The unstable part of the apical stem of duck hepatitis B virus epsilon shows enhanced base pair opening but not pico- to nanosecond dynamics and is essential for reverse transcriptase binding

Biochemistry

Volumn 48, Issue 44, 2009, Pages 10499-10508

  Ampt, Kirsten A M ^a   Van Der Werf, Ramon M ^a   Nelissen, Frank H T ^a   Tessari, Marco ^a   Wijmenga, Sybren S ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BASE PAIRS; BEND ANGLE; HELICAL SEGMENTS; HEPATITIS B VIRUS; IN-VITRO; PREGENOME; RELAXATION STUDIES; REPLICATION SYSTEMS; REVERSE TRANSCRIPTASES; SECONDARY STRUCTURES; STEM-LOOP; STEM-LOOP REGIONS; STRUCTURE AND DYNAMICS; TIME-SCALES;

NUCLEIC ACIDS; RNA; TIME MEASUREMENT;

DYNAMICS;

RNA; RNA DIRECTED DNA POLYMERASE;

ARTICLE; CONTROLLED STUDY; DUCK; ENZYME BINDING; HEPATITIS B VIRUS; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; VIRUS REPLICATION;

BASE PAIRING; BASE SEQUENCE; HEPATITIS B VIRUS, DUCK; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; RNA, VIRAL; RNA-DIRECTED DNA POLYMERASE; VIRUS REPLICATION;

DUCK HEPATITIS B VIRUS; HEPATITIS B VIRUS;

EID: 70449429466     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9011385     Document Type: Article

References (66)

