TP-RT domain interactions of duck hepatitis B virus reverse transcriptase in cis and in trans during protein-primed initiation of DNA synthesis in vitro

Journal of Virology

Volumn 86, Issue 12, 2012, Pages 6522-6536

  Boregowda, Rajeev K ^a   Adams, Christina ^a   Hu, Jianming ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA DIRECTED DNA POLYMERASE; VIRUS PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA SYNTHESIS; DNA TEMPLATE; DUCK HEPATITIS B VIRUS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME RECONSTITUTION; IN VITRO STUDY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PURIFICATION; SEQUENCE ANALYSIS;

DNA PRIMERS; DNA REPLICATION; DNA, VIRAL; HEPATITIS B VIRUS, DUCK; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA-DIRECTED DNA POLYMERASE; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

DUCK HEPATITIS B VIRUS; HEPADNAVIRIDAE;

EID: 84864023867     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00086-12     Document Type: Article

References (56)

1. Agopian A, et al. 2009. A new generation of peptide-based inhibitors targeting HIV-1 reverse transcriptase conformational flexibility. J. Biol. Chem. 284:254 -264.
2. Badtke MP, Cao F, Tavis JE. 2006. Combining genetic and biochemical approaches to identify functional molecular contact points. Biol. Proced. Online 8:77- 86.
3. Badtke MP, Khan I, Cao F, Hu J, Tavis JE. 2009. An interdomain RNA binding site on the hepadnaviral polymerase that is essential for reverse transcription. Virology 390:130 -138.
4. Bartenschlager R, Schaller H. 1988. The amino-terminal domain of the hepadnaviral P-gene encodes the terminal protein (genome-linked protein) believed to prime reverse transcription. EMBO J. 7:4185- 4192.
5. Beck J, Nassal M. 2011. 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. J. Virol. 85:7742-7753.
6. Beck J, Nassal M. 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.
7. Beck J, Nassal M. 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.
8. Boregowda RK, Lin L, Zhu Q, Tian F, Hu J. 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.
9. 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.
10. Chang LJ, Hirsch RC, Ganem D, Varmus HE. 1990. Effects of insertional and point mutations on the functions of the duck hepatitis B virus polymerase. J. Virol. 64:5553-5558.
11. Chen Y, Marion PL. 1996. Amino acids essential for RNase H activity of hepadnaviruses are also required for efficient elongation of minus-strand viral DNA. J. Virol. 70:6151- 6156.
12. Chen Y, Robinson WS, Marion PL. 1994. Selected mutations of the duck hepatitis B virus P gene RNase H domain affect both RNA packaging and priming of minus-strand DNA synthesis. J. Virol. 68:5232-5238.
13. Divita G, Restle T, Goody RS, Chermann JC, Baillon JG. 1994. Inhibition of human immunodeficiency virus type 1 reverse transcriptase dimerization using synthetic peptides derived from the connection domain. J. Biol. Chem. 269:13080 -13083.
14. Fallows DA, Goff SP. 1995. Mutations in the epsilon sequences of human hepatitis B virus affect both RNA encapsidation and reverse transcription. J. Virol. 69:3067-3073.
15. Ganem D, Prince AM. 2004. Hepatitis B virus infection-natural history and clinical consequences. N. Engl. J. Med. 350:1118 -1129.
16. Hu J. 2004. Studying DHBV polymerase by in vitro transcription and translation. Methods Mol. Med. 95:259 -269.
17. Hu J, Anselmo D. 2000. In vitro reconstitution of a functional duck hepatitis B virus reverse transcriptase: posttranslational activation by Hsp90. J. Virol. 74:11447-11455.
18. Hu J, Boyer M. 2006. Hepatitis B virus reverse transcriptase and epsilon RNAsequences required for specific interaction in vitro. J. Virol. 80:2141- 2150.
19. Hu J, Flores D, Toft D, Wang X, Nguyen D. 2004. Requirement of heat shock protein 90 for human hepatitis B virus reverse transcriptase function. J. Virol. 78:13122-13131.
20. Hu J, Lin L. 2009. RNA-protein interactions in hepadnavirus reverse transcription. Front. Biosci. 14:1606 -1618.
21. Hu J, Seeger C. 1996. Expression and characterization of hepadnavirus reverse transcriptases. Methods Enzymol. 275:195-208.
22. Hu J, Seeger C. 1996. Hsp90 is required for the activity of a hepatitis B virus reverse transcriptase. Proc. Natl. Acad. Sci. U. S. A. 93:1060 -1064.
23. Hu J, Seeger C. 1997. RNA signals that control DNA replication in hepadnaviruses. Semin. Virol. 8:205-211.
24. Hu J, Toft D, Anselmo D, Wang X. 2002. In vitro reconstitution of functional hepadnavirus reverse transcriptase with cellular chaperone proteins. J. Virol. 76:269 -279.
