Breaking pseudo-twofold symmetry in the poliovirus 3′-UTR Y-stem by restoring Watson-Crick base pairs

RNA

Volumn 13, Issue 5, 2007, Pages 781-792

  Zoll, J A N ^a,b   Tessari, Marco ^a   Van Kuppeveld, Frank J M ^b   Melchers, Willem J G ^b   Heus, Hans A ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

NMR; Poliovirus; RNA; RNA structure; U U C U base pair

Indexed keywords

GENOMIC RNA; PYRIMIDINE; VIRUS RNA;

3' UNTRANSLATED REGION; ARTICLE; BASE MISPAIRING; BASE PAIRING; NUCLEAR MAGNETIC RESONANCE; NUCLEIC ACID BASE SUBSTITUTION; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; RNA REPLICATION; RNA STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS; VIRUS MUTANT;

3' UNTRANSLATED REGIONS; BASE PAIRING; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; POLIOVIRUS; RNA, VIRAL; VIRUS REPLICATION;

ENTEROVIRUS; POLIOVIRUS;

EID: 34247359126     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.375607     Document Type: Article

References (64)

1. Andino, R., Rieckhof, G.E., Achacoso, P.L., and Baltimore, D. 1993. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5′-end of viral RNA. EMBO J. 12: 3587-3598.
2. Baeyens, K.J., De Bondt, H.L., and Holbrook, S.R. 1995. Structure of an RNA double helix including uracil-uracil base pairs in an internal loop. Nat. Struct. Biol. 2: 56-62.
3. Ban, N., Nissen, P., Hansen, J., Moore, P.B., and Steitz, T.A. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289: 905-920.
4. Barsukov, I.L. and Lian, L.Y. 1993. Structure determinations from NMR data I. Analysis of NMR data. In NMR of macromolecules, a practical approach (ed. G.C.K. Roberts), pp. 315-357. Oxford University Press, New York.
5. Barton, D.J. and Flanegan, J.B. 1997. Synchronous replication of poliovirus RNA: Initiation of negative-strand RNA synthesis requires the guanidine-inhibited activity of protein 2C. J. Virol. 71: 8482-8489.
6. Bax, A., Kontaxis, G., and Tjandra, N. 2001. Dipolar couplings in macromolecular structure determination. Methods Enzymol. 339: 127-174.
7. Bourdelat-Parks, B.N. and Wartell, R.M. 2005. Thermodynamics of RNA duplexes with tandem mismatches containing a uracil-uracil pair flanked by CG/GC or GC/AU closing base pairs. Biochemistry 44: 16710-16717.
8. Brown, D.M., Kauder, S.E., Cornell, C.T., Jang, G.M., Racaniello, V.R., and Semler, B.L. 2004. Cell-dependent role for the poliovirus 3′-noncoding region in positive-strand RNA synthesis. J. Virol. 78: 1344-1351.
9. Campbell, S.A., Lin, J., Dobrikova, E., and Gromeier, M. 2005. Genetic determinants of cell type-specific poliovirus propagation in HEK 293 cells. J. Virol. 79: 6281-6290.
10. Cate, J.H., Gooding, A.R., Podell, E., Zhou, K., Golden, B.L., Kundrot, C.E., Cech, T.E., and Doudna, J.A. 1996. Crystal structure of a group I ribozyme domain: Principles of RNA packing. Science 273: 1678-1685.
11. Clore, G.M., Gronenborn, A.M., and Tjandra, N. 1998. Direct structure refinement against residual dipolar couplings in the presence of rhombicity of unknown magnitude. J. Magn. Reson. 131: 159-162.
12. 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.
13. Dickerson, R.E. 1998. DNA bending: The prevalence of kinkiness and the virtues of normality. Nucleic Acids Res. 26: 1906-1926.
14. Dickerson, R.E. and Chiu, T.K. 1997. Helix bending as a factor in protein/DNA recognition. Biopolymers 44: 361-403.
15. D'Souza, V. and Summers, M.F. 2004. Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus. Nature 431: 586-590.
16. Du, Z., Yu, J., Ulyanov, N.B., Andino, R., and James, T.L. 2004. Solution structure of a consensus stem-loop D RNA domain that plays important roles in regulating translation and replication in enteroviruses and rhinoviruses. Biochemistry 43: 11959-11972.
17. Fourmy, D., Recht, M.I., Blanchard, S.C., and Puglisi, J.D. 1996. Structure of the A-site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science 274: 1367-1371.
18. Furtig, B., Richter, C., Wohnert, J., and Schwalbe, H. 2003. NMR spectroscopy of RNA. ChemBioChem 4: 936-962.
19. Griesinger, C., Otting, G., Wüthrich, K., and Ernst, R.R. 1988. Clean TOCSY for 1H spin system identification in macromolecules. J. Am. Chem. Soc. 110: 7870-7872.