1. Lee, W. M. (1997) Medical progress: Hepatitis B virus infection. N. Engl. J. Med. 337, 1733-1745.
2. Ganem, D., and Schneider, R. (2001) Fields Virology , Lippincott, Williams & Wilkins, Philadelphia.
3. Nassal, M. (2008) Hepatitis B viruses: Reverse transciption a different way. Virus Res. 134, 235-249.
4. Nassal, M. (2000) DNA Virus Replication , Vol.26, Oxford University Press, Oxford, U.K.
5. Beck, J., and Nassal, M. (2007) Hepatitis B virus replication. World J. Gastroenterol. 13, 48-64.
6. Beck, J., Bartos, H., and Nassal, M. (1997) Experimental confirmation of a hepatitis B virus (HBV) ε-like bulge-and-loop structure in avian HBV RNA encapsidation signals. Virology 227, 500-504. (Pubitemid 27241044)
7. Beck, J., and 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. Hu, J. M., and Anselmo, D. (2000) In vitro reconstitution of a functional duck hepatitis B virus reverse transcriptase: Posttranslational activation by Hsp90. J. Virol. 74, 11447-11455.
9. Hu, K. H., Beck, J., and Nassal, M. (2004) SELEX-derived aptamers of the duck hepatitis B virus RNA encapsidation signal distinguish critical and non-critical residues for productive initiation of reverse transcription. Nucleic Acids Res. 32, 4377-4389. (Pubitemid 39232310)
10. Lin, L., Wan, F., and Hu, J. M. (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. (Pubitemid 351822246)
11. Hu, J. M., Flores, D., Toft, D., Wang, X. T., and Nguyen, D. (2004) Requirement of heat shock protein 90 for human hepatitis B virus reverse transcriptase function. J. Virol. 78, 13122-13131. (Pubitemid 39507819)
12. Hu, J. M., and Boyer, M. (2006) Hepatitis B virus reverse transcriptase and ε RNA sequences required for specific interaction in vitro. J. Virol. 80, 2141-2150.
13. Beck, J., and 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.
14. Flodell, S., Schleucher, J., Cromsigt, J., Ippel, H., Kidd-Ljunggren, K., and Wijmenga, S. (2002) The apical stem-loop of the hepatitis B virus encapsidation signal folds into a stable tri-loop with two underlying pyrimidine bulges. Nucleic Acids Res. 30, 4803-4811. (Pubitemid 35331761)
15. Flodell, S., Petersen, M., Girard, F., Zdunek, J., Kidd-Ljunggren, K., Schleucher, J., and Wijmenga, S. (2006) Solution structure of the apical stem-loop of the human hepatitis B virus encapsidation signal. Nucleic Acids Res. 34, 4449-4457. (Pubitemid 44567044)
16. Petzold, K., Duchardt, E., Flodell, S., Larsson, G., Kidd-Ljunggren, K., Wijmenga, S., and Schleucher, J. (2007) Conserved nucleotides in an RNA essential for hepatitis B virus replication show distinct mobility patterns. Nucleic Acids Res. 35, 6854-6861. (Pubitemid 350201805)
17. Girard, F. C., Ottink, O. M., Ampt, K. A. M., Tessari, M., and Wijmenga, S. S. (2007) Thermodynamics and NMR studies on Duck, Heron and Human HBV encapsidation signals. Nucleic Acids Res. 35, 2800-2811.
18. Haasnoot, P. C. J., Brederode, F. T., Olsthoorn, R. C. L., and Bol, J. F. (2000) A conserved hairpin structure in Alfamovirus and Bromovirus subgenomic promoters is required for efficient RNA synthesis in vitro. RNA 6, 708-716.
19. Al-Hashimi, H. M. (2005) Dynamics-based amplification of RNA function and its characterization by using NMR spectroscopy. ChemBioChem 6, 1506-1519.
20. Latham, M. R., Brown, D. J., McCallum, S. A., and Pardi, A. (2005) NMR methods for studying the structure and dynamics of RNA. ChemBioChem 6, 1492-1505. (Pubitemid 41296958)
21. Hall,K.B. (2008)RNAinmotion.Curr.Opin. Chem.Biol. 12, 612-618.
22. Shajani, Z., and Varani, G. (2007)NMRstudies of dynamics in RNA and DNA by C-13 relaxation. Biopolymers 86, 348-359. (Pubitemid 47237804)
23. Al-Hashimi, H. M. (2007) Beyond static structures of RNA by NMR: Folding, refolding, and dynamics at atomic resolution. Biopolymers 86, 345-347.
24. Getz, M., Sun, X. Y., Casiano-Negroni, A., Zhang, Q., and Al-Hashimi, H. M. (2007) NMR studies of RNA dynamics and structural plasticity using NMR residual dipolar couplings. Biopolymers 86, 384-402. (Pubitemid 47237806)
