Identification of NH...N hydrogen bonds by magic angle spinning solid state NMR in a double-stranded RNA associated with myotonic dystrophy

Nucleic Acids Research

Volumn 32, Issue 3, 2004, Pages 1177-1183

  Leppert, Jörg ^b   Urbinati, Carl R ^a   Häfner, Sabine ^b   Ohlenschläger, Oliver ^b   Swanson, Maurice S ^a   Görlach, Matthias ^b   Ramachandran, Ramadurai ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DOUBLE STRANDED RNA; GUANINE; HYDROGEN; NITROGEN; NITROGEN 15; NUCLEIC ACID; RNA; URACIL;

ARTICLE; BASE PAIRING; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; HUMAN CELL; HYDROGEN BOND; MYOTONIC DYSTROPHY; NEUROMUSCULAR DISEASE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; RNA CONFORMATION; RNA STRUCTURE; SOLID STATE; TRINUCLEOTIDE REPEAT; CHEMISTRY; GENETICS; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE;

BASE PAIRING; HYDROGEN BONDING; MYOTONIC DYSTROPHY; NITROGEN; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; RNA, DOUBLE-STRANDED; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 2342482988     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh288     Document Type: Article

References (50)

1. Gesteland,R.F., Atkins,J.F. and Cech,T.R. (1999) The RNA World (2nd edn). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Ohlenschlager,O., Wohnert,J., Ramachandran,R., Sich,C. and Gorlach,M. (2003) Nuclear magnetic resonance studies of ribonucleic acids. Spectroscopy, 17, 537-547.
3. Furtig,B., Richter,C., Wohnert,J. and Schwalbe,H. (2003) NMR spectroscopy of RNA. Chembiochem, 4, 936-962.
4. 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, in press.
5. Stoldt,M., Wohnert,J., Ohlenschlager,O., Gorlach,M. and Brown,L.R. (1999) The NMR structure of the 5S rRNA E-domain-protein L25 complex shows preformed and induced recognition. EMBO J., 18, 6508-6521.
6. Hermann,T. and Patel,D.J. (1999) Stitching together RNA tertiary architectures. J. Mol. Biol., 294, 829-849.
7. 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.
8. Bennett,A.E., Griffin,R.G. and Vega,S. (1994) Recoupling of Homo- and Heteronuclear Dipolar Interactions in Rotating Solids. Springer, Berlin.
9. Griffin,R.G. (1998) Dipolar recoupling in MAS spectra of biological solids. Nat. Struct. Biol., 5 (Suppl.), 508-512.
10. Dusold,S. and Sebald,A. (2000) Dipolar recoupling under magic-angle spinning conditions. Annu. Rep. NMR Spectrosc., 41, 185-264.
11. Castellani,F., van Rossum,B., Diehl,A., Schubert,M., Rehbein,K. and Oschkinat,H. (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature, 420, 98-102.
12. NN-couplings. J. Am. Chem. Soc., 120, 1601-1602.
13. Wohnert,J., Dingley,A.J., Stoldt,M., Gorlach,M., Grzesiek,S. and Brown,L.R. (1999) Direct identification of NH..N hydrogen bonds in non-canonical base pairs of RNA by NMR spectroscopy. Nucleic Acids Res., 27, 3104-3110.
14. Grzesiek,S., Cordier,F. and Dingley,A.J. (2001) Scalar couplings across hydrogen bonds. Methods Enzymol., 338, 111-133.
15. Bennett,A.E., Ok,J.H., Griffin,R.G. and Vega,S. (1992) Chemical shift correlation spectroscopy in rotating solids: Radio frequency-driven dipolar recoupling and longitudinal exchange. J. Chem. Phys., 96, 8624-8627.
16. Bennett,A.E., Rienstra,C.M., Griffith,J.M., Zhen,W., Lansbury,P.T. and Griffin,R.G. (1998) Homonuclear radio frequency-driven recoupling in rotating solids. J. Chem. Phys., 108, 9463-9479.
17. 13C enriched chlorophyll a/water aggregates with 2D dipolar correlation spectroscopy. Chem. Phys. Lett., 237, 502-508.
18. 15N -enriched BPTI in the solid state. J. Biomol. NMR, 16, 209-219.
19. Pauli,J., van Rossum,B., Forster,H., de Groot,H.J. and Oschkinat,H. (2000) Sample optimization and identification of signal patterns of amino acid side chains in 2D RFDR spectra of the alpha-spectrin SH3 domain. J. Magn. Reson., 143, 411-416.
20. 15N signal assignments of the alpha-spectrin SH3 domain by magic angle spinning solid-state NMR at 17.6 Tesla. Chembiochem, 2, 272-281.
21. vanRossum,B.J., Schulten,E.A., Raap,J., Oschkinat,H. and de Groot,H.J. (2002) A 3-D structural model of solid self-assembled chlorophyll a/H(2)O from multispin labeling and MAS NMR 2-D dipolar correlation spectroscopy in high magnetic field. J. Magn. Reson., 155, 1-14.
22. Heise,B., Leppert,J., Ohlenschlager,O., Gorlach,M. and Ramachandran,R. (2002) Chemical shift correlation via RFDR: elimination of resonance offset effects. J. Biomol. NMR, 24, 237-243.
23. Leppert,J., Heise,B., Ohlenschlager,O., Gorlach,M. and Ramachandran,R. (2003) Broadband RFDR with adiabatic inversion pulses. J. Biomol. NMR, 26, 13-24.
