A GCUA tetranucleotide loop found in the poliovirus oriL by in vivo SELEX (un)expectedly forms a YNMG-like structure: Extending the YNMG family with GYYA

RNA

Volumn 12, Issue 9, 2006, Pages 1671-1682

  Melchers, Willem J G ^a   Zoll, Jan ^a   Tessari, Marco ^a   Bakhmutov, Denis V ^b   Gmyl, Anatoly P ^b   Agol, Vadim I ^b,c   Heus, Hans A ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b CHUMAKOV INSTITUTE OF POLIOMYELITIS AND VIRAL ENCEPHALITIDES   (Russian Federation)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

In vivo SELEX; NMR; Poliovirus; RNA structure; RNA tetraloop; RNA protein recognition

Indexed keywords

PROTEINASE; RNA; VIRUS RNA;

AMINO ACID SEQUENCE; ARTICLE; CATALYST; CONTROLLED STUDY; CRYSTALLIZATION; DATA BASE; IN VIVO STUDY; MUTANT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; PROTEIN INTERACTION; RIBOSOME SUBUNIT; RNA REPLICATION; RNA STRUCTURE; THERMODYNAMICS; VIRUS REPLICATION;

BASE PAIRING; BASE SEQUENCE; HEAT; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; PHYLOGENY; POLIOVIRUS; RNA, VIRAL; SELEX APTAMER TECHNIQUE; SEQUENCE ANALYSIS, RNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

ENTEROVIRUS; HALOARCULA MARISMORTUI; POLIOVIRUS;

EID: 33748175067     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.113106     Document Type: Article

References (64)

