A high level of mutation tolerance in the multifunctional sequence encoding the RNA encapsidation signal of an avian hepatitis B virus and slow evolution rate revealed by in vivo infection

Journal of Virology

Volumn 85, Issue 18, 2011, Pages 9300-9313

  Schmid, Bernadette ^a   Rösler, Christine ^a   Nassal, Michael ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DOUBLE STRANDED DNA; HEPATITIS B(E) ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN DETECTION; ARTICLE; CONTROLLED STUDY; DUCK; DUCK HEPATITIS B; DUCK HEPATITIS B VIRUS; EVOLUTION; HEPATITIS B VIRUS; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MIXED INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOUTHERN BLOTTING; VIREMIA; VIRUS CAPSID; VIRUS CULTURE; VIRUS GENOME; VIRUS MUTATION; VIRUS NUCLEOCAPSID; VIRUS REPLICATION;

ANIMALS; HEPATITIS B VIRUS, DUCK; MODELS, BIOLOGICAL; MUTAGENESIS; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; REVERSE TRANSCRIPTION; RNA, VIRAL; RNA-DIRECTED DNA POLYMERASE; VIRUS REPLICATION;

ANAS; AVES; DUCK HEPATITIS B VIRUS; HEPATITIS B VIRUS;

EID: 80052433166     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05005-11     Document Type: Article

References (66)

