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Rapid prediction of multi-dimensional NMR data sets

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Abstract

We present a computational environment for Fast Analysis of multidimensional NMR DAta Sets (FANDAS) that allows assembling multidimensional data sets from a variety of input parameters and facilitates comparing and modifying such “in silico” data sets during the various stages of the NMR data analysis. The input parameters can vary from (partial) NMR assignments directly obtained from experiments to values retrieved from in silico prediction programs. The resulting predicted data sets enable a rapid evaluation of sample labeling in light of spectral resolution and structural content, using standard NMR software such as Sparky. In addition, direct comparison to experimental data sets can be used to validate NMR assignments, distinguish different molecular components, refine structural models or other parameters derived from NMR data. The method is demonstrated in the context of solid-state NMR data obtained for the cyclic nucleotide binding domain of a bacterial cyclic nucleotide-gated channel and on membrane-embedded sensory rhodopsin II. FANDAS is freely available as web portal under WeNMR (http://www.wenmr.eu/services/FANDAS).

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References

  • Ader C, Frey S, Maas W, Schmidt HB, Goerlich D, Baldus M (2010) Amyloid-like interactions within nucleoporin FG hydrogels. Proc Natl Acad Sci 107:6281–6285

    Article  ADS  Google Scholar 

  • Alber F, Forster F, Korkin D, Topf M, Sali A (2008) Integrating diverse data for structure determination of macromolecular assemblies. Annu Revi Biochem Palo Alto Annu Rev Palo Alto Annu Rev 77:443–477

    Google Scholar 

  • Baldus M, Petkova AT, Herzfeld J, Griffin RG (1998) Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems. Mol Phys 95:1197–1207

    Article  ADS  Google Scholar 

  • Brothers MC, Nesbitt A, Hallock M, Rupansinghe S, Tang M, Harris J, Baudry J, Schuler M, Rienstra C (2012). VITAL NMR: using chemical shift derived secondary structure information for a limited set of amino acids to assess homology model accuracy. J Biomol NMR 52:41–56

    Google Scholar 

  • Castellani F, van Rossum B, Diehl A, Schubert M, Rehbein K, Oschkinat H (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 420:98–102

    Article  ADS  Google Scholar 

  • Cukkemane A, Nand D, Gradmann S, Weingarth M, Kaupp B, Baldus M (2012) Solid-state NMR [13C, 15N] resonance assignments of the nucleotide-binding domain of a bacterial cyclic nucleotide-gated channel. Biomol NMR Assign 6:225

  • de Vries SJ, van Dijk M, Bonvin AMJJ (2010) The HADDOCK web server for data-driven biomolecular docking. Nat Protoc 5:883–897

    Article  Google Scholar 

  • Dominguez C, Boelens R, Bonvin AMJJ (2003) HADDOCK: a protein–protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125:1731–1737

    Article  Google Scholar 

  • Etzkorn M, Martell S, Andronesi OC, Seidel K, Engelhard M, Baldus M (2007) Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angew Chem Int Ed 46:459–462

    Article  Google Scholar 

  • Etzkorn M, Seidel K, Li L, Martell S, Geyer M, Engelhard M, Baldus M (2010) Complex formation and light activation in membrane-embedded sensory rhodopsin II as seen by solid-state NMR spectroscopy. Structure 18:293–300

    Article  Google Scholar 

  • Fossi M, Castellani T, Nilges M, Oschkinat H, van Rossum BJ (2005) SOLARIA: a protocol for automated cross-peak assignment and structure calculation for solid-state magic-angle spinning NMR spectroscopy. Angew Chem Int Ed 44:6151–6154

    Article  Google Scholar 

  • Gelis I, Bonvin AMJJ, Keramisanou D, Koukaki M, Gouridis G, Karamanou S, Economou A, Kalodimos CG (2007) Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR. Cell 131:756–769

    Article  Google Scholar 

  • Goddard TD, Kneller D (2006). SPARKY 3. University of California, California

  • Guerry P, Herrmann T (2011) Advances in automated NMR protein structure determination. Q Rev Biophys 44:257–309

    Article  Google Scholar 

  • Han B, Liu Y, Ginzinger S, Wishart D (2011) SHIFTX2: significantly improved protein chemical shift prediction. J Biomol NMR 50:43–57

    Article  Google Scholar 

  • Hefke F, Bagaria A, Reckel S, Ullrich S, Dötsch V, Glaubitz C, Güntert P (2011) Optimization of amino acid type-specific 13C and 15N labeling for the backbone assignment of membrane proteins by solution- and solid-state NMR with the UPLABEL algorithm. J Biomol NMR 49(2):75–84

    Article  Google Scholar 

  • Heise H, Hoyer W, Becker S, Andronesi OC, Riedel D, Baldus M (2005) Molecular-level secondary structure, polymorphism, and dynamics of full-length α-synuclein fibrils studied by solid-state NMR. Proc Natl Acad Sci USA 102(44):15871–15876

