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Solid-state NMR spectroscopy

Nature Reviews Methods Primers volume 1, Article number: 2 (2021) Cite this article

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Abstract

Solid-state nuclear magnetic resonance (NMR) spectroscopy is an atomic-level method to determine the chemical structure, 3D structure and dynamics of solids and semi-solids. This Primer summarizes the basic principles of NMR spectroscopy as applied to the wide range of solid systems. The nuclear spin interactions and the effects of magnetic fields and radiofrequency pulses on nuclear spins in solid-state NMR are the same as in liquid-state NMR spectroscopy. However, because of the orientation dependence of the nuclear spin interactions in the solid state, the majority of high-resolution solid-state NMR spectra are measured under magic-angle spinning (MAS), which has profound effects on the types of radiofrequency pulse sequences required to extract structural and dynamical information. We describe the most common MAS NMR experiments and data analysis approaches for investigating biological macromolecules, organic materials and inorganic solids. Continuing development of sensitivity-enhancement NMR approaches, including 1H-detected fast MAS experiments, dynamic nuclear polarization and experiments in ultra-high magnetic fields, is described. We highlight recent applications of solid-state NMR spectroscopy to biological and materials chemistry. The Primer ends with a discussion of current limitations as well as areas of development of solid-state NMR spectroscopy and points to emerging areas of applications of this sophisticated spectroscopy.

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Fig. 1: Basics of solid-state NMR spectroscopy for structural analysis of biomolecules and materials.
Fig. 2: Some common solid-state NMR pulse sequences.
Fig. 3: Representative solid-state NMR results and experiments.
Fig. 4: Applications of solid-state NMR spectroscopy to biological chemistry.
Fig. 5: Applications of solid-state NMR spectroscopy to materials chemistry.
Fig. 6: Outlook for MAS solid-state NMR spectroscopy.

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References

  1. Levitt, M. H. Spin Dynamics Basic of Nuclear Magnetic Resonance (Wiley, 2008).

  2. Schmidt-Rohr, K. & Spiess, H. W. Multidimensional Solid-State NMR and Polymers Vol. 478 (Academic, 1994).

  3. Facelli, J. C. Chemical shift tensors: theory and application to molecular structural problems. Prog. Nucl. Magn. Reson. Spectrosc. 58, 176–201 (2011).

    Article  Google Scholar 

  4. Keeler, J. Understanding NMR Spectroscopy (Wiley, 2011).

  5. Andrew, E. R., Bradbury, A. & Eades, R. G. Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature 182, 1659–1659 (1958).

    Article  ADS  Google Scholar 

  6. Schaefer, J. & Stejskal, E. O. C13 nuclear magnetic resonance of polymers spinning at magic angle. J. Am. Chem. Soc. 98, 1031–1032 (1976).

    Article  Google Scholar 

  7. Duer, M. J. Introduction to Solid-State NMR Spectroscopy (Blackwell Science, 2004).

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

    Article  Google Scholar 

  9. Tugarinov, V., Kanelis, V. & Kay, L. E. Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nat. Protoc. 1, 749–754 (2006).

    Article  Google Scholar 

  10. Kainosho, M. et al. Optimal isotope labelling for NMR protein structure determinations. Nature 440, 52–57 (2006).

    Article  ADS  Google Scholar 

  11. Lu, J. et al. Molecular structure of β-amyloid fibrils in Alzheimer’s disease brain tissue. Cell 154, 1257–1268 (2013). This paper describes the first structural determination of brain-derived Alzheimer disease Aβ fibrils using NMR spectroscopy and brain-seeded fibrils.

    Article  Google Scholar 

  12. Ashbrook, S. E. & Smith, M. E. Solid state O-17 NMR — an introduction to the background principles and applications to inorganic materials. Chem. Soc. Rev. 35, 718–735 (2006).

    Article  Google Scholar 

  13. Pines, A., Gibby, M. G. & Waugh, J. S. Proton-enhanced NMR of dilute spins in solids. J. Chem. Phys. 59, 569–590 (1973).

    Article  ADS  Google Scholar 

  14. Herzfeld, J. & Berger, A. E. Sideband intensities in NMR spectra of samples spinning at the magic angle. J. Chem. Phys. 73, 6021 (1980).