1. Abraham, T. M., and D. D. Loeb. 2006. Base pairing between the 5' half of epsilon and a cis-acting sequence, phi, makes a contribution to the synthesis of minus-strand DNA for human hepatitis B virus. J. Virol. 80:4380-4387.
2. Abram, M. E., A. L. Ferris, W. Shao, W. G. Alvord, and S. H. Hughes. 2010. Nature, position, and frequency of mutations made in a single cycle of HIV-1 replication. J. Virol. 84:9864-9878.
3. Addison, W. R., et al. 2002. Half-life of the duck hepatitis B virus covalently closed circular DNA pool in vivo following inhibition of viral replication. J. Virol. 76:6356-6363.
4. Asabe, S., et al. 2009. The size of the viral inoculum contributes to the outcome of hepatitis B virus infection. J. Virol. 83:9652-9662.
5. Beck, J., H. Bartos, and M. Nassal. 1997. Experimental confirmation of a hepatitis B virus (HBV) epsilon-like bulge-and-loop structure in avian HBV RNA encapsidation signals. Virology 227:500-504.
6. Beck, J., and M. Nassal. 2003. 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. 278:36128-36138.
7. Beck, J., and M. Nassal. 1998. Formation of a functional hepatitis B virus replication initiation complex involves a major structural alteration in the RNA template. Mol. Cell. Biol. 18:6265-6272.
8. Beck, J., and M. Nassal. 2007. Hepatitis B virus replication. World J. Gastroenterol. 13:48-64.
9. Beck, J., and M. Nassal. 1997. Sequence- and structure-specific determinants in the interaction between the RNA encapsidation signal and reverse transcriptase of avian hepatitis B viruses. J. Virol. 71:4971-4980.
10. Beckel-Mitchener, A., and J. Summers. 1997. A novel transcriptional element in circular DNA monomers of the duck hepatitis B virus. J. Virol. 71:7917-7922.
11. Calvert, J., and J. Summers. 1994. Two regions of an avian hepadnavirus RNA pregenome are required in cis for encapsidation. J. Virol. 68:2084-2090.
12. Chen, M. T., et al. 2004. A function of the hepatitis B virus precore protein is to regulate the immune response to the core antigen. Proc. Natl. Acad. Sci. U. S. A. 101:14913-14918.
13. Dallmeier, K., U. Schultz, and M. Nassal. 2008. Heterologous replacement of the supposed host determining region of avihepadnaviruses: high in vivo infectivity despite low infectivity for hepatocytes. PLoS Pathog. 4:e1000230.
14. Das, A. T., and B. Berkhout. 2010. HIV-1 evolution: frustrating therapies, but disclosing molecular mechanisms. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365:1965-1973.
15. Duffy, S., L. A. Shackelton, and E. C. Holmes. 2008. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9:267-276.
16. Emanuelsson, O., S. Brunak, G. von Heijne, and H. Nielsen. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2:953-971.
17. Flodell, S., et al. 2006. Solution structure of the apical stem-loop of the human hepatitis B virus encapsidation signal. Nucleic Acids Res. 34:4449-4457.
18. Frelin, L., et al. 2009. A mechanism to explain the selection of the hepatitis e antigen-negative mutant during chronic hepatitis B virus infection. J. Virol. 83:1379-1392.
19. Girard, F. C., O. M. Ottink, K. A. Ampt, M. Tessari, and S. S. Wijmenga. 2007. Thermodynamics and NMR studies on duck, heron and human HBV encapsidation signals. Nucleic Acids Res. 35:2800-2811.
20. Guo, J. T., et al. 2003. Conditional replication of duck hepatitis B virus in hepatoma cells. J. Virol. 77:1885-1893.
21. Habig, J. W., and D. D. Loeb. 2003. The conformation of the 3' end of the minus-strand DNA makes multiple contributions to template switches during plus-strand DNA synthesis of duck hepatitis B virus. J. Virol. 77:12401-12411.
22. Haines, K. M., and D. D. Loeb. 2007. The sequence of the RNA primer and the DNA template influence the initiation of plus-strand DNA synthesis in hepatitis B virus. J. Mol. Biol. 370:471-480.
23. Hu, J., and M. Boyer. 2006. Hepatitis B virus reverse transcriptase and epsilon RNA sequences required for specific interaction in vitro. J. Virol. 80:2141-2150.
24. Hu, J., D. Toft, D. Anselmo, and X. Wang. 2002. In vitro reconstitution of functional hepadnavirus reverse transcriptase with cellular chaperone proteins. J. Virol. 76:269-279.
25. Hu, K., J. Beck, and M. Nassal. 2004. SELEX-derived aptamers of the duck hepatitis B virus RNA encapsidation signal distinguish critical and noncritical residues for productive initiation of reverse transcription. Nucleic Acids Res. 32:4377-4389.
26. Huang, M., and J. Summers. 1994. pet, a small sequence distal to the pregenome cap site, is required for expression of the duck hepatitis B virus pregenome. J. Virol. 68:1564-1572.
27. Jiang, H., and D. D. Loeb. 1997. Insertions within epsilon affect synthesis of minus-strand DNA before the template switch for duck hepatitis B virus. J. Virol. 71:5345-5354.
28. Jilbert, A. R., et al. 1998. Characterization of age- and dose-related outcomes of duck hepatitis B virus infection. Virology 244:273-282.
29. Jilbert, A. R., D. S. Miller, C. A. Scougall, H. Turnbull, and C. J. Burrell. 1996. Kinetics of duck hepatitis B virus infection following low dose virus inoculation: one virus DNA genome is infectious in neonatal ducks. Virology 226:338-345.
30. Knaus, T., and M. Nassal. 1993. The encapsidation signal on the hepatitis B virus RNA pregenome forms a stem-loop structure that is critical for its function. Nucleic Acids Res. 21:3967-3975.
31. Köck, J., M. Nassal, K. Deres, H. E. Blum, and F. von Weizsäcker. 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.
32. Lenhoff, R. J., C. A. Luscombe, and J. Summers. 1998. Competition in vivo between a cytopathic variant and a wild-type duck hepatitis B virus. Virology 251:85-95.
