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Dipole tensor-based atomic-resolution structure determination of a nanocrystalline protein by solid-state NMR.

Franks WT, Wylie BJ, Schmidt HL, Nieuwkoop AJ, Mayrhofer RM, Shah GJ, Graesser DT, Rienstra CM
Proc Natl Acad Sci U S A 105 4621-6 (2008)
Cited: 76 times
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Abstract

Magic-angle spinning (MAS) solid-state NMR (SSNMR) techniques have emerged in recent years for solving complete structures of uniformly labeled proteins lacking macroscopic order. Strategies used thus far have relied primarily on semiquantitative distance restraints, analogous to the nuclear Overhauser effect (NOE) routinely used in solution NMR. Here, we present a complementary approach for using relative orientations of molecular fragments, determined from dipolar line shapes. Whereas SSNMR distance restraints typically have an uncertainty of approximately 1 A, the tensor-based experiments report on relative vector (pseudobond) angles with precision of a few degrees. By using 3D techniques of this type, vector angle (VEAN) restraints were determined for the majority of the 56-residue B1 immunoglobulin binding domain of protein G [protein GB1 (a total of 47 HN-HN, 49 HN-HC, and 12 HA-HB restraints)]. By using distance restraints alone in the structure calculations, the overall backbone root-mean-square deviation (bbRMSD) was 1.01 +/- 0.13 A (1.52 +/- 0.12 A for all heavy atoms), which improved to 0.49 +/- 0.05 A (1.19 +/- 0.07 A) on the addition of empirical chemical shift [torsion angle likelihood obtained from shift and sequence similarity (TALOS)] restraints. VEAN restraints further improved the ensemble to 0.31 +/- 0.06 A bbRMSD (1.06 +/- 0.07 A); relative to the structure with distances alone, most of the improvement remained (bbRMSD 0.64 +/- 0.09 A; 1.29 +/- 0.07 A) when TALOS restraints were removed before refinement. These results represent significant progress toward atomic-resolution protein structure determination by SSNMR, capabilities that can be applied to a large range of membrane proteins and fibrils, which are often not amenable to solution NMR or x-ray crystallography.

Reviews - 2jsv mentioned but not cited (1)

  1. From Angstroms to Nanometers: Measuring Interatomic Distances by Solid-State NMR. Shcherbakov AA, Medeiros-Silva J, Tran N, Gelenter MD, Hong M. Chem Rev 122 9848-9879 (2022)

Articles - 2jsv mentioned but not cited (5)

  1. Dipole tensor-based atomic-resolution structure determination of a nanocrystalline protein by solid-state NMR. Franks WT, Wylie BJ, Schmidt HL, Nieuwkoop AJ, Mayrhofer RM, Shah GJ, Graesser DT, Rienstra CM. Proc Natl Acad Sci U S A 105 4621-4626 (2008)
  2. Fast Magic-Angle-Spinning 19F Spin Exchange NMR for Determining Nanometer 19F-19F Distances in Proteins and Pharmaceutical Compounds. Roos M, Wang T, Shcherbakov AA, Hong M. J Phys Chem B 122 2900-2911 (2018)
  3. Protein structure refinement using 13C alpha chemical shift tensors. Wylie BJ, Schwieters CD, Oldfield E, Rienstra CM. J Am Chem Soc 131 985-992 (2009)
  4. Domain swapping and amyloid fibril conformation. van der Wel PC. Prion 6 211-216 (2012)
  5. Detecting and accounting for multiple sources of positional variance in peak list registration analysis and spin system grouping. Smelter A, Rouchka EC, Moseley HNB. J Biomol NMR 68 281-296 (2017)