24. Brook,J.D., McCurrach,M.E., Harley,H.G., Buckler,A.J., Church,D., Aburatani,H., Hunter,K., Stanton,V.P., Thirion,J.P., Hudson,T. et al. (1992) Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell, 68, 799-808.
25. Napierala,M. and Krzyzosiak,W.J. (1997) CUG repeats present in myotonin kinase RNA form metastable 'slippery' hairpins. J. Biol. Chem., 272, 31079-31085.
26. Michalowski,S., Miller,J.W., Urbinati,C.R., Paliouras,M., Swanson,M.S. and Griffith,J. (1999) Visualization of double-stranded RNAs from the myotonic dystrophy protein kinase gene and interactions with CUG-binding protein. Nucleic Acids Res., 27, 3534-3542.
27. Kanadia,R.N., Johnstone,K.A., Mankodi,A., Lungu,C., Thornton,C.A., Esson,D., Timmers,A.M., Hauswirth,W.W. and Swanson,M.S. (2003) A muscleblind knockout model for myotonic dystrophy. Science, 302, 1978-1980.
28. Miller,J.W., Urbinati,C.R., Teng-Umnuay,P., Stenberg,M.G., Byrne,B.J., Thornton,C.A. and Swanson,M.S. (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J., 19, 4439-4448.
29. Charlet,B.N., Savkur,R.S., Singh,G., Philips,A.V., Grice,E.A. and Cooper,T.A. (2002) Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol. Cells, 10, 45-53.
30. Mankodi,A., Takahashi,M.P., Jiang,H., Beck,C.L., Bowers,W.J., Moxley,R.T., Cannon,S.C. and Thornton,C.A. (2002) Expanded CUG repeats trigger aberrant splicing of CIC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol. Cells, 10, 35-44.
31. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual (2nd edn). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Kupce,E. and Freeman,R. (1996) Optimized adiabatic pulses for wideband spin inversion. J. Magn. Reson., A118, 299-303.
33. Tycko,R., Pines,A. and Guckenheimer,J. (1985) Fixed point theory of iterative excitation schemes in NMR. J. Chem. Phys., 83, 2775-2802.
34. Levitt,M.H., Freeman,R. and Frenkiel,T. (1983) Broadband decoupling in high-resolution nuclear magnetic resonance spectroscopy. Adv. Magn. Reson., 11, 47-110.
35. Bak,M., Rasmussen,J.T. and Nielsen,N.C. (2000) SIMPSON: a general simulation program for solid-state NMR spectroscopy. J. Magn. Reson., 147, 296-330.
36. Leppert,J., Ohlenschlager,O., Gorlach,M. and Ramachandran,R. (2004) RFDR with adiabatic pulses: application to internuclear distance measurements. J. Biomol. NMR, 28, 229-233.
37. 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.
38. Wang,Y.X., Huang,S. and Draper,D.E. (1996) Structure of a U.U pair within a conserved ribosomal RNA hairpin. Nucleic Acids Res., 24, 2666-2672.
39. DiVerdi,J.A. and Opella,S.J. (1982) N-H bond lengths in DNA. J. Am. Chem. Soc., 104, 1761-1762.
40. Roberts,J.E., Harbison,G.S., Munowitz,M.G., Herzfeld,J. and Griffin,R.G. (1987) Measurement of heteronuclear bond distances in polycrystalline solids by solid state NMR techniques. J. Am. Chem. Soc., 109, 4163-4169.
41. Howhy,M., Jaroniec,C.P., Reif,B., Rienstra,C.M. and Griffin,R.G. (2000) Local structure and relaxation in solid state NMR: accurate measurement of amide N-H bond length and H-N-H bond angles. J. Am. Chem. Soc., 122, 3218-3219.
42. Zhao,X., Sudmeier,J.L., Bachovchin,W.W. and Levitt,M.H. (2001) Measurement of NH bond lengths by fast magic-angle spinning solid-state NMR spectroscopy: a new method for the quantification of hydrogen bonds. J. Am. Chem. Soc., 123, 11097-11098.
43. Hodgkinson,P. and Emsley,L. (1999) The accuracy of distance measurements in solid-state NMR. J. Magn. Reson., 139, 46-59.
44. Kiihne,S.R., Geahigan,K.B., Oyler,N.A., Zebroski,H., Mehta,M.A. and Drobny,G.P. (1999) Distance measurements in multiply labeled crystalline cytidines by dipolar recoupling solid state NMR. J. Phys. Chem., A103, 3890-3903.
45. Batey,R.T., Inada,M., Kujawinski,E., Puglisi,J.D. and Williamson,J.R. (1992) Preparation of isotopically labeled ribonucleotides for multidimensional NMR spectroscopy of RNA. Nucleic Acids Res., 20, 4515-4523.
46. SantaLucia,J., Jr, Shen,L.X., Cai,Z., Lewis,H. and Tinoco,I., Jr (1995) Synthesis and NMR of RNA with selective isotopic enrichment in the bases. Nucleic Acids Res., 23, 4913-4921.
47. Xu,J., Lapham,J. and Crothers,D.M. (1996) Determining RNA solution structure by segmental isotopic labeling and NMR: application to Caenorhabditis elegans spliced leader RNA 1. Proc. Natl Acad. Sci. USA, 93, 44-48.
48. Dieckmann,T. and Feigon,J. (1997) Assignment methodology for larger RNA oligonucleotides: application to an ATP-binding RNA aptamer. J. Biomol. NMR, 9, 259-272.
49. Kim,I., Lukavsky,P.J. and Puglisi,J.D. (2002) NMR study of 100 kDa HCV IRES RNA using segmental isotope labeling. J. Am. Chem. Soc., 124, 9338-9339.
50. 1H detection in MAS solid-state NMR spectroscopy of biomacromolecules employing pulsed field gradients for residual solvent suppression. J. Am. Chem. Soc., 125, 7788-7789.