Abstract
We present a scheme that allows the simultaneous detection of PAR and PAIN correlation spectra in a single two-dimensional experiment. For both spectra, we obtain almost the same signal-to-noise ratio as if a PAR or PAIN spectrum is recorded separately, which in turn implies that one of the spectra may be considered additional information for free. The experiment is based on the observation that in a PAIN experiment, the PAR condition is always also fulfilled. The performance is demonstrated experimentally using uniformly 13C,15N-labeled samples of N–f–MLF–OH and ubiquitin.
References
Bayro MJ, Huber M, Ramachandran R, Davenport TC, Meier BH, Ernst M, Griffin RG (2009) Dipolar truncation in magic-angle spinning NMR recoupling experiments. J Chem Phys 130(11):114506
Bertini I, Bhaumik A, De Paepe G, Griffin RG, Lelli M, Lewandowski JR, Luchinat C (2010) High-resolution solid-state NMR structure of a 17.6 kDa protein. J Am Chem Soc 132(3):1032–1040
Böckmann A (2008) 3D protein structures by solid-state NMR spectroscopy: ready for high resolution. Angew Chem Int Ed Engl 47(33):6110–6113
Böckmann A, Gardiennet C, Verel R, Hunkeler A, Loquet A, Pintacuda G, Emsley L, Meier BH, Lesage A (2009) Characterization of different water pools in solid-state NMR protein samples. J Biomol NMR 45(3):319–327
Cady SD, Schmidt-Rohr K, Wang J, Soto CS, Degrado WF, Hong M (2010) Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463(7281):689–692
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(6911):98–102
De Paepe G, Lewandowski JR, Loquet A, Bockmann A, Griffin RG (2008) Proton assisted recoupling and protein structure determination. J Chem Phys 129(24):245101–245122
De Paepe G, Lewandowski JR, Loquet A, Eddy M, Megy S, Böckmann A, Griffin RG (2011) Heteronuclear proton assisted recoupling. J Chem Phys 134(9):095101–095119
Ferguson N, Becker J, Tidow H, Tremmel S, Sharpe T, Krause G, Flinders J, Petrovich M, Berriman J, Oschkinat H, Fersht A (2006) General structural motifs of amyloid protofilaments. PNAS 103:16248–16253
Franks W, Wylie B, Frericks Schmidt H, Nieuwkoop A, Mayrhofer R-M, Shah G, Graesser D, Rienstra CM (2008) Dipole tensor-based atomic-resolution structure determination of a nanocrystalline protein by solid-state NMR. Proc Nat Acad Sci 105:4621–4625
Franks WT, Atreya HS, Szyperski T, Rienstra CM (2010) GFT projection NMR spectroscopy for proteins in the solid state. J Biomol NMR 48(4):213–223
Gath J, Habenstein B, Bousset L, Melki R, Meier BH, Böckmann A (2011) Solid-state NMR sequential assignments of α-synuclein. Biomol NMR Assign. doi:10.1007/s12104-011-9324-3
Grommek A, Meier BH, Ernst M (2006) Distance information from proton-driven spin diffusion under MAS. Chem Phys Lett 427(4–6):404–409
Habenstein B, Wasmer C, Bousset L, Sourigues Y, Schütz A, Loquet A, Meier BH, Melki R, Böckmann A (2011) Extensive de novo solid-state NMR assignments of the 33 kDa C-terminal domain of the Ure2 prion. J Biomol NMR 51(3):235–243
Hediger S, Meier BH, Ernst RR (1995) Adiabatic passage Hartmann-Hahn cross polarization in NMR under magic angle sample spinning. Chem Phys Lett 240(1):449–456
Herbst C, Riedel K, Ihle Y, Leppert J, Ohlenschläger O, Görlach M, Ramachandran R (2008) MAS solid state NMR of RNAs with multiple receivers. J Biomol NMR 41:121–125
Higman VA, 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
Huber M, Hiller S, Schanda P, Ernst M, Böckmann A, Verel R, Meier BH (2011) A proton-detected 4D solid-state NMR experiment for protein structure determination. ChemPhysChem 12(5):915–918
Iwata K, Fujiwara T, Matsuki Y, Akutsu H, Takahashi S, Naiki H, Goto Y (2006) 3D structure of amyloid protofilaments of β2-microglobulin fragment probed by solid-state NMR. PNAS 103:18119–18124
Jaroniec C, MacPhee C, Bajaj V, McMahon M, Dobson C, Griffin R (2004) High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy. PNAS 101(3):711–716
Jehle S, Rajagopal P, Bardiaux B, Markovic S, Kühne R, Stout JR, Higman VA, Klevit RE, van Rossum B-J, Oschkinat H (2010) Solid-state NMR and SAXS studies provide a structural basis for the activation of alphaB-crystallin oligomers. Nat Struct Mol Biol 17(9):1037–1042
