NMR structure of the 101-nucleotide core encapsidation signal of the moloney murine leukemia virus

Journal of Molecular Biology

Volumn 337, Issue 2, 2004, Pages 427-442

  D'Souza, Victoria ^a   Dey, Anwesha ^a   Habib, Dina ^a   Summers, Michael F ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

A minor K turn; MLV; MLV, Moloney Murine Leukaemia Virus; NC, nucleocapsid; NMR; NOE, nuclear Overhauser effect; NOESY, NOE spectroscopy; RDC, residual dipolar coupling; Stem loop

Indexed keywords

ADENOSINE; ESTER DERIVATIVE; ISOTOPE; URIDINE; VIRUS RNA;

ANALYTIC METHOD; ARTICLE; BASE MISPAIRING; CONTROLLED STUDY; HYDROGEN BOND; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; RNA STRUCTURE; RNA VIRUS; SIGNAL TRANSDUCTION; VIRUS ASSEMBLY;

MOLONEY MURINE LEUKEMIA VIRUS; MURINAE; MURINE LEUKEMIA VIRUS;

EID: 1442286437     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.01.037     Document Type: Article

References (97)

1. Berkowitz R., Fisher J., Goff S.P. RNA packaging. Curr. Top. Microbiol. Immun. 214:1996;177-218.
2. Rein A. Retroviral RNA packaging: a review. Arch. Virol. 9:1994;513-522.
3. Swanstrom R., Wills J.W. Synthesis, assembly and processing of viral proteins. Coffin J.M., Hughes S.H., Varmus H.E. Retroviruses. 1997;263-334 Cold Spring Harbor Press, Plainview, NY.
4. Berkhout B. Structure and function of the human immunodeficiency virus leader RNA. Prog. Nucl. Acid Res. and Mol. Biol. vol. 54:1996;Academic Press, New York. pp. 1-34.
5. Jewel N.A., Mansky L.M. In the beginning: genome recognition, RNA encapsidation and the initiation of complex retrovirus assembly. J. Gen. Virol. 81:2000;1889-1899.
6. Mann R., Baltimore D. Varying the position of a retrovirus packaging sequence results in the encapsidation of both unspliced and spliced RNA. J. Virol. 54:1985;401-407.
7. Prats A.-C., Roy C., Wang P., Erard M., Housset V., Gabus C., et al. Cis elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J. Virol. 64:1990;774-783.
8. Alford R.L., Honda S., Lawrence C.B., Belmont J.W. RNA secondary structure analysis of the packing signal for moloney murine leukemia virus. Virology. 183:1991;611-619.
9. Fisher J., Goff S.P. Mutational analysis of stem-loops in the RNA packaging signal of the moloney murine leukemia virus. Virology. 244:1998;133-145.
10. Konings D.A.M., Nash M.A., Maizel J.V., Arlinghaus R.B. Novel GACG-hairpin pair motif in the 5′ untranslated region of type C retrovirus related to murine leukemia virus. J. Virol. 66:1992;632-640.
11. Mougel M., Tounekti N., Darlix J.-L., Paoletti J., Ehresmann B., Ehresmann C. Conformational analysis of the 5′ leader and the gag initiation site of Mo-MuLV RNA and allosteric transitions induced by dimerization. Nucl. Acids Res. 21:1993;4677-4684.
12. Mougel M., Zhang Y., Barklis E. cis-Active structural motifs involved in specific encapsidation of moloney murine leukemia virus RNA. J. Virol. 70:1996;5043-5050.
13. Mougel M., Barklis E. A role for two hairpin structures as a core RNA encapsidation signal in murine leukemia virus virions. J. Virol. 71:1997;8061-8065.
14. Tounekti N., Mougel M., Roy C., Marquet R., Darlix J.-L., Paoletti J., et al. Effect of dimerization on the conformation of the encapsidation psi domain of moloney murine leukemia virus RNA. J. Mol. Biol. 223:1992;205-220.
15. Yang S., Temin H.M. A double hairpin structure is necessary for the efficient encapsidation of spleen necrosis virus retroviral RNA. EMBO J. 13:1994;713-726.