    Article  ADS  Google Scholar 

  15. Bielecki, A., Kolbert, A. C. & Levitt, M. H. Frequency-switched pulse sequences: homonuclear decoupling and dilute spin NMR in solids. Chem. Phys. Lett. 155, 341–346 (1989).

    Article  ADS  Google Scholar 

  16. Mote, K. R., Agarwal, V. & Madhu, P. K. Five decades of homonuclear dipolar decoupling in solid-state NMR: status and outlook. Prog. Nucl. Magn. Reson. Spectrosc. 97, 1–39 (2016).

    Article  Google Scholar 

  17. Paruzzo, F. M. & Emsley, L. High-resolution 1H NMR of powdered solids by homonuclear dipolar decoupling. J. Magn. Reson. 309, 106598 (2019).

    Article  Google Scholar 

  18. Perras, F. A., Goh, T. W., Wang, L. L., Huang, W. & Pruski, M. Enhanced 1H-X D-HMQC performance through improved 1H homonuclear decoupling. Solid State Nucl. Magn. Reson. 98, 12–18 (2019).

    Article  Google Scholar 

  19. Barbet-Massin, E. et al. Rapid proton-detected NMR assignment for proteins with fast magic angle spinning. J. Am. Chem. Soc. 136, 12489–12497 (2014).

    Article  Google Scholar 

  20. Takegoshi, K., Nakamura, S. & Terao, T. C-13–H-1 dipolar-assisted rotational resonance in magic-angle spinning NMR. Chem. Phys. Lett. 344, 631–637 (2001).

    Article  ADS  Google Scholar 

  21. Bax, A., Freeman, R. & Kempsell, S. P. Natural-abundance 13C–13C coupling observed via double-quantum coherence. J. Am. Chem. Soc. 102, 4849–4851 (1980).

    Article  Google Scholar 

  22. Lesage, A., Bardet, M. & Emsley, L. Through-bond carbon–carbon connectivities in disordered solids by NMR. J. Am. Chem. Soc. 121, 10987–10993 (1999).

    Article  Google Scholar 

  23. Harris, R. K. Applications of solid-state NMR to pharmaceutical polymorphism and related matters. J. Pharm. Pharmacol. 59, 225–239 (2007).

    Article  Google Scholar 

  24. King, I. J., Fayon, F., Massiot, D., Harris, R. K. & Evans, J. S. O. A space group assignment of ZrP2O7 obtained by P-31 solid state NMR. Chem. Commun. 18, 1766–1767 (2001).

    Article  Google Scholar 

  25. Cadars, S., Lesage, A. & Emsley, L. Chemical shift correlations in disordered solids. J. Am. Chem. Soc. 127, 4466–4476 (2005).

    Article  Google Scholar 

  26. De Paëpe, G. Dipolar recoupling in magic angle spinning solid-state nuclear magnetic resonance. Annu. Rev. Phys. Chem. 63, 661–684 (2012).

    Article  ADS  Google Scholar 

  27. Terao, T., Miura, H. & Saika, A. I–S dipolar switching-angle spinning 2D NMR (SLF). J. Chem. Phys. 85, 3816–3826 (1986).

    Article  ADS  Google Scholar 

  28. Mueller, K. T. et al. Dynamic-angle spinning of quadrupolar nuclei. J. Magn. Reson. 86, 470 (1990).

    ADS  Google Scholar 

  29. Apperley, D. C., Harris, R. K. & Hodgkinson, P. Solid-state NMR: Basic Principles and Practice (Momentum, 2012).

  30. Ashbrook, S. E. & Sneddon, S. New methods and applications in solid-state NMR spectroscopy of quadrupolar nuclei. J. Am. Chem. Soc. 136, 15440–15456 (2014).

    Article  Google Scholar 

  31. Gan, Z., Gor’kov, P., Cross, T. A., Samoson, A. & Massiot, D. Seeking higher resolution and sensitivity for NMR of quadrupolar nuclei at ultrahigh magnetic fields. J. Am. Chem. Soc. 124, 5634–5635 (2002).

    Article  Google Scholar 

  32. Frydman, L. & Harwood, J. S. Isotropic spectra of half-integer quadrupolar spins from bidimensional magic-angle-spinning NMR. J. Am. Chem. Soc. 117, 5367–5368 (1995). This paper revolutionizes the structural study of quadrupolar nuclei in many materials by removing the line broadening that affects the solid-state NMR spectra.