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  1. Amyloid polymorphism: structural basis and neurobiological relevance. Tycko R. Neuron 86 632-645 (2015)
  2. Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR. McDermott A. Annu Rev Biophys 38 385-403 (2009)
  3. Protein structure determination by magic-angle spinning solid-state NMR, and insights into the formation, structure, and stability of amyloid fibrils. Comellas G, Rienstra CM. Annu Rev Biophys 42 515-536 (2013)
  4. Recent advances in magic angle spinning solid state NMR of membrane proteins. Wang S, Ladizhansky V. Prog Nucl Magn Reson Spectrosc 82 1-26 (2014)
  5. Homonuclear dipolar recoupling techniques for structure determination in uniformly 13C-labeled proteins. Ladizhansky V. Solid State Nucl Magn Reson 36 119-128 (2009)
  6. Structural biology of supramolecular assemblies by magic-angle spinning NMR spectroscopy. Quinn CM, Polenova T. Q Rev Biophys 50 e1 (2017)
  7. Membrane proteins in their native habitat as seen by solid-state NMR spectroscopy. Brown LS, Ladizhansky V. Protein Sci 24 1333-1346 (2015)
  8. Macromolecular NMR spectroscopy for the non-spectroscopist: beyond macromolecular solution structure determination. Bieri M, Kwan AH, Mobli M, King GF, Mackay JP, Gooley PR. FEBS J 278 704-715 (2011)
  9. Nanoscale studies of protein-membrane interactions in blood clotting. Morrissey JH, Tajkhorshid E, Rienstra CM. J Thromb Haemost 9 Suppl 1 162-167 (2011)
  10. Protein-phospholipid interactions in blood clotting. Morrissey JH, Davis-Harrison RL, Tavoosi N, Ke K, Pureza V, Boettcher JM, Clay MC, Rienstra CM, Ohkubo YZ, Pogorelov TV, Tajkhorshid E. Thromb Res 125 Suppl 1 S23-5 (2010)
  11. Retinal conformation and dynamics in activation of rhodopsin illuminated by solid-state H NMR spectroscopy. Brown MF, Martínez-Mayorga K, Nakanishi K, Salgado GF, Struts AV. Photochem Photobiol 85 442-453 (2009)
  12. Protein-membrane interactions: blood clotting on nanoscale bilayers. Morrissey JH, Pureza V, Davis-Harrison RL, Sligar SG, Rienstra CM, Kijac AZ, Ohkubo YZ, Tajkhorshid E. J Thromb Haemost 7 Suppl 1 169-172 (2009)
  13. Prions: En route from structural models to structures. Böckmann A, Meier BH. Prion 4 72-79 (2010)
  14. Recent advances in solid-state nuclear magnetic resonance techniques to quantify biomolecular dynamics. Watt ED, Rienstra CM. Anal Chem 86 58-64 (2014)
  15. Challenges in numerical simulations of solid-state NMR experiments: spin exchange pulse sequences. Vosegaard T. Solid State Nucl Magn Reson 38 77-83 (2010)
  16. Dihedral Angle Measurements for Structure Determination by Biomolecular Solid-State NMR Spectroscopy. van der Wel PCA. Front Mol Biosci 8 791090 (2021)