    Article  ADS  Google Scholar 

  • Higman V, Flinders J, Hiller M, Jehle S, Markovic S, Fiedler S, van Rossum B-J, Oschkinat H (2009) Assigning large proteins in the solid state: a MAS NMR resonance assignment strategy using selectively and extensively 13C-labelled proteins. J Biomol NMR 44(4):245–260

    Article  Google Scholar 

  • Hohenfeld IP, Wegener AA, Engelhard M (1999). Purification of histidine tagged bacteriorhodopsin, pharaonis halorhodopsin and pharaonis sensory rhodopsin II functionally expressed in Escherichia coli. FEBS Lett 442:198–202

  • Hong M, Jakes K (1999) Selective and extensive C-13 labeling of a membrane protein for solid-state NMR investigations. J Biomol NMR 14:71–74

    Article  Google Scholar 

  • Hu KN, Qiang W, Tycko R (2011) A general Monte Carlo/simulated annealing algorithm for resonance assignment in NMR of uniformly labeled biopolymers. J Biomol NMR 50:267–276

    Article  Google Scholar 

  • Jehle S, Vollmar BS, Bardiaux B, Dove KK, Rajagopal P, Gonen T, Oschkinat H, Klevit RE (2011) N-terminal domain of αB-crystallin provides a conformational switch for multimerization and structural heterogeneity. Proc Natl Acad Sci 108:6409–6414

    Article  ADS  Google Scholar 

  • Kato H, van Ingen H, Zhou B-R, Feng H, Bustin M, Kay LE, Bai Y (2011) Architecture of the high mobility group nucleosomal protein 2-nucleosome complex as revealed by methyl-based NMR. Proc Natl Acad Sci 108:12283–12288

    Article  Google Scholar 

  • Klare JP, Bordignon E, Doebber M, Fitter J, Kriegsmann J, Chizhov I, Steinhoff HJ, Engelhard M (2006) Effects of solubilization on the structure and function of the sensory rhodopsin II/transducer complex. J Mol Biol 356:1207–1221

    Article  Google Scholar 

  • Lange A, Seidel K, Verdier L, Luca S, Baldus M (2003) Analysis of proton–proton transfer dynamics in rotating solids and their use for 3D structure determination. J Am Chem Soc 125:12640–12648

    Article  Google Scholar 

  • Lange A, Giller K, Hornig S, Martin-Eauclaire M-F, Pongs O, Becker S, Baldus M (2006) Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440:959–962

    Article  ADS  Google Scholar 

  • LeMaster DM, Kushlan DM (1996) Dynamical mapping of E. coli thioredoxin via C-13 NMR relaxation analysis. J Am Chem Soc 118:9255–9264

    Article  Google Scholar 

  • Linge JP, Habeck M, Rieping W, Nilges M (2003) ARIA: automated NOE assignment and NMR structure calculation. Bioinformatics 19:315–316

    Article  Google Scholar 

  • Loquet A, Bardiaux B, Gardiennet C, Blanchet C, Baldus M, Nilges M, Malliavin T, Bockmann A (2008) 3D structure determination of the Crh protein from highly ambiguous solid-state NMR restraints. J Am Chem Soc 130:3579–3589

    Article  Google Scholar 

  • Loquet A, Sgourakis NG, Gupta R, Giller K, Riedel D, Goosmann C, Griesinger C, Kolbe M, Baker D, Becker S, Lange A (2012) Atomic model of the type III secretion system needle. Nat Adv (online publication)

  • Manolikas T, Herrmann T, Meier BH (2008) Protein structure determination from 13C spin-diffusion solid-state NMR spectroscopy. J Am Chem Soc 130:3959–3966

    Article  Google Scholar 

  • Melquiond ASJ, Karaca E, Kastritis PL, Bonvin AMJJ (2012) Next challenges in protein–protein docking: from proteome to interactome and beyond. WIREs Comput Mol Sci 2:642–651

    Article  Google Scholar 

  • Nand D, Cukkemane A, Becker S, Baldus M (2012) Fractional deuteration applied to biomolecular solid-state NMR spectroscopy. J Biomol NMR 52:91–101

    Google Scholar 

  • Neal S, Nip AM, Zhang HY, Wishart DS (2003) Rapid and accurate calculation of protein H-1, C-13 and N-15 chemical shifts. J Biomol NMR 26:215–240

    Article  Google Scholar 

  • Nelson SJ, Schneider DM, Wand AJ (1991) Implementation of the main chain directed assignment strategy—computer-assisted approach. Biophys J 59:1113–1122

    Article  Google Scholar 

  • Renault M, Cukkemane A, Baldus M (2010) Solid-state NMR spectroscopy on complex biomolecules. Angew Chem Int Ed 49:8346–8357

    Article  Google Scholar 

  • Renault M, Bos MP, Tommassen J, Baldus M (2011) Solid-state NMR on a large multidomain integral membrane protein: the outer membrane protein assembly factor BamA. J Am Chem Soc 133:4175–4177