    Article  Google Scholar 

  33. Schurko, R. W. Ultra-wideline solid-state NMR spectroscopy. Acc. Chem. Res. 46, 1985–1995 (2013).

    Article  Google Scholar 

  34. Spiess, H. W. 2H NMR for studying mobility and orientation in polymers. Adv. Polym. Sci. 66, 23–56 (1985).

    Article  Google Scholar 

  35. Davis, J. H. The description of membrane lipid conformation, order and dynamics by 2H-NMR. Biochim. Biophys. Acta 737, 117–171 (1983).

    Article  Google Scholar 

  36. Petrache, H. I., Dodd, S. W. & Brown, M. F. Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by H-2 NMR spectroscopy. Biophys. J. 79, 3172–3192 (2000).

    Article  Google Scholar 

  37. Kamp, F. et al. Bexarotene binds to the amyloid precursor protein transmembrane domain, alters its α-helical conformation, and inhibits γ-secretase nonselectively in liposomes. ACS Chem. Neurosci. 9, 1702–1713 (2018).

    Article  Google Scholar 

  38. Hologne, M., Faelber, K., Diehl, A. & Reif, B. Characterization of dynamics of perdeuterated proteins by MAS solid-state NMR. J. Am. Chem. Soc. 127, 11208–11209 (2005).

    Article  Google Scholar 

  39. Shi, X. Y. & Rienstra, C. M. Site-specific internal motions in GB1 protein microcrystals revealed by 3D 2H–13C–13C solid-state NMR spectroscopy. J. Am. Chem. Soc. 138, 4105–4119 (2016).

    Article  Google Scholar 

  40. Gelenter, M. D., Wang, T., Liao, S. Y., O’Neill, H. & Hong, M. 2H–13C correlation solid-state NMR for investigating dynamics and water accessibilities of proteins and carbohydrates. J. Biomol. NMR 68, 257–270 (2017).

    Article  Google Scholar 

  41. Comellas, G. & Rienstra, C. M. Protein structure determination by magic-angle spinning solid-state NMR, and insights into the formation, structure, and stability of amyloid fibrils. Annu. Rev. Biophys. 42, 515–536 (2013).

    Article  Google Scholar 

  42. Chevelkov, V., Rehbein, K., Diehl, A. & Reif, B. Ultra-high resolution in proton solid-state NMR at high levels of deuteration. Angew. Chem. Int. Ed. 45, 3878–3881 (2006). This paper reports the first demonstration of high-resolution 1H correlation solid-state NMR spectra.

    Article  Google Scholar 

  43. Penzel, S. et al. Protein resonance assignment at MAS frequencies approaching 100 kHz: a quantitative comparison of J-coupling and dipolar-coupling-based transfer methods. J. Biomol. NMR 63, 165–186 (2015).

    Article  Google Scholar 

  44. Andreas, L. B. et al. Structure of fully protonated proteins by proton-detected magic-angle spinning NMR. Proc. Natl Acad. Sci. USA 113, 9187–9192 (2016). This paper describes the first de novo structure obtained from 1H-detected solid-state NMR experiments.

    Article  Google Scholar 

  45. Xiang, S. et al. Sequential backbone assignment based on dipolar amide-to-amide correlation experiments. J. Biomol. NMR 62, 303–311 (2015).

    Article  Google Scholar 

  46. Schanda, P., Huber, M., Verel, R., Ernst, M. & Meier, B. H. Direct detection of 3hJ(NC′) hydrogen-bond scalar couplings in proteins by solid-state NMR spectroscopy. Angew. Chem. Int. Ed. 48, 9322–9325 (2009).

    Article  Google Scholar 

  47. Hiller, S., Wasmer, C., Wider, G. & Wuthrich, K. Sequence-specific resonance assignment of soluble nonglobular proteins by 7D APSY-NMR spectroscopy. J. Am. Chem. Soc. 129, 10823–10828 (2007).

    Article  Google Scholar 

  48. Mobli, M. & Hoch, J. C. Nonuniform sampling and non-Fourier signal processing methods in multidimensional NMR. Prog. Nucl. Magn. Reson. Spectrosc. 83, 21–41 (2014).