25. Lee, J. H., and Pardi, A. (2007) Thermodynamics and kinetics for base-pair opening in the P1 duplex of the Tetrahymena group I ribozyme. Nucleic Acids Res. 35, 2965-2974.
26. Hoogstraten, C. G., Wank, J. R., and Pardi, A. (2000) Active site dynamics in the lead-dependent ribozyme. Biochemistry 39, 9951-9958.
27. Legault, P., Hoogstraten, C. G., Metlitzky, E., and Pardi, A. (1998) Order, dynamics and metal-binding in the lead-dependent ribozyme. J. Mol. Biol. 284, 325-335.
28. Addess, K. J., Basilion, J. P., Klausner, R. D., Rouault, T. A., and Pardi, A. (1997) Structure and dynamics of the iron responsive element RNA: Implications for binding of the RNA by iron regulatory binding proteins. J. Mol. Biol. 274, 72-83.
29. Showalter, S. A., Baker, N. A., Tang, C. G., and Hall, K. (2005) Iron responsive element RNA flexibility described by NMR and isotropic reorientational eigenmode dynamics. J. Biomol. NMR 32, 179-193. (Pubitemid 41258799)
30. Vermeulen, A., McCallum, S. A., and Pardi, A. (2005) Comparison of the global structure and dynamics of native and unmodified tRNA. Biochemistry 44, 6024-6033. (Pubitemid 40570696)
31. Shajani, Z., and Varani, G. (2005) C-13 NMR relaxation studies of RNAbase and ribose nuclei reveal a complex pattern of motions in the RNA binding site for human U1A protein. J. Mol. Biol. 349, 699-715.
32. Shajani, Z., Drobny, G., and Varani, G. (2007) Binding of U1A protein changes RNA dynamics as observed by C-13 NMR relaxation studies. Biochemistry 46, 5875-5883.
33. Oberstrass, F. C., Allain, F. H. T., and Ravindranathan, S. (2008) Changes in dynamics of SRE-RNA on binding to the VTS1p-SAM domain studied by C-13 NMR relaxation. J. Am. Chem. Soc. 130, 12007-12020.
34. Eldho, N. V., and Dayie, K. T. (2007) Internal bulge and tetraloop of the catalytic domain 5 of a group II intron ribozyme are flexible: Implications for catalysis. J. Mol. Biol. 365, 930-944.
35. Blad, H., Reiter, N. J., Abildgaard, F., Markley, J. L., and Butcher, S. E. (2005) Dynamics and metal ion binding in the U6 RNA intramolecular stem-loop as analyzed by NMR. J. Mol. Biol. 353, 540-555.
36. Duchardt, E., and Schwalbe, H. (2005) Residue specific ribose and nucleobase dynamics of the cUUCGg RNA tetraloop motif by NMR C-13 relaxation. J. Biomol. NMR 32, 295-308. (Pubitemid 41511511)
37. Ferner, J., Villa, A., Duchardt, E., Widjajakusuma, E., Wohnert, J., Stock, G., and Schwalbe, H. (2008) NMR and MD studies of the temperature-dependent dynamics of RNA YNMG-tetraloops. Nucleic Acids Res. 36, 1928-1940.
38. Zhang, Q., Sun, X. Y., Watt, E. D., and Al-Hashimi, H. M. (2006) Resolving the motional modes that code for RNA adaptation. Science 311, 653-656. (Pubitemid 43191308)
39. Zhang, Q., Stelzer, A. C., Fisher, C. K., and Al-Hashimi, H. M. (2007) Visualizing spatially correlated dynamics that directs RNA conformational transitions. Nature 450, 1263-1267.
40. Chowdhury, S., Maris, C., Allain, F. H. T., and Narberhaus, F. (2006) Molecular basis for temperature sensing by an RNA thermometer. EMBO J. 25, 2487-2497. (Pubitemid 44012231)
41. Williamson, J. R. (2000) Induced fit in RNA-protein recognition. Nat. Struct. Biol. 7, 834-837.
42. Leulliot, N., and Varani, G. (2001) Current topics in RNA-protein recognition: Control of specificity and biological function through induced fit and conformational capture. Biochemistry 40, 7947-7956. (Pubitemid 32641191)
43. Hansen, M. R., Mueller, L., and Pardi, A. (1998) Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nat. Struct. Biol. 5, 1065-1074.
44. 15NNMR assignments of Duck HBV apical stem loop of the epsilon encapsidation signal. Biomol. NMR Assignments 2, 159-162.
45. Cromsigt, J., van Buuren, B., Schleucher, J., and Wijmenga, S. (2001) Resonance assignment and structure determination for RNA. Methods Enzymol. 338, 371-399. (Pubitemid 32666588)
