicroscopy. Cell 77: 943-950.
9. Wynne SA, Crowther RA, Leslie AG, (1999) The crystal structure of the human hepatitis B virus capsid. Mol Cell 3: 771-780.
10. Zlotnick A, Cheng N, Conway JF, Booy FP, Steven AC, et al. (1996) Dimorphism of hepatitis B virus capsids is strongly influenced by the C-terminus of the capsid protein. Biochemistry 35: 7412-7421.
11. Wingfield PT, Stahl SJ, Williams RW, Steven AC, (1995) Hepatitis core antigen produced in Escherichia coli: subunit composition, conformational analysis, and in vitro capsid assembly. Biochemistry 34: 4919-4932.
12. Beames B, Lanford RE, (1993) Carboxy-terminal truncations of the HBV core protein affect capsid formation and the apparent size of encapsidated HBV RNA. Virology 194: 597-607.
13. Nassal M, (1992) 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 66: 4107-4116.
14. Yu M, Summers J, (1991) A domain of the hepadnavirus capsid protein is specifically required for DNA maturation and virus assembly. J Virol 65: 2511-2517.
15. Porterfield JZ, Dhason MS, Loeb DD, Nassal M, Stray SJ, et al. (2010) Full-length hepatitis B virus core protein packages viral and heterologous RNA with similarly high levels of cooperativity. J Virol 84: 7174-7184.
16. Conway JF, Cheng N, Zlotnick A, Wingfield PT, Stahl SJ, et al. (1997) Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy. Nature 386: 91-94.
17. Bottcher B, Wynne SA, Crowther RA, (1997) Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386: 88-91.
18. Zlotnick A, Cheng N, Stahl SJ, Conway JF, Steven AC, et al. (1997) 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 94: 9556-9561.
19. Watts NR, Conway JF, Cheng N, Stahl SJ, Belnap DM, et al. (2002) The morphogenic linker peptide of HBV capsid protein forms a mobile array on the interior surface. Embo J 21: 876-884.
20. Cheng N, Conway JF, Watts NR, Hainfeld JF, Joshi V, et al. (1999) Tetrairidium, a four-atom cluster, is readily visible as a density label in three-dimensional cryo-EM maps of proteins at 10-25 A resolution. J Struct Biol 127: 169-176.
21. Lewellyn EB, Loeb DD, (2011) Serine phosphoacceptor sites within the core protein of hepatitis B virus contribute to genome replication pleiotropically. PLoS One 6: e17202.
22. Lan YT, Li J, Liao W, Ou J, (1999) Roles of the three major phosphorylation sites of hepatitis B virus core protein in viral replication. Virology 259: 342-348.
23. Machida A, Ohnuma H, Tsuda F, Yoshikawa A, Hoshi Y, et al. (1991) Phosphorylation in the carboxyl-terminal domain of the capsid protein of hepatitis B virus: evaluation with a monoclonal antibody. J Virol 65: 6024-6030.
24. Yeh CT, Ou JH, (1991) Phosphorylation of hepatitis B virus precore and core proteins. J Virol 65: 2327-2331.
25. Melegari M, Wolf SK, Schneider RJ, (2005) Hepatitis B virus DNA replication is coordinated by core protein serine phosphorylation and HBx expression. J Virol 79: 9810-9820.
26. Kock J, Nassal M, Deres K, Blum HE, von Weizsacker F, (2004) Hepatitis B virus nucleocapsids formed by carboxy-terminally mutated core proteins contain spliced viral genomes but lack full-size DNA. J Virol 78: 13812-13818.
27. Gazina EV, Fielding JE, Lin B, Anderson DA, (2000) Core protein phosphorylation modulates pregenomic RNA encapsidation to different extents in human and duck hepatitis B viruses. J Virol 74: 4721-4728.
28. Chen C, Wang JC, Zlotnick A, (2011) A Kinase Chaperones Hepatitis B Virus Capsid Assembly and Captures Capsid Dynamics in vitro. PLoS Pathog 7: e1002388.
29. Daub H, Blencke S, Habenberger P, Kurtenbach A, Dennenmoser J, et al. (2002) Identification of SRPK1 and SRPK2 as the major cellular protein kinases phosphorylating hepatitis B virus core protein. J Virol 76: 8124-8137.
30. Ricco R, Kanduc D, (2010) Hepatitis B virus and Homo sapiens proteome-wide analysis: A profusion of viral peptide overlaps in neuron-specific human proteins. Biologics 4: 75-81.
31. Eckhardt SG, Milich DR, McLachlan A, (1991) Hepatitis B virus core antigen has two nuclear localization sequences in the arginine-rich carboxyl terminus. J Virol 65: 575-582.
32. Kann M, Sodeik B, Vlachou A, Gerlich WH, Helenius A, (1999) Phosphorylation-dependent binding of hepatitis B virus core particles to the nuclear pore complex. J Cell Biol 145: 45-55.
