Skip to main content

Magnetic field induced residual dipolar couplings of imino groups in nucleic acids from measurements at a single magnetic field

Journal of Biomolecular NMR volume 39, pages 91–96 (2007)Cite this article

Abstract

For base-paired nucleic acids, variations in 1JNH and the imino 1H chemical shift are both dominated by hydrogen bond length. In the absence of molecular alignment, the 1JNH coupling for the imino proton then can be approximated by 1JNH = (1.21Hz/ppm)δH − 103.5 ± 0.6 Hz, where δH represents the chemical shift of the imino proton in ppm. This relation permits imino residual dipolar couplings (RDCs) resulting from magnetic susceptibility anisotropy (MSA) to be extracted from measurement of (1JNH + RDC) splittings at a single magnetic field strength. Magnetic field-induced RDCs were measured for tRNAVal and the alignment tensor determined from magnetic-field alignment of tRNAVal agrees well with the tensor calculated by summation of the MSA tensors of the individual nucleobases.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  • Al-Hashimi HM, Tolman JR, Majumdar A, Gorin A, Patel DJ (2001) Determining stoichiometry in homomultimeric nucleic acid complexes using magnetic field induced residual dipolar couplings. J Am Chem Soc 123:5806–5807

    Article  Google Scholar 

  • Barfield M, Dingley AJ, Feigon J, Grzesiek S (2001) A DFT study of the interresidue dependencies of scalar J-coupling and magnetic shielding in the hydrogen-bonding regions of a DNA tripler. J Am Chem Soc 123:4014–4022

    Article  Google Scholar 

  • Beger RD, Marathias VM, Volkman BF, Bolton PH (1998) Determination of internuclear angles of DNA using paramagnetic assisted magnetic alignment. J Magn Reson 135:256–259

    ADS  Article  Google Scholar 

  • Bertini I, Del Bianco C, Gelis I, Katsaros N, Luchinat C, Parigi G, Peana M, Provenzani A, Zoroddu MA (2004) Experimentally exploring the conformational space sampled by domain reorientation in calmodulin. Proc Natl Acad Sci USA 101:6841–6846

    ADS  Article  Google Scholar 

  • Blackledge M (2005) Recent progress in the study of biomolecular structure and dynamics in solution from residual dipolar couplings. Prog Nucl Magn Reson Spectrosc 46:23–61

    Article  Google Scholar 

  • Bothner-By AA (1996) Magnetic field induced alignment of molecules. In: Grant DM, Harris RK (eds) Encyclopedia of nuclear magnetic resonance, vol 5. Wiley, Chichester, pp 2932–2938

    Google Scholar 

  • Bothner-By AA, Gayathri C, Van Zijl PCM, Maclean C, Lai JJ, Smith KM (1985) High-field orientation effects in the high-resolution proton NMR-spectra of diverse porphyrins. Magn Reson Chem 23:935–938

    Article  Google Scholar 

  • Bryce DL, Boisbouvier J, Bax A (2004) Experimental and theoretical determination of nucleic acid magnetic susceptibility: importance for the study of dynamics by field-induced residual dipolar couplings. J Am Chem Soc 126:10820–10821

    Article  Google Scholar 

  • Clore GM, Starich MR, Gronenborn AM (1998) Measurement of residual dipolar couplings of marcomolecules aligned in the nematic phase of a colloidal suspension of rod-shaped viruses. J Am Chem Soc 120:10571–10572

    Article  Google Scholar 

  • Dingley AJ, Masse JE, Peterson RD, Barfield M, Feigon J, Grzesiek S (1999) Internucleotide scalar couplings across hydrogen bonds in Watson-Crick and Hoogsteen base pairs of a DNA triplex. J Am Chem Soc 121:6019–6027

    Article  Google Scholar 

  • Gaponenko V, Dvoretsky A, Walsby C, Hoffman BM, Rosevear PR (2000) Calculation of z-coordinates and orientational restraints using a metal binding tag. Biochemistry 39:15217–15224

    Article  Google Scholar 

  • Gayathri C, Bothner-By AA, Van Zijl PCM, Maclean C (1982) Dipolar magnetic-field effects in NMR-spectra of liquids. Chem Phys Lett 87:192–196

    ADS  Article  Google Scholar 

  • Hansen MR, Mueller L, Pardi A (1998) Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nat Struct Biol 5:1065–1074

    Article  Google Scholar 

  • Kung HC, Wang KY, Goljer I, Bolton PH (1995) Magnetic alignment of duplex and quadruplex DNAs. J Magn Reson Ser B 109:323–325

    Article  Google Scholar 

  • Lohman JAB, MacLean C (1978) Alignment effects on high resolution NMR spectra induced by the magnetic field. Chem Phys 35:269–274

    Article  Google Scholar 

  • Losonczi JA, Andrec M, Fischer MWF, Prestegard JH (1999) Order matrix analysis of residual dipolar couplings using singular value decomposition. J Magn Reson 138:334–342

    ADS  Article  Google Scholar 

  • Lukavsky PJ, Kim I, Otto GA, Puglisi JD (2003) Structure of HCVIRES domain II determined by NMR. Nat Struct Biol 10:1033–1038

    Article  Google Scholar 

  • Ma C, Opella SJ (2000) Lanthanide ions bind specifically to an added “EF-hand” and orient a membrane protein in micelles for solution NMR spectroscopy. J Magn Reson 146:381–384

    ADS  Article  Google Scholar 

  • Pervushin KV, Wider G, Wuthrich K (1998) Single transition-to-single transition polarization transfer (ST2-PT) in [N-15,H-1]-TROSY. J Biomol NMR 12:345–348