16. Roy C., Tounekti N., Mougel M., Darlix J.-L., Paoletti C., Ehresmann C., et al. An analytical study of the dimerization of in vitro generated RNA of moloney murine leukemia virus MoMuLV. Nucl. Acids Res. 18:1990;7287-7292.
17. Girard P.-M., Bonnet-Mathoniere B., Mauriaux D., Paoletti J. A short autocomplementary sequence in the 5′ leader region is responsible for dimerization of MoMuLV genomic RNA. Biochemistry. 34:1995;9785-9794.
18. De Tapia M., Metzler V., Mougel M., Ehresmann B., Ehresmann C. Dimerization of MoMuLV genomic RNA: redefinition of the role of the palindromic stem-loop H1 (278-303) and new roles for stem-loops H2 (310-352) and H3 (355-374). Biochemistry. 37:1998;6077-6085.
19. Ly H., Nierlich D.P., Olsen J.C., Kaplan A.H. Moloney murine sarcoma virus genomic RNAs dimerize via a two-step process: a concentration-dependent kissing-loop interaction is driven by initial contact between consecutive guanines. J. Virol. 73:1999;7255-7261.
20. Oroudjev E.M., Kang P.C.E., Kohlstaedt L.A. An additional dimer linkage structure in moloney murine leukemia virus RNA. J. Mol. Biol. 291:1999;603-613.
21. Kim C.-H., Tinoco I. Jr. A retroviral RNA kissing cokmplex containing only two G-C base-pairs. Proc. Natl Acad. Sci. USA. 97:2000;9396-9401.
22. Yu S.S., Kim J.-M., Kim S. The 17 nucleotides downstream from the env gene stop codon are important for murine leukemia virus packaging. J. Virol. 74:2000;8775-8780.
23. D'Souza V., Melamed J., Habib D., Pullen K., Wallace K., Summers M.F. Identification of a high-affinity nucleocapsid protein binding site within the moloney murine leukemia virus Y-RNA packaging signal. Implications for genome recognition. J. Mol. Biol. 314:2001;217-232.
24. De Guzman R.N., Wu Z.R., Stalling C.C., Pappalardo L., Borer P.N., Summers M.F. Structure of the HIV-1 nucleocapsid protein bound to the SL3 Ψ-RNA recognition element. Science. 279:1998;384-388.
25. Amarasinghe G.K., De Guzman R.N., Turner R.B., Chancellor K., Wu Z.-R., Summers M.F. NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the Ψ-RNA packaging signal. J. Mol. Biol. 301:2000;491-511.
26. Lukavsky P.J., Kim I., Otto G.A., Puglisi J.D. Structure of HCV IRES domain II determined by NMR. Nature Struct. Biol. 10:2003;1033-1038.
27. Kolk M.H., van der Graaf M., Wijmenga S.S., Pleij C.W.A., Heus H.A., Hilbers C.W. NMR structure of a classical pseudoknot: interplay of single- and double-stranded RNA. Science. 280:1998;434-438.
28. Varani L., Gunderson S.I., Mattaj I.W., Kay L.E., Neuhaus D., Varani G. The NMR structure of the 38 kDa U1A protein-PIE RNA complex reveals the basis of cooperativity in regulation of polyadenylation by human U1A protein. Nature Struct. Biol. 7:2000;329-335.
29. Dieckmann T., Feigon J. Assignment methodology for larger RNA oligonucleotides: application to an ATP-binding RNA aptamer. J. Biomol. NMR. 9:1997;259-272.
30. Saudek, V., Piotto, M. & Sklenar, V. (1994) WATERGATE: WATER suppression by GrAdient-Tailored Excitation. In Bruker Report, vol. 140/94, pp. 6-9.
31. 2O in protein NMR. Application to sensitivity enhancement and NOE measurement. J. Am. Chem. Soc. 115:1993;12593-12593.
32. Wüthrich K. NMR of Proteins and Nucleic Acids. 1986;Wiley, New York.
33. Legault P., Pardi A. Unusual dynamics and pKa shift at the active site of a lead-dependent ribozyme. J. Am. Chem. Soc. 119:1997;6621-6628.
