A Tyr residue in the reverse transcriptase domain can mimic the protein-priming tyr residue in the terminal protein domain of a hepadnavirus P protein

Journal of Virology

Volumn 85, Issue 15, 2011, Pages 7742-7753

  Beck, Jürgen ^a   Nassal, Michael ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DNA POLYMERASE; MALTOSE BINDING PROTEIN; MINIP PROTEIN; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE; TRANSFER RNA; TYROSINE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; DUCK HEPATITIS B VIRUS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HEPADNAVIRUS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; REVERSE TRANSCRIPTION; RNA BINDING; VIRUS GENOME; VIRUS REPLICATION;

HEPADNAVIRIDAE; MODELS, MOLECULAR; RECOMBINANT PROTEINS; RNA, VIRAL; RNA-DIRECTED DNA POLYMERASE; SUBSTRATE SPECIFICITY; VIRAL PROTEINS; VIRUS REPLICATION;

DUCK HEPATITIS B VIRUS; HEPADNAVIRIDAE; TOBACCO ETCH VIRUS;

EID: 79960400918     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00482-11     Document Type: Article

References (63)

1. Badtke, M. P., I. Khan, F. Cao, J. Hu, and J. E. Tavis. 2009. An interdomain RNA binding site on the hepadnaviral polymerase that is essential for reverse transcription. Virology 390:130-138.
2. Bartenschlager, R., and H. Schaller. 1992. Hepadnaviral assembly is initiated by polymerase binding to the encapsidation signal in the viral RNA genome. EMBO J. 11:3413-3420.
3. Bartholomeusz, A., B. G. Tehan, and D. K. Chalmers. 2004. Comparisons of the HBV and HIV polymerase, and antiviral resistance mutations. Antivir. Ther. 9:149-160.
4. Beck, J., and M. Nassal. 1996. A sensitive procedure for mapping the boundaries of RNA elements binding in vitro translated proteins defines a minimal hepatitis B virus encapsidation signal. Nucleic Acids Res. 24:4364-4366.
5. Beck, J., and M. Nassal. 1995. Efficient hammerhead ribozyme-mediated cleavage of the structured hepatitis B virus encapsidation signal in vitro and in cell extracts, but not in intact cells. Nucleic Acids Res. 23:4954-4962.
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. 2001. Reconstitution of a functional duck hepatitis B virus replication initiation complex from separate reverse transcriptase domains expressed in Escherichia coli. J. Virol. 75:7410-7419.
10. Beck, J., M. Vogel, and M. Nassal. 2002. dNTP versus NTP discrimination by phenylalanine 451 in duck hepatitis B virus P protein indicates a common structure of the dNTP-binding pocket with other reverse transcriptases. Nucleic Acids Res. 30:1679-1687
11. Boregowda, R. K., L. Lin, Q. Zhu, F. Tian, and J. Hu. 2011. Cryptic protein priming sites in two different domains of duck hepatitis B virus reverse transcriptase for initiating DNA synthesis in vitro. J. Virol. 85:7754-7765.
12. Burgess, R. R. 2009. Refolding solubilized inclusion body proteins. Methods Enzymol. 463:259-282.
13. Cao, F., et al. 2005. Identification of an essential molecular contact point on the duck hepatitis B virus reverse transcriptase. J. Virol. 79:10164-10170.
14. Cooper, J. A., and T. Hunter. 1981. Changes in protein phosphorylation in Rous sarcoma virus-transformed chicken embryo cells. Mol. Cell. Biol. 1:165-178.
15. Crimmins, D. L., S. M. Mische, and N. D. Denslow. 2005. Chemical cleavage of proteins in solution. Curr. Protoc. Protein Sci. Chapter11:Unit 11-4.
16. Das, K., et al. 2001. Molecular modeling and biochemical characterization reveal the mechanism of hepatitis B virus polymerase resistance to lamivudine (3TC) and emtricitabine (FTC). J. Virol. 75:4771-4779.
17. Ferrer-Orta, C., R. Agudo, E. Domingo, and N. Verdaguer. 2009. Structural insights into replication initiation and elongation processes by the FMDV RNA-dependent RNA polymerase. Curr. Opin. Struct. Biol. 19:752-758.
18. Galligan, J. T., S. E. Marchetti, and J. C. Kennell. 2011. Reverse transcription of the pFOXC mitochondrial retroplasmids of Fusarium oxysporum is protein primed. Mob DNA 2:1.
19. 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.
20. Harris, D., P. N. Yadav, and V. N. Pandey. 1998. Loss of polymerase activity due to Tyr-to-Phe substitution in the YMDD motif of human immunodeficiency virus type-1 reverse transcriptase is compensated by Met-to-Val substitution within the same motif. Biochemistry 37:9630-9640.
21. 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.
22. 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.
23. 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.
24. Kamtekar, S., et al. 2006. The phi29 DNA polymerase:protein-primer structure suggests a model for the initiation to elongation transition. EMBO J. 25:1335-1343.
25. Lanford, R. E., L. Notvall, H. Lee, and B. Beames. 1997. Transcomplementation of nucleotide priming and reverse transcription between independently expressed TP and RT domains of the hepatitis B virus reverse transcriptase. J. Virol. 71:2996-3004.
26. Lin, L., F. Wan, and J. Hu. 2008. Functional and structural dynamics of hepadnavirus reverse transcriptase during protein-primed initiation of reverse transcription: effects of metal ions. J. Virol. 82:5703-5714.