    Article  Google Scholar 

  • Peti W, Meiler J, Bruschweiler R, Griesinger C (2002) Model-free analysis of protein backbone motion from residual dipolar couplings. J Am Chem Soc 124:5822–5833

    Article  Google Scholar 

  • Piotto M, Saudek V, Sklenár V (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous sloutions. J Biomol NMR 2:661–665

    Article  Google Scholar 

  • Prestegard JH, Bougault CM, Kishore AI (2004) Residual dipolar couplings in structure determination of biomolecules. Chem Rev 104:3519–3540

    Article  Google Scholar 

  • Rodriguez-Castaneda F, Haberz P, Leonov A, Griesinger C (2006) Paramagnetic tagging of diamagnetic proteins for solution NMR. Magn Reson Chem 44:S10–S16

    Article  Google Scholar 

  • Ruckert M, Otting G (2000) Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J Am Chem Soc 122:7793–7797

    Article  Google Scholar 

  • Saenger W (1984). Principles of nucleic acid structure. Springer Verlag, New York

    Book  Google Scholar 

  • Sashital DG, Cornilescu G, Butcher SE (2004) U2-U6 RNA folding reveals a group II intron-like domain and a four-helix junction. Nat Struct Mol Biol 11:1237–1242

    Article  Google Scholar 

  • Sass H-J, Musco G, Stahl SJ, Wingfield PT, Grzesiek S (2000) Solution NMR of proteins within polyacrylamide gels: diffusional properties and residual alignment by mechanical stress or embedding of oriented purple membranes. J Biomol NMR 18:303–309

    Article  Google Scholar 

  • Sass J, Cordier F, Hoffmann A, Rogowski M, Cousin A, Omichinski JG, Lowen H, Grzesiek S (1999) Purple membrane induced alignment of biological macromolecules in the magnetic field. J Am Chem Soc 121:2047–2055

    Article  Google Scholar 

  • Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278:1111–1114

    ADS  Article  Google Scholar 

  • Tjandra N, Grzesiek S, Bax A (1996) Magnetic field dependence of nitrogen-proton J splittings in N-15-enriched human ubiquitin resulting from relaxation interference and residual dipolar coupling. J Am Chem Soc 118:6264–6272

    Article  Google Scholar 

  • Tjandra N, Omichinski JG, Gronenborn AM, Clore GM, Bax A (1997) Use of dipolar 1H-15N and 1H-13C couplings in the structure determination of magnetically oriented macromolecules in solution. Nat Struct Biol 4:732–738

    Article  Google Scholar 

  • Tolman JR, Flanagan JM, Kennedy MA, Prestegard JH (1995) Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution. Proc Natl Acad Sci USA 92:9279–9283

    ADS  Article  Google Scholar 

  • Tolman JR, Ruan K (2006) NMR residual dipolar couplings as probes of biomolecular dynamics. Chem Rev 106:1720–1736

    Article  Google Scholar 

  • Tycko R, Blanco FJ, Ishii Y (2000) Alignment of biopolymers in strained gels: a new way to create detectable dipole-dipole couuplings in high-resolution biomolecular NMR. J Am Chem Soc 122:9340–9341

    Article  Google Scholar 

  • van Buuren BNM, Schleucher J, Wittmann V, Griesinger C, Schwalbe H, Wijmenga SS (2004) NMR spectroscopic determination of the solution structure of a branched nucleic acid from residual dipolar couplings by using isotopically labeled nucleotides. Angew Chem Int Ed 43:187–192

    Article  Google Scholar 

  • Vermeulen A, McCallum SA, Pardi A (2005) Comparison of the global structure and dynamics of native and unmodified tRNA. Biochemistry 44:6024–6033

    Article  Google Scholar 

  • Vermeulen A, Zhou H, Pardi A (2000) Determining DNA global structure and DNA bending by application of NMR residual dipolar couplings. J Am Chem Soc 122:9638–9647

    Article  Google Scholar 

  • Wohnert J, Franz KJ, Nitz M, Imperiali B, Schwalbe H (2003) Protein alignment by a coexpressed lanthanide-binding tag for the measurement of residual dipolar couplings. J Am Chem Soc 125:13338–13339

    Article  Google Scholar 

Download references

Acknowledgement

This work was supported in part by the Intramural Research Program of the NIDDK, NIH, and by the Intramural AIDS-Targeted Antiviral Program of the Office of the Director, NIH, and NIH grant AI33098 (AP); MPL was supported in part by an NIH Training Grant T32 GM65103. We thank Dr. Sam E. Butcher and Dipa Sashital for providing us with the15N-enriched U2-U6 sample.

Author information

Affiliations

  1. Laboratory of Chemical Physics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, 20892, USA

    Jinfa Ying, Alexander Grishaev & Ad Bax

  2. Department of Chemistry and Biochemistry, 215 UCB, University of Colorado, Boulder, CO, 80309-0215, USA

    Michael P. Latham & Arthur Pardi

Authors
  1. Jinfa Ying
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander Grishaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael P. Latham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arthur Pardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ad Bax
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Arthur Pardi or Ad Bax.

Additional information

Jinfa Ying, Alexander Grishaev and Michael P. Latham contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Ying, J., Grishaev, A., Latham, M.P. et al. Magnetic field induced residual dipolar couplings of imino groups in nucleic acids from measurements at a single magnetic field. J Biomol NMR 39, 91–96 (2007). https://doi.org/10.1007/s10858-007-9181-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10858-007-9181-7

Keywords

  • Alignment
  • Chemical shift
  • Dipolar coupling
  • Magnetic susceptibility anisotropy
  • RDC
  • tRNAVal