46. Wijmenga, S. S., and van Buuren, B. N. M. (1998) The use of NMR methods for conformational studies of nucleic acids. Prog. Nucl. Magn. Reson. Spectrosc. 32, 287-387.
47. 3H fold. Nucleic Acids Res. 32, 3228-3239.
48. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) Nmrpipe: A Multidimensional Spectral Processing System Based on Unix Pipes. J. Biomol. NMR 6, 277-293.
49. Kneller, D. G., and Kuntz, I. D. (1993) Ucsf Sparky: An Nmr Display, Annotation and Assignment Tool. J. Cell. Biochem. 254-254
50. Schleucher, J., Schwendinger, M., Sattler, M., Schmidt, P., Schedletzky, O., Glaser, S. J., Sorensen, O. W., and Griesinger, C. (1994) A General Enhancement Scheme in Heteronuclear Multidimensional NMR Employing Pulsed-Field Gradients. J. Biomol. NMR 4, 301-306.
51. Yamazaki, T., Muhandiram, R., and Kay, L. E. (1994) NMR Experiments for the Measurement of Carbon Relaxation Properties in Highly Enriched, Uniformly C-13,N-15-Labeled Proteins: Application to C-13(Alpha) Carbons. J. Am. Chem. Soc. 116, 8266-8278.
52. Korzhnev, D. M., Skrynnikov, N. R., Millet, O., Torchia, D. A., and Kay, L. E. (2002) An NMR experiment for the accurate measurement of heteronuclear spin-lock relaxation rates. J. Am. Chem. Soc. 124, 10743-10753.
53. Korzhnev, D. M., Billeter, M., Arseniev, A. S., and Orekhov, V. Y. (2001) NMR studies of Brownian tumbling and internal motions in proteins. Prog. Nucl. Magn. Reson. Spectrosc. 38, 197-266.
54. Hansen, A. L., and Al-Hashimi, H. M. (2007) Dynamics of large elongated RNA by NMR carbon relaxation. J. Am. Chem. Soc. 129, 16072-16082.
55. Loria, J. P., Rance, M., and Palmer, A. G. (1999) A relaxation- compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J. Am. Chem. Soc. 121, 2331-2332.
56. Mulder, F. A., Mittermaier, A., Hon, B., Dahlquist, F. W., and Kay, L. E. (2001) Studying excited states of proteins by NMR spectroscopy. Nat. Struct. Biol. 8, 932-935.
57. Wu, B., Petersen, M., Girard, F., Tessari, M., and Wijmenga, S. S. (2006) Prediction of molecular alignment of nucleic acids in aligned media. J. Biomol. NMR 35, 103-115. (Pubitemid 43986213)
58. Lu, X. J., and Olson,W.K. (2003) 3DNA: A software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res. 31, 5108-5121.
59. Stueber, D., and Grant, D. M. (2002) C-13 and N-15 chemical shift tensors in adenosine, guanosine dihydrate, 2′-deoxythymidine, and cytidine. J. Am. Chem. Soc. 124, 10539-10551.
60. de la Torre, J. G., Huertas, M. L., and Carrasco, B. (2000) HYDRONMR: Prediction of NMRrelaxation of globular proteins from atomic-level structures and hydrodynamic calculations. J. Magn. Reson. 147, 138-146.
61. Mandel, A. M., Akke, M., and Palmer, A. G. (1995) Backbone Dynamics of Escherichia coli Ribonuclease Hi: Correlations with Structure and Function in an Active Enzyme. J. Mol. Biol. 246, 144-163.
62. Cromsigt, J. A. M. T. C., Hilbers, C. W., and Wijmenga, S. S. (2001) Prediction of proton chemical shifts in RNA: Their use in structure refinement and validation. J. Biomol. NMR 21, 11-29.
63. Nelissen, F. H. T., van Gammeren, A. J., Tessari, M., Girard, F. C., Heus, H. A., and Wijmenga, S. S. (2008) Multiple segmental and selective isotope labeling of large RNA for NMR structural studies. Nucleic Acids Res. 36, e89.
64. O'Neil-Cabello, E., Bryce, D. L., Nikonowicz, E. P., and Bax, A. (2004) Measurement of five dipolar couplings from a single 3D NMR multiplet applied to the study of RNA dynamics. J. Am. Chem. Soc. 126, 66-67.
65. Shajani, Z., and Varani, G. (2008) C-13 relaxation studies of the DNA target sequence for HhaI methyltransferase reveal unique motional properties. Biochemistry 47, 7617-7625. (Pubitemid 352019493)
66. Duchardt, E., Nilsson, L., and Schleucher, J. (2008) Cytosine ribose flexibility in DNA: A combined NMR C-13 spin relaxation and molecular dynamics simulation study. Nucleic Acids Res. 36, 4211-4219. (Pubitemid 351984836)