    Article  Google Scholar 

  49. Paramasivam, S. et al. Enhanced sensitivity by nonuniform sampling enables multidimensional MAS NMR spectroscopy of protein assemblies. J. Phys. Chem. B 116, 7416–7427 (2012).

    Article  Google Scholar 

  50. Orton, H. W. et al. Protein NMR resonance assignment without spectral analysis: 5D solid-state automated projection spectroscopY (SO-APSY). Angew. Chem. Int. Ed. 59, 2380–2384 (2020).

    Article  Google Scholar 

  51. Schmidt, E. & Guntert, P. A new algorithm for reliable and general NMR resonance assignment. J. Am. Chem. Soc. 134, 12817–12829 (2012).

    Article  Google Scholar 

  52. Tycko, R. On the problem of resonance assignments in solid state NMR of uniformly N-15, C-13-labeled proteins. J. Magn. Reson. 253, 166–172 (2015).

    Article  ADS  Google Scholar 

  53. Stanek, J. et al. Automated backbone NMR resonance assignment of large proteins using redundant linking from a single simultaneous acquisition. J. Am. Chem. Soc. 142, 5793–5799 (2020).

    Article  Google Scholar 

  54. Hong, M. & Schmidt-Rohr, K. Magic-angle-spinning NMR techniques for measuring long-range distances in biological macromolecules. Acc. Chem. Res. 46, 2154–2163 (2013).

    Article  Google Scholar 

  55. Castellani, F. et al. Structure of a protein determined by solid-state magic-angle spinning NMR spectroscopy. Nature 420, 98–102 (2002). This report demonstrates the first complete protein structure determined by solid-state NMR spectroscopy.

    Article  ADS  Google Scholar 

  56. Grommek, A., Meier, B. H. & Ernst, M. Distance information from proton-driven spin diffusion under MAS. Chem. Phys. Lett. 427, 404–409 (2006).

    Article  ADS  Google Scholar 

  57. Linser, R., Bardiaux, B., Higman, V., Fink, U. & Reif, B. 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, 5905–5912 (2011).

    Article  Google Scholar 

  58. Roos, M., Wang, T., Shcherbakov, A. A. & Hong, M. Fast magic-angle-spinning 19F spin exchange NMR for determining nanometer 19F–19F distances in proteins and phamaceutical compounds. J. Phys. Chem. B 122, 2900–2911 (2018).

    Article  Google Scholar 

  59. Gullion, T. & Schaefer, J. Rotational echo double resonance NMR. J. Magn. Reson. 81, 196–200 (1989).

    ADS  Google Scholar 

  60. Cegelski, L. REDOR NMR for drug discovery. Bioorg. Med. Chem. Lett. 23, 5767–5775 (2013).

    Article  Google Scholar 

  61. Jaroniec, C. P., Filip, C. & Griffin, R. G. 3D TEDOR NMR experiments for the simultaneous measurement of multiple carbon–nitrogen distances in uniformly 13C, 15N-labeled solids. J. Am. Chem. Soc. 124, 10728–10742 (2002).

    Article  Google Scholar 

  62. Tang, M., Waring, A. J. & Hong, M. Phosphate-mediated arginine insertion into lipid membranes and pore formation by a cationic membrane peptide from solid-state NMR. J. Am. Chem. Soc. 129, 11438–11446 (2007).

    Article  Google Scholar 

  63. Yang, H. et al. REDOR NMR reveals multiple conformers for a protein kinase C ligand in a membrane environment. ACS Cent. Sci. 4, 89–96 (2018).

    Article  Google Scholar 

  64. Elkins, M. R. et al. Cholesterol-binding site of the influenza M2 protein in lipid bilayers from solid-state NMR. Proc. Natl Acad. Sci. USA 114, 12946–12951 (2017).

    Article  Google Scholar 

  65. Brus, J. et al. Structure of framework aluminum Lewis sites and perturbed aluminum atoms in zeolites as determined by 27Al{1H} REDOR (3Q) MAS NMR spectroscopy and DFT/molecular mechanics. Angew. Chem. Int. Ed. Engl. 54, 541–545 (2015).

    Google Scholar 

  66. Peng, L., Liu, Y., Kim, N., Readman, J. E. & Grey, C. P. Detection of Brønsted acid sites in zeolite HY with high-field 17O-MAS-NMR techniques. Nat. Mater. 4, 216–219 (2005).