Lange A, Becker S, Seidel K, Giller K, Pongs O, Baldus M (2005) A concept for rapid protein-structure determination by solid-state NMR spectroscopy. Angew Chem Int Edit 44(14):2089–2092
Lange V, Becker-Baldus J, Kunert B, van Rossum B-J, Casagrande F, Engel A, Roske Y, Scheffel FM, Schneider E, Oschkinat H (2010) A MAS NMR study of the bacterial ABC transporter ArtMP. ChemBioChem 11(4):547–555
Lewandowski JR, De Paepe G, Griffin RG (2007) Proton assisted insensitive nuclei cross polarization. J Am Chem Soc 129(4):728–729
Lewandowski JR, De Paëpe G, Eddy MT, Struppe J, Maas W, Griffin RG (2009) Proton assisted recoupling at high spinning frequencies (dagger). J Phys Chem B 113(27):9062–9069
Linser R, Bardiaux B, Higman V, Fink U, Reif B (2011) Structure calculation from unambiguous long-range amide and methyl 1H−1H distance restraints for a microcrystalline protein with MAS solid-state NMR spectroscopy. J Am Chem Soc 133(15):5905–5912
Loquet A, Bardiaux B, Gardiennet C, Blanchet C, Baldus M, Nilges M, Malliavin T, Böckmann A (2008) 3D structure determination of the Crh protein from highly ambiguous solid-state NMR restraints. J Am Chem Soc 130(11):3579–3589
Mani R, Tang M, Wu X, Buffy JJ, Waring AJ, Sherman MA, Hong M (2006) Membrane-bound dimer structure of a β-Hairpin antimicrobial peptide from rotational-echo double-resonance solid-state NMR. Biochemistry 45(27):8341–8349
Manolikas T, Herrmann T, Meier BH (2008) Protein structure determination from C-13 spin-diffusion solid-state NMR spectroscopy. J Am Chem Soc 130(12):3959–3966
Nielsen JT, Bjerring M, Jeppesen MD, Pedersen RO, Pedersen JM, Hein KL, Vosegaard T, Skrydstrup T, Otzen DE, Nielsen NC (2009) Unique identification of supramolecular structures in amyloid fibrils by solid-state NMR spectroscopy. Angewandte Chemie Int Ed 48(12):2118–2121
Nieuwkoop AJ, Wylie BJ, Franks WT, Shah GJ, Rienstra CM (2009) Atomic resolution protein structure determination by three-dimensional transferred echo double resonance solid-state nuclear magnetic resonance spectroscopy. J Chem Phys 131(9):095101
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(12):4175–4177
Scholz I, Meier BH, Ernst M (2007) Operator-based triple-mode Floquet theory in solid-state NMR. J Chem Phys 127(20):204504–204513
Schütz AK, Soragni A, Hornemann S, Aguzzi A, Ernst M, Böckmann A, Meier BH (2011) The amyloid-congo red interface at atomic resolution. Angew Chem Int Ed Engl 50(26):5956–5960
Todokoro Y, Yumen I, Fukushima K, Kang S-W, Park J-S, Kohno T, Wakamatsu K, Akutsu H, Fujiwara T (2006) Structure of tightly membrane-bound mastoparan-X, a G-protein-activating peptide. Determined by solid-state NMR. Biophys J 91(4):1368–1379
Traaseth NJ, Shi L, Verardi R, Mullen DG, Barany G, Veglia G (2009) Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach. Proc Natl Acad Sci USA 106(25):10165–10170
van Melckebeke H, Wasmer C, Lange A, Ab E, Loquet A, Böckmann A, Meier BH (2010) Atomic-resolution three-dimensional structure of HET-s(218–289) amyloid fibrils by solid-state NMR spectroscopy. J Am Chem Soc 132(39):13765–13775
Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH (2008) Amyloid fibrils of the HET-s(218–289) prion form a beta solenoid with a triangular hydrophobic core. Science 319(5869):1523–1526
Zhang Y, Doherty T, Li J, Lu W, Barinka C, Lubkowski J, Hong M (2010) Resonance assignment and three-dimensional structure determination of a human α-defensin, HNP-1, by solid-state NMR. J Mol Biol 397(2):408–422
Zhou DH, Shea JJ, Nieuwkoop AJ, Franks WT, Wylie BJ, Mullen C, Sandoz D, Rienstra CM (2007) Solid-state protein-structure determination with proton-detected triple-resonance 3D magic-angle-spinning NMR spectroscopy. Angew Chem Int Edit 46(44):8380–8383
Acknowledgments
This work was supported by the Swiss National Science Foundation (Grant 200020_134681).The European Commission under the Seventh Framework Program (FP7), contract Bio-NMR 261863 and the Danish National Research Foundation.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nielsen, A.B., Székely, K., Gath, J. et al. Simultaneous acquisition of PAR and PAIN spectra. J Biomol NMR 52, 283–288 (2012). https://doi.org/10.1007/s10858-012-9616-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10858-012-9616-7