25. Hu J, Toft DO, Seeger C. 1997. Hepadnavirus assembly and reverse transcription require a multi-component chaperone complex which is incorporated into nucleocapsids. EMBO J. 16:59-68.
26. Itzen A, Blankenfeldt W, Goody RS. 2011. Adenylylation: renaissance of a forgotten post-translational modification. Trends Biochem. Sci. 36:221- 228.
27. Lanford RE, Kim YH, Lee H, Notvall L, Beames B. 1999. Mapping of the hepatitis B virus reverse transcriptase TP and RT domains by transcomplementation for nucleotide priming and by protein-protein interaction. J. Virol. 73:1885-1893.
28. Lanford RE, Notvall L, Beames B. 1995. Nucleotide priming and reverse transcriptase activity of hepatitis B virus polymerase expressed in insect cells. J. Virol. 69:4431- 4439.
29. Lanford RE, Notvall L, Lee H, Beames B. 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.
30. Lin L, Hu J. 2008. Inhibition of hepadnavirus reverse transcriptase-epsilon RNA interaction by porphyrin compounds. J. Virol. 82:2305- 2312.
31. Lin L, Wan F, Hu J. 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.
32. McGlynn KA, London WT. 2011. The global epidemiology of hepatocellular carcinoma: present and future. Clin. Liver Dis. 15:223-243.
33. Nassal M, Rieger A. 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.
34. Pollack JR, Ganem D. 1994. Site-specific RNA binding by a hepatitis B virus reverse transcriptase initiates two distinct reactions: RNA packaging and DNA synthesis. J. Virol. 68:5579 -5587.
35. Radziwill G, Tucker W, Schaller H. 1990. Mutational analysis of the hepatitis B virus P gene product: domain structure and RNase H activity. J. Virol. 64:613- 620.
36. Rieger A, Nassal M. 1996. Specific hepatitis B virus minus-strand DNA synthesis requires only the 5' encapsidation signal and the 3'-proximal direct repeat DR1. J. Virol. 70:585-589.
37. Seeger C, Hu J. 1997. Why are hepadnaviruses DNA and not RNA viruses? Trends Microbiol. 5:447- 450.
38. Seeger C, Leber EH, Wiens LK, Hu J. 1996. Mutagenesis of a hepatitis B virus reverse transcriptase yields temperature-sensitive virus. Virology 222:430-439.
39. Seeger C, Zoulim F, Mason WS. 2007. Hepadnaviruses, p 2977-3030. In Knipe DM, et al (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
40. Stahl M, Beck J, Nassal M. 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.
41. 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.
42. Tavis JE, Ganem D. 1996. Evidence for activation of the hepatitis B virus polymerase by binding of its RNA template. J. Virol. 70:5741-5750.
43. Tavis JE, Ganem D. 1993. Expression of functional hepatitis B virus polymerase in yeast reveals it to be the sole viral protein required for correct initiation of reverse transcription. Proc. Natl. Acad. Sci. U. S. A. 90:4107- 4111.
44. Tavis JE, Ganem D. 1995. RNA sequences controlling the initiation and transfer of duck hepatitis B virus minus-strand DNA. J. Virol. 69:4283- 4291.
45. Tavis JE, Massey B, Gong Y. 1998. The duck hepatitis B virus polymerase is activated by its RNA packaging signal, epsilon. J. Virol. 72:5789 -5796.
46. Tavis JE, Perri S, Ganem D. 1994. Hepadnavirus reverse transcription initiates within the stem-loop of the RNA packaging signal and employs a novel strand transfer. J. Virol. 68:3536 -3543.
47. Toh H, Hayashida H, Miyata T. 1983. Sequence homology between retroviral reverse transcriptase and putative polymerases of hepatitis B virus and cauliflower mosaic virus. Nature 305:827- 829.
48. Wang GH, Seeger C. 1993. Novel mechanism for reverse transcription in hepatitis B viruses. J. Virol. 67:6507- 6512.
49. Wang GH, Seeger C. 1992. The reverse transcriptase of hepatitis B virus acts as a protein primer for viral DNA synthesis. Cell 71:663- 670.
50. Wang GH, Zoulim F, Leber EH, Kitson J, Seeger C. 1994. Role of RNA in enzymatic activity of the reverse transcriptase of hepatitis B viruses. J. Virol. 68:8437- 8442.
51. Wang X, Hu J. 2002. Distinct requirement for two stages of proteinprimed initiation of reverse transcription in hepadnaviruses. J. Virol. 76: 5857-5865.
52. Wang X, Qian X, Guo HC, Hu J. 2003. Heat shock protein 90-independent activation of truncated hepadnavirus reverse transcriptase. J. Virol. 77:4471- 4480.
53. 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.
54. Zahn KE, Tchesnokov EP, Gotte M, Doublie S. 2011. Phosphonoformic acid inhibits viral replication by trapping the closed form of the DNA polymerase. J. Biol. Chem. 286:25246 -25255.
55. Zhang Z, Tavis JE. 2006. The duck hepatitis B virus reverse transcriptase functions as a full-length monomer. J. Biol. Chem. 281:35794 -35801.
56. Zoulim F, Seeger C. 1994. Reverse transcription in hepatitis B viruses is primed by a tyrosine residue of the polymerase. J. Virol. 68:6 -13.