    Article  ADS  Google Scholar 

  67. Shcherbakov, A. A. & Hong, M. Rapid measurement of long-range distances in proteins by multidimensional 13C–19F REDOR NMR under fast magic-angle spinning. J. Biomol. NMR 71, 31–43 (2018).

    Article  Google Scholar 

  68. Shcherbakov, A. A., Mandala, V. S. & Hong, M. High-sensitivity detection of nanometer 1H–19F distances for protein structure determination by 1H-detected fast MAS NMR. J. Phys. Chem. B 123, 4387–4391 (2019).

    Article  Google Scholar 

  69. Wang, M. et al. Fast magic angle spinning 19F NMR of HIV-1 capsid protein assemblies. Angew. Chem. Int. Ed. 57, 16375–16379 (2018).

    Article  Google Scholar 

  70. Ruiz-Preciado, M. A. et al. Supramolecular modulation of hybrid perovskite solar cells via bifunctional halogen bonding revealed by two-dimensional 19F solid-state NMR spectroscopy. J. Am. Chem. Soc. 142, 1645–1654 (2020).

    Article  Google Scholar 

  71. Gilchrist, M. L. Jr et al. Measurement of interfluorine distances in solids. J. Magn. Reson. 152, 1–6 (2001).

    Article  ADS  Google Scholar 

  72. Steigel, A. & Spiess, H. W. Dynamic NMR Spectroscopy (Springer Verlag, 1978).

  73. Geahigan, K. B., Meints, G. A., Hatcher, M. E., Orban, J. & Drobny, G. P. The dynamic impact of CpG methylation in DNA. Biochemistry 39, 4939–4946 (2000).

    Article  Google Scholar 

  74. Copié, V. et al. Deuterium solid-state nuclear magnetic resonance studies of methyl group dynamics in bacteriorhodopsin and retinal model compounds: evidence for a 6-s-trans chromophore in the protein. Biochemistry 33, 3280–3286 (1994).

    Article  Google Scholar 

  75. Munowitz, M. G., Griffin, R. G., Bodenhausen, G. & Huang, T. H. Two-dimensional rotational spin-echo NMR in solids: correlation of chemical shift and dipolar interactions. J. Am. Chem. Soc. 103, 2529–2533 (1981).

    Article  Google Scholar 

  76. Hong, M. et al. Coupling amplification in 2D MAS NMR and its application to torsion angle determination in peptides. J. Magn. Reson. 129, 85–92 (1997).

    Article  ADS  Google Scholar 

  77. deAzevedo, E. R. et al. Intermediate motions as studied by solid-state separated local field NMR experiments. J. Chem. Phys. 128, 104505 (2008).

    Article  ADS  Google Scholar 

  78. Hohwy, M., Jaroniec, C. P., Reif, B., Rienstra, C. M. & Griffin, R. G. Determination of local structure and relaxation properties in solid-state NMR: accurate measurement of amide N–H bond lengths and H–N–H bond angles. J. Am. Chem. Soc. 122, 3218–3219 (2000).

    Article  Google Scholar 

  79. Hou, G. J., Lu, X. Y., Vega, A. J. & Polenova, T. Accurate measurement of heteronuclear dipolar couplings by phase-alternating R-symmetry (PARS) sequences in magic angle spinning NMR spectroscopy. J. Chem. Phys. 141, e104202 (2014).

    Article  ADS  Google Scholar 

  80. van Rossum, B.-J., de Groot, C. P., Ladizhansky, V., Vega, S. & de Groot, H. J. M. A method for measuring heteronuclear (1H–13C) distances in high speed MAS NMR. J. Am. Chem. Soc. 122, 3465–3472 (2000).

    Article  Google Scholar 

  81. Schanda, P., Huber, M., Boisbouvier, J., Meier, B. H. & Ernst, M. Solid-state NMR measurements of asymmetric dipolar couplings provide insight into protein side-chain motion. Angew. Chem. Int. Ed. 50, 11005–11009 (2011).

    Article  Google Scholar 

  82. Asami, S. & Reif, B. Comparative study of REDOR and CPPI derived order parameters by 1H-detected MAS NMR and MD simulations. J. Phys. Chem. B 121, 8719–8730 (2017).