27. Loeb, D. D., R. C. Hirsch, and D. Ganem. 1991. Sequence-independent RNA cleavages generate the primers for plus-strand DNA synthesis in hepatitis B viruses: implications for other reverse transcribing elements. EMBO J. 10: 3533-3540.
28. Nassal, M. 2008. Hepatitis B viruses: reverse transcription a different way. Virus Res. 134:235-249.
29. Nassal, M. 2009. New insights into HBV replication: new opportunities for improved therapies. Fut. Virol. 4:55-70.
30. 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.
31. Paul, A. V., et al. 2003. Biochemical and genetic studies of the VPg uridylylation reaction catalyzed by the RNA polymerase of poliovirus. J. Virol. 77:891-904.
32. 2+ in the activity of phi6 RNA-dependent RNA polymerase. Nucleic Acids Res. 36:6633-6644.
33. Protzer, U., M. Nassal, P. W. Chiang, M. Kirschfink, and H. Schaller. 1999. Interferon gene transfer by a hepatitis B virus vector efficiently suppresses wild-type virus infection. Proc. Natl. Acad. Sci. U. S. A. 96:10818-10823.
34. Rantalainen, K. I., K. Eskelin, P. Tompa, and K. Makinen. 2011. Structural flexibility allows the functional diversity of potyvirus genome-linked protein VPg. J. Virol. 85:2449-2457.
35. Receveur-Brechot, V., J. M. Bourhis, V. N. Uversky, B. Canard, and S. Longhi. 2006. Assessing protein disorder and induced folding. Proteins 62: 24-45.
36. Richards, O. C., et al. 2006. Intramolecular and intermolecular uridylylation by poliovirus RNA-dependent RNA polymerase. J. Virol. 80:7405-7415.
37. Salas, M. 1991. Protein-priming of DNA replication. Annu. Rev. Biochem. 60:39-71.
38. Sarafianos, S. G., et al. 2009. Structure and function of HIV-1 reverse transcriptase: molecular mechanisms of polymerization and inhibition. J. Mol. Biol. 385:693-713.
39. Schmidt, A., S. Endres, and S. Rothenfusser. 2011. Pattern recognition of viral nucleic acids by RIG-I-like helicases. J. Mol. Med. 89:5-12.
40. 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.
41. 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.
42. 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.
43. Steitz, T. A. 1999. DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem. 274:17395-17398.
44. Steitz, T. A. 2006. Visualizing polynucleotide polymerase machines at work. EMBO J. 25:3458-3468.
45. Takeuchi, O., and S. Akira. 2009. Innate immunity to virus infection. Immunol. Rev. 227:75-86.
46. 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.
47. Tavis, J. E., B. Massey, and Y. Gong. 1998. The duck hepatitis B virus polymerase is activated by its RNA packaging signal, epsilon. J. Virol. 72: 5789-5796.
48. Tavis, J. E., S. Perri, and D. Ganem. 1994. Hepadnavirus reverse transcrip-tion initiates within the stem-loop of the RNA packaging signal and employs a novel strand transfer. J. Virol. 68:3536-3543.
49. van Dijk, A. A., E. V. Makeyev, and D. H. Bamford. 2004. Initiation of viral RNA-dependent RNA polymerization. J. Gen. Virol. 85:1077-1093.
50. 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.
51. Walker, A., C. Skamel, J. Vorreiter, and M. Nassal. 2008. Internal core protein cleavage leaves the hepatitis B virus capsid intact and enhances its capacity for surface display of heterologous whole chain proteins. J. Biol. Chem. 283:33508-33515.
52. Wang, G. H., and C. Seeger. 1993. Novel mechanism for reverse transcription in hepatitis B viruses. J. Virol. 67:6507-6512.
53. 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.
54. Wang, G. H., F. Zoulim, E. H. Leber, J. Kitson, and C. Seeger. 1994. Role of RNA in enzymatic activity of the reverse transcriptase of hepatitis B viruses. J. Virol. 68:8437-8442.
55. Wang, X., X. Qian, H. C. Guo, and J. Hu. 2003. Heat shock protein 90-independent activation of truncated hepadnavirus reverse transcriptase. J. Virol. 77:4471-4480.
56. Weber, M., et al. 1994. Hepadnavirus P protein utilizes a tyrosine residue in the TP domain to prime reverse transcription. J. Virol. 68:2994-2999.
57. Wimmer, E., and A. V. Paul. 2010. The making of a picornavirus genome, p. 33-55. In E. Ehrenfeld, E. Domingo, and R. Roos (ed.), The picornaviruses. ASM Press, Washington, DC.
58. Wright, P. E., and H. J. Dyson. 2009. Linking folding and binding. Curr. Opin. Struct. Biol. 19:31-38.
59. Wu, S., and Y. Zhang. 2007. LOMETS: a local meta-threading-server for protein structure prediction. Nucleic Acids Res. 35:3375-3382.
60. Yao, E., and J. E. Tavis. 2003. Kinetics of synthesis and turnover of the duck hepatitis B virus reverse transcriptase. J. Biol. Chem. 278:1201-1205.
61. Zhang, Z., and J. E. Tavis. 2006. The duck hepatitis B virus reverse transcriptase functions as a full-length monomer. J. Biol. Chem. 281:35794-35801.
62. Zoulim, F., and S. Locarnini. 2009. Hepatitis B virus resistance to nucleos-(t)ide analogues. Gastroenterology 137(e1-2):1593-1608.
63. Zoulim, F., and C. Seeger. 1994. Reverse transcription in hepatitis B viruses is primed by a tyrosine residue of the polymerase. J. Virol. 68:6-13.