20. 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.
21. Harms, J., Schluenza, F., Zarivach, R., Bashan, A., Gat, S., Agmon, I., Bartels, H., Franceschi, F., and Yonath, A. 2001. High-resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107: 679-688.
22. Harris, K.S., Xiang, W., Alexander, L., Lane, W.S., Paul, A.V., and Wimmer, E. 1994. Interaction of poliovirus polypeptide 3CDpro with the 5′- and 3′-termini of the poliovirus genome. J. Biol. Chem. 269: 27004-27014.
23. Hermann, T. and Westhof, E. 1999. Non-Watson-Crick base pairs in RNA-protein recognition. Chem. Biol. 12: R335-R343.
24. Heus, H.A. and Hilbers, C.W. 2003. Structures of noncanonical tandem base pairs in RNA helices. Nucleosides Nucleotides Nucleic Acids 22: 559-571.
25. Holbrook, S.R., Cheong, C., Tinoco Jr., I., and Kim, S.H. 1991. Crystal structure of an RNA double helix incorporating a track of non-Watson-Crick base pairs. Nature 353: 579-581.
26. Jucker, F.M., Heus, H.A., Yip, P.F., Moors, E.H., and Pardi, A. 1996. A network of heterogeneous hydrogen bonds in GNRA tetraloops. J. Mol. Biol. 164: 968-980.
27. Kierzek, R., Burkard, M.E., and Turner, D.H. 1999. Thermodynamics of single mismatches in RNA duplexes. Biochemistry 38: 14214-14223.
28. Kolk, M.H., Wijmenga, S.S., Heus, H.A., and Hilbers, C.W. 1998. On the structure determination of a 44n RNA pseudoknot: Assignment strategies and derivation of torsion angle restraints. J. Biomol. NMR 12: 423-433.
29. Koradi, R., Billeter, M., and Wüthrich, K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14: 51-55.
30. Lescrinier, E.M.H.P., Tessari, M., van Kuppeveld, F.J.M., Melchers, W.J.G., Hilbers, C.W., and Heus, H.A. 2003. Structure of the pyrimidine-rich internal loop in the poliovirus 3′-UTR: The importance of maintaining pseudo-twofold symmetry in RNA helices containing two adjacent noncanonical base pairs. J. Mol. Biol. 331: 759-769.
31. Lietzke, S.E., Barnes, C.L., Berglund, J.A., and Kundrot, C.E. 1996. The structure of an RNA dodecamer shows how tandem U-U base pairs increase the range of stable RNA structures and the diversity of recognition sites. Structure 4: 917-930.
32. Lu, X. 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.
33. Lukavsky, P.J., Kim, I., Otto, G.A., and Puglisi, J.D. 2003. Structure of HCV IRES domain II determined by NMR. Nat. Struct. Biol. 10: 1033-1038.
34. Lynch, S.R. and Puglisi, J.D. 2001. Structure of a eukaryotic decoding region A-site RNA. J. Mol. Biol. 306: 1023-1035.
35. McKay, D.B. 1996. Structure and function of the hammerhead ribozyme: An unfinished story. RNA 2: 395-403.
36. Melchers, W.J., Hoenderop, J.G., Bruins Slot, H.J., Pleij, C.W., Pilipenko, E.V., Agol, V.I., and Galama, J.M. 1997. Kissing of the two predominant hairpin loops in the coxsackie B virus 3′-untranslated region is the essential structural feature of the origin of replication required for negative-strand RNA synthesis. J. Virol. 71: 686-696.
37. Melchers, W.J., Bakkers, J.M., Bruins Slot, H.J., Galama, J.M., Agol, V.I., and Pilipenko, E.V. 2000. Cross-talk between orientation-dependent recognition determinants of a complex control RNA element, the enterovirus oriR. RNA 6: 976-987.
38. Mellits, K.H., Meredith, J.M., Rohll, J.B., Evans, D.J., and Almond, J.W. 1998. Binding of a cellular factor to the 3′-untranslated region of the RNA genomes of entero- and rhinoviruses plays a role in virus replication. J. Gen. Virol. 79: 1715-1723.
39. Merkle, I., van Ooij, M.J., van Kuppeveld, F.J.M., Glaudemans, D.H., Galama, J.M., Henke, A., Zell, R., and Melchers, W.J.G. 2002. Biological significance of a human enterovirus B-specific RNA element in the 3′-nontranslated region. J. Virol. 76: 9900-9909.
40. Milligan, J.F., Groebe, D.R., Witherell, G.W., and Uhlenbeck, O.C. 1987. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 15: 8783-8798.
41. Mooers, B.H., Logue, J.S., and Berglund, J.A. 2005. The structural basis of myotonic dystrophy from the crystal structure of CUG repeats. Proc. Natl. Acad. Sci. 102: 16626-16631.