    Article  Google Scholar 

  83. Xue, K., Mühlbauer, M., Mamone, S., Sarkar, R. & Reif, B. Accurate determination of 1H–15N dipolar couplings using inaccurate settings of the magic angle in solid-state NMR spectroscopy. Angew. Chem. Int. Ed. 58, 4286–4290 (2019).

    Article  Google Scholar 

  84. Paluch, P. et al. Theoretical study of CP-VC: a simple, robust and accurate MAS NMR method for analysis of dipolar C–H interactions under rotation speeds faster than ca. 60 kHz. J. Magn. Res. 252, 67–77 (2015).

    Article  ADS  Google Scholar 

  85. deAzevedo, E. R., Bonagamba, T. J., Hu, W. & Schmidt-Rohr, K. Centerband-only detection of exchange: efficient analysis of dynamics in solids by NMR. J. Am. Chem. Soc. 121, 8411–8412 (1999).

    Article  Google Scholar 

  86. Krushelnitsky, A. et al. Direct observation of millisecond to second motions in proteins by dipolar CODEX NMR spectroscopy. J. Am. Chem. Soc. 131, 12097–12099 (2009).

    Article  Google Scholar 

  87. Giraud, N. et al. Quantitative analysis of backbone dynamics in a crystalline protein from nitrogen-15 spin-lattice relaxation. J. Am. Chem. Soc. 127, 18190–18201 (2005).

    Article  Google Scholar 

  88. Chevelkov, V., Diehl, A. & Reif, B. Measurement of 15N-T1 relaxation rates in a perdeuterated protein by MAS solid-state NMR spectroscopy. J. Chem. Phys. 128, 052316 (2008).

    Article  ADS  Google Scholar 

  89. Lewandowski, J. R., Sass, H. J., Grzesiek, S., Blackledge, M. & Emsley, L. Site-specific measurement of slow motions in proteins. J. Am. Chem. Soc. 133, 16762–16765 (2011).

    Article  Google Scholar 

  90. Rovo, P. & Linser, R. Microsecond timescale protein dynamics: a combined solid-state NMR approach. ChemPhysChem 19, 34–39 (2018).

    Article  Google Scholar 

  91. Marion, D., Gauto, D. F., Ayala, I., Giandoreggio-Barranco, K. & Schanda, P. Microsecond protein dynamics from combined Bloch–McConnell and near-rotary-resonance R1p relaxation-dispersion MAS NMR. ChemPhysChem 20, 276–284 (2019).

    Article  Google Scholar 

  92. Giraud, N., Blackledge, M., Böckmann, A. & Emsley, L. The influence of nitrogen-15 proton-driven spin diffusion on the measurement of nitrogen-15 longitudinal relaxation times. J. Magn. Reson. 184, 51–61 (2007).

    Article  ADS  Google Scholar 

  93. Phan, V., Fry, E. A. & Zilm, K. W. Accounting for the temperature dependence of C-13 spin-lattice relaxation of methyl groups in the glycyl-alanyl-leucine model system under MAS with spin diffusion. J. Biomol. NMR 73, 411–421 (2019).

    Article  Google Scholar 

  94. Kirchhain, H. & van Wullen, L. Solid state NMR at very high temperatures. Prog. Nucl. Magn. Reson. Spectrosc. 114, 71–85 (2019).

    Article  Google Scholar 

  95. Meier, T. et al. NMR at pressures up to 90 GPa. J. Magn. Res. 292, 44–47 (2018).

    Article  ADS  Google Scholar 

  96. Chamas, A. et al. High temperature/pressure MAS-NMR for the study of dynamic processes in mixed phase systems. Magn. Reson. Imaging 56, 37–44 (2019).

    Article  Google Scholar 

  97. Overhauser, A. W. Polarization of nuclei in metals. Phys. Rev. 92, 411–415 (1953).

    Article  ADS  MATH  Google Scholar 

  98. Carver, T. R. & Slichter, C. P. Polarization of nuclear spins in metals. Phys. Rev. 92, 212–213 (1953).

    Article  ADS  Google Scholar 

  99. Ni, Q. Z. et al. High frequency dynamic nuclear polarization. Acc. Chem. Res. 46, 1933–1941 (2013).

    Article  Google Scholar 

  100. Lilly Thankamony, A. S., Wittmann, J. J., Kaushik, M. & Corzilius, B. Dynamic nuclear polarization for sensitivity enhancement in modern solid-state NMR. Prog. Nucl. Magn. Reson. Spectrosc. 102–103, 120–195 (2017).