1. Ackerman, E.J., Saxena, S.K., and Ulbrich, N. 1988. α-Sarcin causes a specific cut in 28S rRNA when microinjected into Xenopus oocytes. J. Biol. Chem. 263: 17076-17083.
2. Allain, F.H. and Varani, G. 1995. Structure of the P1 helix from group I self-splicing introns. J. Mol. Biol. 250: 333-353.
3. Andino, R., Rieckhof, G.E., Trono, D., and Baltimore, D. 1990. Substitutions in the protease (3Cpro) gene of poliovirus can suppress a mutation in the 5′ noncoding region. J. Virol. 64: 607-612.
4. 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.
5. Antao, V.P. and Tinoco Jr., I. 1991. Thermodynamic parameters for loop formation in RNA and DNA hairpin tetraloops. Nucleic Acids Res. 21: 5901-5905.
6. Antao, V.P., Lai, S.Y., and Tinoco Jr., I. 1991. Thermodynamic parameters for loop formation in RNA and DNA hairpin tetraloops. Nucleic Acids Res. 20: 819-824.
7. 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.
8. Batey, R.T., Sagar, M.B., and Doudna, J.A. 2001. Structural and energetic analysis of RNA recognition by a universally conserved protein from the signal recognition particle. J. Mol. Biol. 307: 229-246.
9. Bax, A., Kontaxis, G., and Tjandra, N. 2001. Dipolar couplings in macromolecular structure determination. Methods Enzymol. 339: 127-174.
10. Cai, Z., Gorin, A., Frederick, R., Ye, X., Hu, W., Majumdar, A., Kettani, A., and Patel, D.J. 1998. Solution structure of P22 transcriptional antitermination N peptide-boxB RNA complex. Nat. Struct. Biol. 5: 203-212.
11. Cannone, J.J., Subramanian, S., Schnare, M.N., Collett, J.R., D'Souza, L.M., Du, Y., Feng, B., Lin, N., Madabusi, L.V., Muller, K.M., et al. 2002. The comparative RNA Web (CRW) site: An online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3: 2.
12. 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.
13. Cheong, C., Varani, G., and Tinoco Jr., I. 1990. Solution structure of an unusually stable RNA hairpin, 5′GGAC(UUCG)GUCC. Nature 346: 680-682.
14. 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.
15. Dickerson, R.E. 1998. DNA bending: The prevalence of kinkiness and the virtues of normality. Nucleic Acids Res. 26: 1906-1926.
16. Dickerson, R.E. and Chiu, T.K. 1997. Helix bending as a factor in protein/DNA recognition. Biopolymers 44: 361-403.
17. Du, Z., Yu, J., Andino, R., and James, T.L. 2003. Extending the family of UNCG-like tetraloop motifs: NMR structure of a CACG tetraloop from coxsackievirus B3. Biochemistry 42: 4373-4383.
18. 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.
19. Ennifar, E., Nikulin, A., Tishchenko, S., Serganov, A., Nevskaya, N., Garber, M., Ehresmann, B., Ehresmann, C., Nikonov, S., and Dumas, P. 2000. The crystal structure of UUCG tetraloop. J. Mol. Biol. 304: 35-42.
20. Gamarnik, A.V. and Andino, R. 1997. Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA 3: 882-892.
21. _. 1998. Switch from translation to RNA replication in a positive-stranded RNA virus. Genes & Dev. 12: 2293-2304.
22. Gralla, J., and Crothers, D.M. 1973. Free energy of imperfect nucleic acid helices. III. Small internal loops resulting from mismatches. J. Mol Biol. 78: 301-319.
23. 1H spin system identification in macromolecules. J. Am. Chem. Soc. 110: 7870-7872.
24. Gutell, R.R., Weiser, B., Woese, C.R., and Noller, H.F. 1985. Comparative anatomy of 16-S-like ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol. 32: 155-216.
25. 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.
26. Harms, J., Schluenzen, 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.
27. Heus, H.A. and Hilbers, C.W. 2003. Structures of non-canonical tandem base pairs in RNA helices: Review. Nucleosides Nucleotides Nucleic Acids 22: 559-571.
28. Heus, H.A. and Pardi, A. 1991. Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops. Science 253: 191-194.
29. Hilbers, C.W., Heus, H.A., van Dongen, M.J.P., and Wijmenga, S.S. 1994. The hairpin elements of nucleic acid structure: DNA and RNA folding. In Nucleic acids and molecular biology (eds. F. Eckstein and D.M.J. Lilley), Vol. 8. pp. 56-104. Springer Verlag, Berlin.
30. Ihle, Y., Ohlenschlager, O., Hafner, S., Duchardt, E., Zacharias, M., Seitz, S., Zell, R., Ramachandran, R., and Gorlach, M. 2005. A novel cGUUAg tetraloop structure with a conserved yYNMGg-type backbone conformation from cloverleaf 1 of bovine enterovirus 1 RNA. Nucleic Acids Res. 33: 2003-2011.
31. Jeener, J., Meier, B.H., Bachmann, P., and Ernst, R.R. 1970. Investigation of exchange processes by two dimensional NMR spectroscopy. J. Chem. Phys. 71: 4546-4553.
32. 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. 264: 968-980.
33. Klein, D.J., Moore, P.B., and Steitz, T.A. 2004. The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J. Mol. Biol. 340: 141-177.
34. Koradi, R., Billeter, M., and Wüthrich, K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14: 51-55.