33. Schmitz A, Schwarz A, Foss M, Zhou L, Rabe B, et al. (2010) Nucleoporin 153 arrests the nuclear import of hepatitis B virus capsids in the nuclear basket. PLoS Pathog 6: e1000741.
34. Dryden KA, Wieland SF, Whitten-Bauer C, Gerin JL, Chisari FV, et al. (2006) Native hepatitis B virions and capsids visualized by electron cryomicroscopy. Mol Cell 22: 843-850.
35. Roseman AM, Berriman JA, Wynne SA, Butler PJ, Crowther RA, (2005) A structural model for maturation of the hepatitis B virus core. Proc Natl Acad Sci U S A 102: 15821-15826.
36. Perlman DH, Berg EA, O'Connor P B, Costello CE, Hu J, (2005) Reverse transcription-associated dephosphorylation of hepadnavirus nucleocapsids. Proc Natl Acad Sci U S A 102: 9020-9025.
37. Pugh J, Zweidler A, Summers J, (1989) Characterization of the major duck hepatitis B virus core particle protein. J Virol 63: 1371-1376.
38. Chua PK, Tang FM, Huang JY, Suen CS, Shih C, (2010) Testing the balanced electrostatic interaction hypothesis of hepatitis B virus DNA synthesis by using an in vivo charge rebalance approach. J Virol 84: 2340-2351.
39. Basagoudanavar SH, Perlman DH, Hu J, (2007) Regulation of hepadnavirus reverse transcription by dynamic nucleocapsid phosphorylation. J Virol 81: 1641-1649.
40. Lewellyn EB, Loeb DD, (2011) The arginine clusters of the carboxy-terminal domain of the core protein of hepatitis B virus make pleiotropic contributions to genome replication. J Virol 85: 1298-1309.
41. Liao W, Ou JH, (1995) Phosphorylation and nuclear localization of the hepatitis B virus core protein: significance of serine in the three repeated SPRRR motifs. J Virol 69: 1025-1029.
42. Churchill ME, Travers AA, (1991) Protein motifs that recognize structural features of DNA. Trends Biochem Sci 16: 92-97.
43. Happel N, Doenecke D, (2009) Histone H1 and its isoforms: contribution to chromatin structure and function. Gene 431: 1-12.
44. Roque A, Ponte I, Arrondo JL, Suau P, (2008) Phosphorylation of the carboxy-terminal domain of histone H1: effects on secondary structure and DNA condensation. Nucleic Acids Res 36: 4719-4726.
45. Alexandrow MG, Hamlin JL, (2005) Chromatin decondensation in S-phase involves recruitment of Cdk2 by Cdc45 and histone H1 phosphorylation. J Cell Biol 168: 875-886.
46. Th'ng JP, Guo XW, Swank RA, Crissman HA, Bradbury EM, (1994) Inhibition of histone phosphorylation by staurosporine leads to chromosome decondensation. J Biol Chem 269: 9568-9573.
47. Tihova M, Dryden KA, Le TV, Harvey SC, Johnson JE, et al. (2004) Nodavirus coat protein imposes dodecahedral RNA structure independent of nucleotide sequence and length. J Virol 78: 2897-2905.
48. Johnson KN, Tang L, Johnson JE, Ball LA, (2004) Heterologous RNA encapsidated in Pariacoto virus-like particles forms a dodecahedral cage similar to genomic RNA in wild-type virions. J Virol 78: 11371-11378.
49. Yu M, Summers J, (1994) Phosphorylation of the duck hepatitis B virus capsid protein associated with conformational changes in the C terminus. J Virol 68: 2965-2969.
50. Seifer M, Standring DN, (1994) A protease-sensitive hinge linking the two domains of the hepatitis B virus core protein is exposed on the viral capsid surface. J Virol 68: 5548-5555.
51. Hilmer JK, Zlotnick A, Bothner B, (2008) Conformational equilibria and rates of localized motion within hepatitis B virus capsids. J Mol Biol 375: 581-594.
52. Ning X, Nguyen D, Mentzer L, Adams C, Lee H, et al. (2011) Secretion of genome-free hepatitis B virus-single strand blocking model for virion morphogenesis of para-retrovirus. PLoS Pathog 7: e1002255.
53. Dhason MS, Wang JC, Hagan MF, Zlotnick A, (2012) Differential assembly of Hepatitis B Virus core protein on single- and double-stranded nucleic acid suggest the dsDNA-filled core is spring-loaded. Virology 430: 20-29.
54. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, et al. (2007) EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 157: 38-46.
55. Yan X, Dryden KA, Tang J, Baker TS, (2007) Ab initio random model method facilitates 3D reconstruction of icosahedral particles. J Struct Biol 157: 211-225.
56. Yan X, Sinkovits RS, Baker TS, (2007) AUTO3DEM-an automated and high throughput program for image reconstruction of icosahedral particles. J Struct Biol 157: 73-82.
57. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
58. Porterfield JZ, Zlotnick A, (2010) A simple and general method for determining the protein and nucleic acid content of viruses by UV absorbance. Virology 407: 281-288.