    Article  Google Scholar 

  101. Bajaj, V. S. et al. Dynamic nuclear polarization at 9 T using a novel 250 GHz gyrotron microwave source. J. Magn. Reson. 160, 85–90 (2003).

    Article  ADS  Google Scholar 

  102. Rossini, A. J. et al. Dynamic nuclear polarization surface enhanced NMR spectroscopy. Acc. Chem. Res. 46, 1942–1951 (2013).

    Article  Google Scholar 

  103. Lesage, A. et al. Surface enhanced NMR spectroscopy by dynamic nuclear polarization. J. Am. Chem. Soc. 132, 15459–15461 (2010). This is the first paper introducing impregnation DNP and showing how it can enable the study of surface structures of materials, using nanoporous silica material as an example.

    Article  Google Scholar 

  104. Sauvée, C. et al. Highly efficient, water-soluble polarizing agents for dynamic nuclear polarization at high frequency. Angew. Chem. Int. Ed. Engl. 52, 10858–10861 (2013).

    Article  Google Scholar 

  105. Zagdoun, A. et al. Large molecular weight nitroxide biradicals providing efficient dynamic nuclear polarization at temperatures up to 200 K. J. Am. Chem. Soc. 135, 12790–12797 (2013).

    Article  Google Scholar 

  106. Bertini, I., Luchinat, C., Parigi, G. & Ravera, E. NMR of Paramagnetic Molecules: Applications to Metallobiomolecules and Models 2nd edn (Elsevier Science BV, 2017).

  107. Pell, A. J., Pintacuda, G. & Grey, C. P. Paramagnetic NMR in solution and the solid state. Prog. Nucl. Magn. Reson. Spectrosc. 111, 1–271 (2019).

    Article  Google Scholar 

  108. Solomon, I. Relaxation processes in a system of two spins. Phys. Rev. 99, 559–565 (1955).

    Article  ADS  Google Scholar 

  109. Buffy, J. J. et al. Solid-state NMR investigation of the depth of insertion of protegin-1 in lipid bilayers using paramagnetic Mn2+. Biophys. J. 85, 2363–2373 (2003).

    Article  ADS  Google Scholar 

  110. Parthasarathy, S. et al. Molecular-level examination of Cu2+ binding structure for amyloid fibrils of 40-residue Alzheimer’s β by solid-state NMR spectroscopy. J. Am. Chem. Soc. 133, 3390–3400 (2011).

    Article  Google Scholar 

  111. Nadaud, P. S., Helmus, J. J., Sengupta, I. & Jaroniec, C. P. Rapid acquisition of multidimensional solid-state NMR spectra of proteins facilitated by covalently bound paramagnetic tags. J. Am. Chem. Soc. 132, 9561–9563 (2010).

    Article  Google Scholar 

  112. Öster, C. et al. Characterization of protein–protein interfaces in large complexes by solid-state NMR solvent paramagnetic relaxation enhancements. J. Am. Chem. Soc. 139, 12165–12174 (2017).

    Article  Google Scholar 

  113. Knight, M. J. et al. Structure and backbone dynamics of a microcrystalline metalloprotein by solid-state NMR. Proc. Natl Acad. Sci. USA 109, 11095–11100 (2012).

    Article  ADS  Google Scholar 

  114. Wickramasinghe, N. P. et al. Nanomole-scale protein solid-state NMR by breaking intrinsic 1HT1 boundaries. Nat. Methods 6, 215–218 (2009).

    Article  Google Scholar 

  115. Wu, X. L. & Zilm, K. W. Complete spectral editing in CPMAS NMR. J. Magn. Reson. A 102, 205–213 (1993).

    Article  ADS  Google Scholar 

  116. Schmidt-Rohr, K. & Mao, J. D. Efficient CH-group selection and identification in C-13 solid-state NMR by dipolar DEPT and H-1 chemical-shift filtering. J. Am. Chem. Soc. 124, 13938–13948 (2002).