42. Ohlenschlager, O., Wohnert, J., Bucci, E., Seitz, S., Hafner, S., Ramachandran, R., Zell, R., and Gorlach, M. 2004. The structure of the stem-loop D subdomain of coxsackievirus B3 cloverleaf RNA and its interaction with the proteinase 3C. Structure 12: 237-248.
43. Ottiger, M., Delaglio, F., and Bax, A. 1998. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131: 373-378.
44. Pilipenko, E.V., Poperechny, K.V., Maslova, S.V., Melchers, W.J.G., Bruins Slot, H.J., and Agol, V.I. 1996. Cis-element, oriR, involved in the initiation of (-) strand poliovirus RNA: A quasiglobular multidomain RNA structure maintained by tertiary ("kissing") interactions. EMBO J. 15: 5428-5438.
45. Plateau, P. and Guéron, M. 1982. Exchangeable proton NMR without baseline distortion, using new strong-pulse sequences. J. Am. Chem. Soc. 104: 7310-7311.
46. Rueckert, R. 1996. Picornaviridae and their replication. In Virology (ed. B.N. Fields), pp. 609-654. Raven Press, New York.
47. Saenger, W. 1984. Principles of nucleic acid structure. Springer,New York.
48. Schwieters, C.D., Kuszewski, J.J., Tjandra, N., and Clore, G.M. 2003. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160: 66-74.
49. Shaka, A.J. and Freeman, R. 1983. Simplification of NMR spectra by filtration through multiple quantum coherence. J. Magn. Reson. 51: 169-173.
50. Stein, E.G., Rice, L.M., and Brünger, A.T. 1997. Torsion-angle molecular dynamics as a new efficient tool for NMR structure calculation. J. Magn. Reson. 124: 154-164.
51. Tanaka, Y., Fujii, S., Hiroaki, H., Sakata, T., Tanaka, T., Uesugi, S., Tomita, K., and Kyogoku, Y. 1999. A-form RNA double helix in the single crystal structure of r(UGAGCUUCGGCUC). Nucleic Acids Res. 27: 949-955.
52. Tanaka, Y., Kojima, C., Yamazaki, T., Kodama, T.S., Yasuno, K., Miyashita, S., Ono, A., Ono, A., Kainosho, M., and Kyogoku, Y. 2000. Solution structure of an RNA duplex including a C-U base pair. Biochemistry 39: 7074-7080.
53. Theimer, C.A., Finger, L.D., Trantirek, L., and Feigon, J. 2003. Mutations linked to dyskeratosis congenita cause changes in the structural equilibrium in telomerase RNA. Proc. Natl. Acad. Sci. 100: 449-454.
54. Todd, S., Nguyen, J.H., and Semler, L. 1995. RNA-protein interactions directed by the 3′-end of human rhinovirus genomic RNA. J. Virol. 69: 3605-3614.
55. Todd, S., Towner, J.S., Brown, D.M., and Semler, B.L. 1997. Replication-competent picornaviruses with complete genomic RNA 3′-noncoding region deletions. J. Virol. 71: 8868-8874.
56. van Ooij, M.J., Glaudemans, D.H., Heus, H.A., van Kuppeveld, F.J., and Melchers, W.J. 2006. Structural and functional integrity of the coxsackievirus B3 ori/R: Spacing between coaxial RNA helices. J. Gen. Virol. 87: 689-695.
57. Vicens, Q. and Westhof, E. 2001. Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A-site. Structure 9: 647-658.
58. Vicens, Q. and Westhof, E. 2002. Crystal structure of a complex between the aminoglycoside tobramycin and an oligonucleotide containing the ribosomal decoding a site. Chem. Biol. 9: 747-755.
59. Vicens, Q. and Westhof, E. 2003. Crystal structure of geneticin bound to a bacterial 16S ribosomal RNA A-site oligonucleotide. J. Mol. Biol. 326: 1175-1188.
60. Wang, J., Bakkers, J.M., Galama, J.M., Bruins Slot, H.J., Pilipenko, E.V., Agol, V.I., and Melchers, W.J. 1999. Structural requirements of the higher order RNA kissing element in the enteroviral 3′-UTR. Nucleic Acids Res. 27: 485-490.
61. Wijmenga, S.S., Mooren, M.W., and Hilbers, C.W. 1993. NMR of nucleic acids; from spectrum to structure. In NMR of macromolecules, a practical approach (ed. G.C.K. Roberts), pp. 217-288. Oxford University Press, New York.
62. Wimberly, B.T., Brodersen, D.E., Clemons Jr., W.M., Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. 2000. Structure of the 30S ribosomal subunit. Nature 407: 327-339.
63. Xia, T., McDowell, J.A., and Turner, D.H. 1997. Thermodynamics of nonsymmetric tandem mismatches adjacent to G.C base pairs in RNA. Biochemistry 36: 12486-12497.
64. Zoll, J., Galama, J.M.D., van Kuppeveld, F.J.M., and Melchers, W.J.G. 1996. Mengovirus leader is involved in the inhibition of host cell protein synthesis. J. Virol. 70: 4948-4952.