34. Ravindranathan S., Butcher S.E., Feigon J. Adenine protonation in domain B of the hairpin ribozyme. Biochemistry. 39:2000;16026-16032.
35. Cai Z., Tinoco I. Jr. Solution structure of loop A from the hairpin ribozyme from tobacco ringspot virus satellite. Biochemistry. 35:1996;6026-6036.
36. Huppler A., Nikstad L.J., Allmann A.M., Brow D.A., Butcher S.E. Metal binding and base ionization in the U6 RNA intramolecular stem-loop structure. Nature Struct. Biol. 9:2002;431-435.
37. Jucker F.M., Heus H.A., Yip P.F., Moors E.H.M., Pardi A. A network of heterogeneous hydrogen bonds in GNRA tetraloops. J. Mol. Biol. 264:1996;968-980.
38. Clore, G. M. & Kuszewski, J. (2003). Improving the accuracy of NMR structures of RNA by means of conformational database potentials of mean force as assessed by complete dipplar coupling cross-validation. J. Am. Chem. Soc., 125, 1518-1525.
39. Rife J.P., Stallings S.C., Correll C.C., Dallas A., Steitz T.A., Moore P.B. Comparison of the crystal and solution structures of two RNA oligonucleotides. Biophys. J. 76:1999;66-75.
40. Leonard G.A., McAuley-Hecht K.E., Ebel S., Lough D.M., Brown T., Hunter W.N. Crystal and molecular structure of r(CGCGAAUUAGCG): an RNA duplex containing two G(anti).A(anti) base-pairs. Structure. 2:1994;483-494.
41. Klosterman P.S., Shah S.A., Steitz T.A. Crystal structures of two plasmid copy control related RNA duplexes: an 18 base base-pair duplex at 1.20 Å resolution and a 19 base-pair duplex at 1.55 Å resolution. Biochemistry. 38:1999;14784-14792.
42. Trikha J., Filman D.J., Hogle J.M. Crystal structure of a 14 base-pair RNA duplex with non-symmetrical tandem G-U wobble base-pairs. Nucl. Acids Res. 27:1999;1728-1739.
43. Tolman J.R., Flanagan J.M., Kennedy M.A., Prestegard J.H. Nuclear magnetic dipolar interactions in field-oriented proteins: information for structure determination in solution. Proc. Natl Acad. Sci. USA. 92:1995;9279-9283.
44. Tjandra N., Bax A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science. 278:1997;1111-1114.
45. Hansen M.R., Mueller L., Pardi A. Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nature Struct. Biol. 5:1998;1065-1074.
46. Trantirek L., Urbasek M., Stefl R., Feigon J., Sklenar V. A method for direct determination of helical parameters in nucleic acids using residual dipolar couplings. J. Am. Chem. Soc. 122:2000;10454-10455.
47. Wu Z.-R., Delaglio F., Tjandra N., Zhurkin V.B., Bax A. Overall structure and sugar dynamics of a DNA dodecamer from homo- and heteronuclear dipolar couplings and 31P chemical shift anisotropy. J. Biomol. NMR. 26:2003;297-315.
48. Tycko R., Blanco F.J., Ishii Y. Alignment to biopolymers in strained gels: a new way to create detectable dipole-dipole couplings in high-resolution biomolecular NMR. J. Am. Chem. Soc. 122:2000;9340-9341.
49. Sass H.J., Musco G., Stahl S.J., Wingfield P.T., Grzesiek S. Solution NMR of proteins within polyacrylamide gels: diffusional properties and residual alignment by mechanical stress or embedding of oriented purple membranes. J. Biomol. NMR. 18:2000;303-309.
50. Ottiger M., Delaglio F., Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131:1998;373-378.
51. Lawrence D.C., Stover C.C., Noznitsky J., Wu Z.-R., Summers M.F. Structure of the intact stem adn bulge of HIV-1 Ψ-RNA stem loop SL1. J. Mol. Biol. 326:2003;529-542.
52. Pan B., Mitra S.N., Sundaralingam M. Structure of a 16-mer RNA duplex r(GCAGACUUAAAUCUGC)2 with wobble C*A+mismatches. J. Mol. Biol. 283:1998;977-984.