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  2. Proton assisted recoupling and protein structure determination. De Paëpe G, Lewandowski JR, Loquet A, Böckmann A, Griffin RG. J Chem Phys 129 245101 (2008)
  3. A software framework for analysing solid-state MAS NMR data. Stevens TJ, Fogh RH, Boucher W, Higman VA, Eisenmenger F, Bardiaux B, van Rossum BJ, Oschkinat H, Laue ED. J Biomol NMR 51 437-447 (2011)
  4. Assigning large proteins in the solid state: a MAS NMR resonance assignment strategy using selectively and extensively 13C-labelled proteins. Higman VA, Flinders J, Hiller M, Jehle S, Markovic S, Fiedler S, van Rossum BJ, Oschkinat H. J Biomol NMR 44 245-260 (2009)
  5. alphaB-crystallin: a hybrid solid-state/solution-state NMR investigation reveals structural aspects of the heterogeneous oligomer. Jehle S, van Rossum B, Stout JR, Noguchi SM, Falber K, Rehbein K, Oschkinat H, Klevit RE, Rajagopal P. J Mol Biol 385 1481-1497 (2009)
  6. Protocols for the sequential solid-state NMR spectroscopic assignment of a uniformly labeled 25 kDa protein: HET-s(1-227). Schuetz A, Wasmer C, Habenstein B, Verel R, Greenwald J, Riek R, Böckmann A, Meier BH. Chembiochem 11 1543-1551 (2010)
  7. Solid-state NMR analysis of membrane proteins and protein aggregates by proton detected spectroscopy. Zhou DH, Nieuwkoop AJ, Berthold DA, Comellas G, Sperling LJ, Tang M, Shah GJ, Brea EJ, Lemkau LR, Rienstra CM. J Biomol NMR 54 291-305 (2012)
  8. High-resolution solid-state NMR structure of a 17.6 kDa protein. Bertini I, Bhaumik A, De Paëpe G, Griffin RG, Lelli M, Lewandowski JR, Luchinat C. J Am Chem Soc 132 1032-1040 (2010)
  9. Ultrahigh resolution protein structures using NMR chemical shift tensors. Wylie BJ, Sperling LJ, Nieuwkoop AJ, Franks WT, Oldfield E, Rienstra CM. Proc Natl Acad Sci U S A 108 16974-16979 (2011)
  10. Cryogenic temperature effects and resolution upon slow cooling of protein preparations in solid state NMR. Linden AH, Franks WT, Akbey Ü, Lange S, van Rossum BJ, Oschkinat H. J Biomol NMR 51 283-292 (2011)
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  14. Resolution and polarization distribution in cryogenic DNP/MAS experiments. Barnes AB, Corzilius B, Mak-Jurkauskas ML, Andreas LB, Bajaj VS, Matsuki Y, Belenky ML, Lugtenburg J, Sirigiri JR, Temkin RJ, Herzfeld J, Griffin RG. Phys Chem Chem Phys 12 5861-5867 (2010)
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  16. Optimal degree of protonation for ¹H detection of aliphatic sites in randomly deuterated proteins as a function of the MAS frequency. Asami S, Szekely K, Schanda P, Meier BH, Reif B. J Biomol NMR 54 155-168 (2012)
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  19. β-Helical architecture of cytoskeletal bactofilin filaments revealed by solid-state NMR. Vasa S, Lin L, Shi C, Habenstein B, Riedel D, Kühn J, Thanbichler M, Lange A. Proc Natl Acad Sci U S A 112 E127-36 (2015)
  20. Determination of relative tensor orientations by γ-encoded chemical shift anisotropy/heteronuclear dipolar coupling 3D NMR spectroscopy in biological solids. Hou G, Paramasivam S, Byeon IJ, Gronenborn AM, Polenova T. Phys Chem Chem Phys 12 14873-14883 (2010)
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  22. Atomic resolution protein structure determination by three-dimensional transferred echo double resonance solid-state nuclear magnetic resonance spectroscopy. Nieuwkoop AJ, Wylie BJ, Franks WT, Shah GJ, Rienstra CM. J Chem Phys 131 095101 (2009)
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  24. New applications of solid-state NMR in structural biology. van der Wel PCA. Emerg Top Life Sci 2 57-67 (2018)
  25. bcTol : a highly water-soluble biradical for efficient dynamic nuclear polarization of biomolecules. Jagtap AP, Geiger MA, Stöppler D, Orwick-Rydmark M, Oschkinat H, Sigurdsson ST. Chem Commun (Camb) 52 7020-7023 (2016)
  26. Determination of protein structures in the solid state from NMR chemical shifts. Robustelli P, Cavalli A, Vendruscolo M. Structure 16 1764-1769 (2008)
  27. Resonance assignment and three-dimensional structure determination of a human alpha-defensin, HNP-1, by solid-state NMR. Zhang Y, Doherty T, Li J, Lu W, Barinka C, Lubkowski J, Hong M. J Mol Biol 397 408-422 (2010)
  28. 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. Hefke F, Bagaria A, Reckel S, Ullrich SJ, Dötsch V, Glaubitz C, Güntert P. J Biomol NMR 49 75-84 (2011)
  29. Restraints on backbone conformations in solid state NMR studies of uniformly labeled proteins from quantitative amide 15N-15N and carbonyl 13C-13C dipolar recoupling data. Hu KN, Qiang W, Bermejo GA, Schwieters CD, Tycko R. J Magn Reson 218 115-127 (2012)
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  31. Proton-driven spin diffusion in rotating solids via reversible and irreversible quantum dynamics. Veshtort M, Griffin RG. J Chem Phys 135 134509 (2011)
  32. Spectral editing of two-dimensional magic-angle-spinning solid-state NMR spectra for protein resonance assignment and structure determination. Schmidt-Rohr K, Fritzsching KJ, Liao SY, Hong M. J Biomol NMR 54 343-353 (2012)
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