    Article  Google Scholar 

  • Renault M, Pawsey S, Bos MP, Koers EJ, Nand D, Tommassen-van Boxtel R, Rosay M, Tommassen J, Maas WE, Baldus M (2012a) Solid-state NMR spectroscopy on cellular preparations enhanced by dynamic nuclear polarization. Angew Chem Int Ed 51:2998–3001

    Article  Google Scholar 

  • Renault M, Tommassen-van Boxtel R, Bos MP, Post JA, Tommassen J, Baldus M (2012b) Cellular solid-state nuclear magnetic resonance spectroscopy. Proc Natl Acad Sci 109:4863–4868

    Article  ADS  Google Scholar 

  • Rosen MK, Gardner KH, Willis RC, Parris WE, Pawson T, Kay LE (1996) Selective methyl group protonation of perdeuterated proteins. J Mol Biol 263:627–636

    Article  Google Scholar 

  • Ruschak AM, Kay LE (2010) Methyl groups as probes of supra-molecular structure, dynamics and function. J Biomol NMR 46:75–87

    Article  Google Scholar 

  • Scholz I, Huber M, Manolikas T, Meier BH, Ernst M (2008) MIRROR recoupling and its application to spin diffusion under fast magic-angle spinning. Chem Phys Lett 460:278–283

    Article  ADS  Google Scholar 

  • Schunke S, Stoldt M, Novak K, Kaupp UB, Willbold D (2009) Solution structure of the Mesorhizobium loti K1 channel cyclic nucleotide-binding domain in complex with cAMP. EMBO Rep 10:729–735

    Article  Google Scholar 

  • Seidel K, Etzkorn M, Heise H, Becker S, Baldus M (2005) High-resolution solid-state NMR studies on uniformly C-13, N-15 -labeled ubiquitin. Chem BioChem 6:1638–1647

    Google Scholar 

  • Seidel K, Etzkorn M, Schneider R, Ader C, Baldus M (2009) Comparative analysis of nmr chemical shift predictions for proteins in the solid phase. Solid State NMR 35:235–242

    Article  Google Scholar 

  • Shen Y, Bax A (2010) SPARTA+: a modest improvement in empirical NMR chemical shift prediction by means of an artificial neural network. J Biomol NMR 48:13–22

    Article  Google Scholar 

  • Stevens T, Fogh R, Boucher W, Higman V, Eisenmenger F, Bardiaux B, van Rossum B-J, Oschkinat H, Laue E (2011) A software framework for analysing solid-state MAS NMR data. J Biomol NMR 51:437–447

    Article  Google Scholar 

  • Vuister GW, Kim SJ, Wu C, Bax A (1994) 2d and 3d NMR-study of phenylalanine residues in proteins by reverse isotopic labeling. J Am Chem Soc 116:9206–9210

    Article  Google Scholar 

  • Wang Y, Jardetzky O (2002) Probability-based protein secondary structure identification using combined NMR chemical-shift data. Protein Sci 11:852–861

    Google Scholar 

  • Wegener AA, Klare JP, Engelhard M, Steinhoff HJ (2001) Structural insights into the early steps of receptor-transducer signal transfer in archaeal phototaxis. EMBO J 20:5312–5319

    Article  Google Scholar 

  • Zimmerman DE, Kulikowski CA, Huang YP, Feng WQ, Tashiro M, Shimotakahara S, Chien CY, Powers R, Montelione GT (1997) Automated analysis of protein NMR assignments using methods from artificial intelligence. J Mol Biol 269:592–610

    Article  Google Scholar 

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Acknowledgments

This work was supported by the Netherlands Organization for Scientific Research (NWO) (grants 700.26.121 and 700.10.443 to M.B.) and by the European Community’s Seventh Framework Program, BioNMR project, contract number 211800, and the FP7 e-Infrastructure project WeNMR (contract no. 261572, www.wenmr.eu). We would like to thank Dieter Oesterhelt (Martinsried) for informing us that N. pharaonis can grow with acetate as sole carbon source. Initial work of J. Sauermann on the extraction of N. pharaonis lipids is gratefully acknowledged.

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Authors and Affiliations

  1. Faculty of Science, Bijvoet Center for Biomolecular Research, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Sabine Gradmann, Christian Ader, Deepak Nand, Abhishek Cukkemane, Marc van Dijk, Alexandre M. J. J. Bonvin & Marc Baldus

  2. Department of Physical Biochemistry, Max Planck Institute for Molecular Physiology, Otto-Hahn-Strasse 11, 44227, Dortmund, Germany

    Ines Heinrich, Marc Dittmann & Martin Engelhard

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  1. Sabine Gradmann
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  2. Christian Ader
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  8. Alexandre M. J. J. Bonvin
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  10. Marc Baldus
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Correspondence to Marc Baldus.

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Gradmann, S., Ader, C., Heinrich, I. et al. Rapid prediction of multi-dimensional NMR data sets. J Biomol NMR 54, 377–387 (2012). https://doi.org/10.1007/s10858-012-9681-y

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