53. Hoogstraten C.G., Legault P., Pardi A. NMR solution structure of a lead-dependent ribozyme: evidence for dynamics in RNA catalysis. J. Mol. Biol. 284:1998;337-350.
54. Lietzke S.E., Barnes C.L., Berglund J.A., Kundrot C.E. 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. 4:1996;917-930.
55. Wang Y.-X., Huang S., Draper D.E. Structure of a U-U pair within a conserved ribosomal RNA hairpin. Nucl. Acids Res. 24:1996;2666-2672.
56. Shi K., Wahi M., Sundaralingam M. Crystal structure of an RNA duplex r(GGGCGCUCC)2 with non-adjacent G-U base-pairs. Nucl. Acids Res. 27:1999;2196-2201.
57. Correll C.C., Freeborn B., Moore P.B., Steitz T.A. Metals, motifs, and recognition in the crystal structure of a 5S rRNA domain. Cell. 91:1997;705-712.
58. Wimberly B.T., Brodersen D.E., Clemons W.M. Jr, Morgan-Warren R.J., Carter A.P., Vonrhein C., et al. Structure of the 30s ribosomal subunit. Nature. 407:2000;327-339.
59. Ye X., Kumar R.A., Patel D.J. Molecular recognition in the bovine immunodeficiency virus tat peptide-TAR RNA complex. Chem. Biol. 2:1995;827-840.
60. Cate J.H., Gooding A.R., Podell E., Zhou K., Golden B.L., Kundrot C.E., et al. Crystal structure of a group I ribozyme domain: principles of RNA packaging. Science. 273:1996;1678-1685.
61. Klein D.J., Schmeing T.M., Moore P.B., Steitz T.A. The kink-turn: a new RNA secondary structure motif. EMBO J. 20:2001;4214-4221.
62. Nissen P., Ippolito J.A., Ban N., Moore P.B., Steitz T.A. RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc. Natl Acad. Sci. USA. 98:2001;4899-4903.
63. Bieth E., Gabus C., Darlix J.-L. A study of the dimer formation of Rous sarcoma virus RNA and of its effect on viral protein synthesis in vitro. Nucl. Acids Res. 18:1990;119-127.
64. Darlix J.-L., Gabus C., Nugeyre M.-T., Clavel F., Barre-Sinoussi F. Cis elements and trans-acting factors involved in the RNA dimerization of the human immunodeficiency virus HIV-1. J. Mol. Biol. 216:1990;689-699.
65. Bonnet-Mathoniere B., Girard P.-M., Muriaux D., Paoletti J. Nucleocapsid protein 10 activates dimerization of the RNA of moloney murine leukaemia virus in vitro. Eur. J. Biochem. 238:1996;129-135.
66. Girard P.-M., de Rocquigny H., Roques B.-P., Paoletti J. A model of Psi dimerization: destabilization of the C278-G303 stem-loop by the nucleocapsid protein (NCp10) of MoMuLV. Biochemistry. 35:1996;8705-8714.
67. Nagaswamy U., Voss N., Zhang Z., Fox G.E. Database of non-canonical base-pairs found in known RNA structures. Nucl. Acids Res. 28:2000;375-376.
68. Nagaswamy U., Larios-Sanz M., Hury J., Collins S., Zhang Z., Zhao Q., Fox G.E. NCIR: a database of non-canonical interactions in known RNA structures. Nucl. Acids Res. 30:2002;395-397.
69. Patel D.J. Adaptive recognition in RNA complexes with peptides and protein modules. Curr. Opin. Struct. Biol. 9:1999;74-87.
70. Mollova E.T., Hansen M.R., Pardi A. Global structure of RNA determined with residual dipolar couplings. J. Am. Chem. Soc. 122:2000;11561-11562.
71. Hennig M., Carlomagno T., Williamson J.R. Residual dipolar coupling TOCSY for direct through space correlations of base protons and phosphorus nuclei in RNA. J. Am. Chem. Soc. 123:2001;3395-3396.
72. Vallurupalli P., Moore P.B. Measurement of H2′-C2′ and H3′-C3′ dipolar couplings in RNA molecules. J. Biomol. NMR. 24:2002;63-66.
73. Miclet E., O'Neil-Cabello E., Nikonowicz E.P., Live D., Bax A. 1H-1H dipolar couplings provide a unique probe of RNA backbone structure. J. Am. Chem. Soc. 125:2003;15740-15741.