33. Liu, N., R. Tian, and D. D. Loeb. 2003. Base pairing among three cis-acting sequences contributes to template switching during hepadnavirus reverse transcription. Proc. Natl. Acad. Sci. U. S. A. 100:1984-1989.
34. Loeb, D. D., A. A. Mack, and R. Tian. 2002. A secondary structure that contains the 5' and 3' splice sites suppresses splicing of duck hepatitis B virus pregenomic RNA. J. Virol. 76:10195-10202.
35. Maguire, M. L., and D. D. Loeb. 2010. cis-acting sequences that contribute to synthesis of minus-strand DNA are not conserved between hepadnaviruses. J. Virol. 84:12824-12831.
36. Mason, W. S., S. Litwin, and A. R. Jilbert. 2008. Immune selection during chronic hepadnavirus infection. Hepatol. Int. 2:3-16.
37. Mason, W. S., S. Litwin, C. Xu, and A. R. Jilbert. 2007. Hepatocyte turnover in transient and chronic hepadnavirus infections. J. Viral Hepat. 14(Suppl. 1):22-28.
38. Nassal, M. 2008. Hepatitis B viruses: reverse transcription a different way. Virus Res. 134:235-249.
39. Nassal, M., et al. 2007. A structural model for duck hepatitis B virus core protein derived by extensive mutagenesis. J. Virol. 81:13218-13229.
40. Nassal, M., and A. Rieger. 1996. A bulged region of the hepatitis B virus RNA encapsidation signal contains the replication origin for discontinuous first-strand DNA synthesis. J. Virol. 70:2764-2773.
41. Nudler, E. 2009. RNA polymerase active center: the molecular engine of transcription. Annu. Rev. Biochem. 78:335-361.
42. Obert, S., et al. 1996. A splice hepadnavirus RNA that is essential for virus replication. EMBO J. 15:2565-2574.
43. Orr, H. A. 2009. Fitness and its role in evolutionary genetics. Nat. Rev. Genet. 10:531-539.
44. Ostrow, K. M., and D. D. Loeb. 2004. Chimeras of duck and heron hepatitis B viruses provide evidence for functional interactions between viral components of pregenomic RNA encapsidation. J. Virol. 78:8780-8787.
45. Ostrow, K. M., and D. D. Loeb. 2004. Underrepresentation of the 3' region of the capsid pregenomic RNA of duck hepatitis B virus. J. Virol. 78:2179- 2186.
46. Prassolov, A., et al. 2003. New hepatitis B virus of cranes that has an unexpected broad host range. J. Virol. 77:1964-1976.
47. Pult, I., N. Abbott, Y. Y. Zhang, and J. Summers. 2001. Frequency of spontaneous mutations in an avian hepadnavirus infection. J. Virol. 75:9623- 9632.
48. Reaiche, G. Y., M. F. Le Mire, W. S. Mason, and A. R. Jilbert. 2010. The persistence in the liver of residual duck hepatitis B virus covalently closed circular DNA is not dependent upon new viral DNA synthesis. Virology 406:286-292.
49. Sanjuan, R., M. R. Nebot, N. Chirico, L. M. Mansky, and R. Belshaw. 2010. Viral mutation rates. J. Virol. 84:9733-9748.
50. Schaaf, S. G., J. Beck, and M. Nassal. 1999. A small 2'-OH- and basedependent recognition element downstream of the initiation site in the RNA encapsidation signal is essential for hepatitis B virus replication initiation. J. Biol. Chem. 274:37787-37794.
51. Schlicht, H. J., J. Salfeld, and H. Schaller. 1987. The duck hepatitis B virus pre-C region encodes a signal sequence which is essential for synthesis and secretion of processed core proteins but not for virus formation. J. Virol. 61:3701-3709.
52. Stahl, M., J. Beck, and M. Nassal. 2007. Chaperones activate hepadnavirus reverse transcriptase by transiently exposing a C-proximal region in the terminal protein domain that contributes to epsilon RNA binding. J. Virol. 81:13354-13364.
53. Stahl, M., M. Retzlaff, M. Nassal, and J. Beck. 2007. 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. 35:6124-6136.
54. Tang, H., and A. McLachlan. 2002. A pregenomic RNA sequence adjacent to DR1 and complementary to epsilon influences hepatitis B virus replication efficiency. Virology 303:199-210.
55. Tavis, J. E., and D. Ganem. 1996. Evidence for activation of the hepatitis B virus polymerase by binding of its RNA template. J. Virol. 70:5741-5750.
56. Tavis, J. E., and D. Ganem. 1995. RNA sequences controlling the initiation and transfer of duck hepatitis B virus minus-strand DNA. J. Virol. 69:4283-4291.
57. Tohidi-Esfahani, R., K. Vickery, and Y. Cossart. 2010. The early host innate immune response to duck hepatitis B virus infection. J. Gen. Virol. 91:509-520.
58. Triyatni, M., et al. 2001. Sequence comparison of an Australian duck hepatitis B virus strain with other avian hepadnaviruses. J. Gen. Virol. 82:373-378.
59. Vorreiter, J., et al. 2007. Monoclonal antibodies providing topological information on the duck hepatitis B virus core protein and avihepadnaviral nucleocapsid structure. J. Virol. 81:13230-13234.
60. Walters, K. A., M. A. Joyce, W. R. Addison, K. P. Fischer, and D. L. Tyrrell. 2004. Superinfection exclusion in duck hepatitis B virus infection is mediated by the large surface antigen. J. Virol. 78:7925-7937.
61. Wang, G. H., and C. Seeger. 1993. Novel mechanism for reverse transcription in hepatitis B viruses. J. Virol. 67:6507-6512.
62. Wang, G. H., and C. Seeger. 1992. The reverse transcriptase of hepatitis B virus acts as a protein primer for viral DNA synthesis. Cell 71:663-670.
63. Zhang, Y. Y., and J. Summers. 1999. Enrichment of a precore-minus mutant of duck hepatitis B virus in experimental mixed infections. J. Virol. 73:3616-3622.
64. Zhang, Y. Y., and J. Summers. 2000. Low dynamic state of viral competition in a chronic avian hepadnavirus infection. J. Virol. 74:5257-5265.
65. Zhang, Y. Y., and J. Summers. 2004. Rapid production of neutralizing antibody leads to transient hepadnavirus infection. J. Virol. 78:1195-1201.
66. Zoulim, F., and S. Locarnini. 2009. Hepatitis B virus resistance to nucleos-(t)ide analogues. Gastroenterology 137:1593-1608.e2.