35. Legault, P., Li, J., Mogridge, J., Kay, L.E., and Greenblatt, J. 1998. NMR structure of the bacteriophage λ N peptide/boxB RNA complex: Recognition of a GNRA fold by an arginine-rich motif. Cell 93: 289-299.
36. Leontis, N.B., Stombaugh, J., and Westhof, E. 2002. The non-Watson-Crick base pairs and their associated isostericity matrices. Nucleic Acids Res. 30: 3497-3531.
37. 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-2-fold symmetry in RNA helices containing two adjacent non-canonical base-pairs. J. Mol. Biol. 331: 759-769.
38. 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.
39. Lyons, T., Murray, K.E., Roberts, A.W., and Barton, D.J. 2001. Poliovirus 5′-terminal cloverleaf RNA is required in cis for VPg uridylylation and the initiation of negative-strand RNA synthesis. J. Virol. 75: 10696-10708.
40. Michel, F. and Westhof, E. 1990. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J. Mol. Biol. 216: 585-610.
41. Mosimann, S.C., Cherney, M.M., Sia, S., Plotch, S., and James, M.N. 1997. Refined X-ray crystallographic structure of the poliovirus 3C gene product. J. Mol. Biol. 273: 1032-1047.
42. Murphy, F.L. and Cech, T.R. 1994. GAAA tetraloop and conserved bulge stabilize tertiary structure of a group I intron domain. J. Mol. Biol. 236: 49-63.
43. Nissen, P., Ippolito, J.A., Ban, N., Moore, P.B., and Steitz, T.A. 2001. RNA tertiary interactions in the large ribosomal subunit: The A-minor motif. Proc. Natl. Acad. Sci. 98: 4899-4903.
44. Ohlenschlager, O., Wohnert, J., Bucci, E., Seitz, S., Hafner, S., Ramachandran, R., Zell, R., and Gorlach, M. 2004. The structure of the stemloop D subdomain of coxsackievirus B3 cloverleaf RNA and its interaction with the proteinase 3C. Structure 12: 237-248.
45. 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.
46. Pace, N.R., Smith, D.K., Olsen, G.J., and James, B.D. 1989. Phylogenetic comparative analysis and the secondary structure of ribonuclease P RNA - A review. Gene 82: 65-75.
47. Parsley, T.B., Towner, J.S., Blyn, L.B., Ehrenfeld, E., and Semler, B.L. 1997. Poly (rC) binding protein 2 forms a ternary complex with the 5′-terminal sequences of poliovirus RNA and the viral 3CD proteinase. RNA 3: 1124-1134.
48. Plateau, P. and Guéron, M. 1982. Exchangeable proton NMR without baseline distortion, using new strong-pulse sequences. J. Am. Chem. Soc. 104: 7310-7311.
49. Poritz, M.A., Strub, K., and Walter, P. 1988. Human SRP RNA and E. coli 4.5S RNA contain a highly homologous structural domain. Cell 55: 4-6.
50. Proctor, D.J., Schaak, J.E., Bevilacqua, J.M., Falzone, C.J., and Bevilacqua, P.C. 2002. Isolation and characterization of a family of stable RNA tetraloops with the motif YNMG that participate in tertiary interactions. Biochemistry 41: 12062-12075.
51. Schluenzen, F., Tocilj, A., Zarivach, R., Harms, J., Gluehmann, M., Janell, D., Bashan, A., Bartels, H., Agmon, I., Franceschi, F., et al. 2000. Structure of functionally activated small ribosomal subunit at 3.3 A° resolution. Cell 102: 615-623.
52. 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.
53. Semler, B.L. and Wimmer, E., eds. 2002. Molecular biology of picornaviruses. ASM Press, Washington, DC.
54. Serra, M.J. and Turner, D.H. 1995. Predicting thermodynamic properties of RNA. Methods Enzymol. 259: 242-261.
55. Shaka, A.J. and Freeman, R. 1983. Simplification of NMR spectra by filtration through multiple quantum coherence. J. Magn. Reson. 51: 169-173.
56. 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.
57. Su, L., Chen, L., Egli, M., Berger, J.M., and Rich, A. 1999. Minor groove RNA triplex in the crystal structure of a ribosomal frameshifting viral pseudoknot. Nat. Struct. Biol. 6: 285-292.
58. Uhlenbeck, O.C. 1990. Tetraloops and RNA folding. Nature 346: 613-614.
59. van Knippenberg, P.H. 1986. Structural and functional aspects of the N6,N6 dimethyladenosines in 16S ribosomal RNA. In Structure, function and genetics of ribosomes (eds. B. Hardesty and B. Kramer), pp. 412-424. Springer-Verlag, New York.
60. Varani, G., Cheong, C., and Tinoco Jr., I. 1991. Structure of an unusually stable RNA hairpin. Biochemistry 30: 3280-3289.
61. Walker, P.A., Leong, L.E., and Porter, A.G. 1995. Sequence and structural determinants of the interaction between the 5′-noncoding region of picornavirus RNA and rhinovirus protease 3C. J. Biol. Chem. 270: 14510-14516.
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. Woese, C.R., Winker, S., and Gutell, R.R. 1990. Architecture of ribosomal RNA: Constraints on the sequence of "tetra-loops." Proc. Natl. Acad. Sci. 87: 8467-8471.
64. Zell, R., Sidigi, K., Bucci, E., Stelzner, A., and Gorlach, M. 2002. Determinants of the recognition of enteroviral cloverleaf RNA by coxsackievirus B3 proteinase 3C. RNA 8: 188-201.