74. O'Neil-Cabello E., Bryce D.L., Nikonowicz E.P., Bax A. Measurement of five dipolar couplings from a single 3D NMR multiplet applied to the study of RNA dynamics. J. Am. Chem. Soc. 126:2004;66-67.
75. Milligan J.F., Uhlenbeck O.C. Synthesis of small RNAs using T7 RNA polymerase. Methods Enzymol. 180:1989;51-62.
76. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR. 6:1995;277-293.
77. Johnson B.A., Blevins R.A. NMRview: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR. 4:1994;603-614.
78. Jeener J., Meier B.H., Bachmann P., Ernst R.R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71:1979;4546-4553.
79. Macura S., Ernst R.R. Elucidation of cross relaxation in liquids by two-dimensional NMR spectroscopy. Mol. Phys. 41:1980;95-117.
80. Bothner-By A., Stephens R.L., Lee J.-M., Warren C.D., Jeanloz R.W. Structure determination of a tetrasaccharide: transient nuclear Overhauser effects in the rotating frame. J. Am. Chem. Soc. 106:1984;811-813.
81. Bax A., Griffey R.H., Hawkins B.L. Correlation of proton and nitrogen-15 chemical shifts by multiple quantum NMR. J. Magn. Reson. 55:1983;301-315.
82. Bax A., Summers M.F. 1H and 13C assignments from sensitivity enhanced detection of heteronuclear multiple bond connectivity by 2D multiple quantum NMR. J. Am. Chem. Soc. 108:1986;2093-2094.
83. Fesik S.W., Zuiderweg E.R.P. Heteronuclear three-dimensional NMR spectroscopy. A strategy for the simplification of homonuclear two-dimensional NMR spectra. J. Magn. Reson. 78:1988;588-593.
84. Vuister G.W., Clore G.M., Gronenborn A.M., Powers R., Garrett D.S., Tschudin R., Bax A. Increased resolution and improved spectral quality in four-dimensional 13C/13C-separated HMQC-NOESY-HMQC spectra using pulsed field gradients. J. Magn. Reson., ser. B. 101:1993;210213.
85. Piotto M., Saudek V., Sklenar V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR. 2:1992;661-665.
86. 15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: application to interleukin 1β Biochemistry. 28:1989;6150-6156.
87. Kay L.E., Torchia D.A., Bax A. Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry. 28:1989;8972-8979.
88. Mikael Akke R.F., Jiang F., Patel D., Palmer A.G. III. Base dynamics in a UUCG tetraloop RNA hairpin characterized by 15N spin relaxation: correlations with structure and stability. RNA. 3:1997;702-709.
89. 13C decoupling. J. Magn. Reson. 98:1992;428-435.
90. Güntert P., Mumenthaler C., Wüthrich K. Torsion angle dynamics for protein structure calculations with a new program, DYANA. J. Mol. Biol. 273:1997;283-298.
91. Case D.A. AMBER 7 Users Manual. 2002;University of California, San Francisco.
92. Dickerson R.E. Definitions and nomenclature of nucleic acid structure parameters. J. Biomol. Struct. Dynam. 6:1989;627-634.
93. Saenger W. Principles of Nucleic Acid Structure. 1984;Springer-Verlag, New York, NY.
94. Dossett P., Hus J.-C., Marion D., Blackledge M. A novel interactive tool for rigid-body modeling of multi-domain macromolecules using residual dipolar couplings. J. Biomol. NMR. 20:2001;223-231.
95. DeLano Scientific. The PyMOL Molecular Graphics System. 2002;DeLano, W. L.
96. Lavery R., Sklenar H. Defining the structure of irregular nucleic acids: conventions and principles. J. Biomol. Struct. Dynam. 6:1989;655-667.
97. Lavery R., Sklenar H. The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dynam. 6:1988;63-91.