    Article  Google Scholar 

  117. Mao, J. D. & Schmidt-Rohr, K. Methylene spectral editing in solid-state C-13 NMR by three-spin coherence selection. J. Magn. Reson. 176, 1–6 (2005).

    Article  ADS  Google Scholar 

  118. Rienstra, C. M., Hohwy, M., Hong, M. & Griffin, R. G. 2D and 3D 15N–13C–13C NMR chemical shift correlation spectroscopy of solids: assignment of MAS spectra of peptides. J. Am. Chem. Soc. 122, 10979–10990 (2000).

    Article  Google Scholar 

  119. Baldus, M., Petkova, A. T., Herzfeld, J. & Griffin, R. G. Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems. Mol. Phys. 95, 1197–1207 (1998).

    Article  ADS  Google Scholar 

  120. Pauli, J., Baldus, M., Van Rossum, B.-J., De Groot, H. & Oschkinat, H. Backbone and side-chain 13C and 15N signal assignments of the α-spectrin SH3 domain by magic-angle spinning solid-state NMR at 17.6 Tesla. ChemBioChem 2, 272–281 (2001).

    Article  Google Scholar 

  121. De Paëpe, G., Lewandowski, J. R., Loquet, A., Böckmann, A. & Griffin, R. G. Proton assisted recoupling and protein structure determination. J. Chem. Phys. 129, 245101 (2008).

    Article  ADS  Google Scholar 

  122. Gelenter, M. D. & Hong, M. Efficient 15N–13C polarization transfer by third-spin-assisted pulsed cross-polarization magic-angle-spinning NMR for protein structure determination. J. Phys. Chem. B 122, 8367–8379 (2018).

    Article  Google Scholar 

  123. Ishii, Y. C-13–C-13 dipolar recoupling under very fast magic angle spinning in solid-state nuclear magnetic resonance: applications to distance measurements, spectral assignments, and high-throughput secondary-structure determination. J. Chem. Phys. 114, 8473–8483 (2001).

    Article  ADS  Google Scholar 

  124. Jaroniec, C. P., Tounge, B. A., Rienstra, C. M., Herzfeld, J. & Griffin, R. G. Recoupling of heteronuclear dipolar interactions with rotational-echo double-resonance at high magic-angle spinning frequencies. J. Magn. Reson. 146, 132–139 (2000).

    Article  ADS  Google Scholar 

  125. Su, Y., Hu, F. & Hong, M. Paramagnetic Cu(II) for probing membrane protein structure and function: inhibition mechanism of the influenza M2 proton channel. J. Am. Chem. Soc. 134, 8693–8702 (2012).

    Article  Google Scholar 

  126. Theint, T. et al. Structural studies of amyloid fibrils by paramagnetic solid-state nuclear magnetic resonance spectroscopy. J. Am. Chem. Soc. 140, 13161–13166 (2018).

    Article  Google Scholar 

  127. Su, Y., Mani, R. & Hong, M. Asymmetric insertion of membrane proteins in lipid bilayers by solid-state NMR paramagnetic relaxation enhancement: a cell-penetrating peptide example. J. Am. Chem. Soc. 130, 8856–8864 (2008).

    Article  Google Scholar 

  128. Mandala, V. S., Loftis, A. R., Shcherbakov, A. A., Pentelute, B. L. & Hong, M. Atomic structures of closed and open influenza B M2 proton channel reveal the conduction mechanism. Nat. Struc. Mol. Biol. 27, 160–167 (2020).

    Article  Google Scholar 

  129. Das, B. B. et al. Structure determination of a membrane protein in proteoliposomes. J. Am. Chem. Soc. 134, 2047–2056 (2012).

    Article  Google Scholar 

  130. Phyo, P. et al. Gradients in wall mechanics and polysaccharides along growing inflorescence stems. Plant Physiol. 175, 1593–1607 (2017).

    Article  Google Scholar 

  131. Williams, J. K., Zhang, Y., Schmidt-Rohr, K. & Hong, M. pH-dependent conformation, dynamics, and aromatic interaction of the gating tryptophan residue of the influenza M2 proton channel from solid-state NMR. Biophys. J. 104, 1698–1708 (2013).

    Article  ADS  Google Scholar 

  132. Chevelkov, V., Fink, U. & Reif, B. Accurate determination of order parameters from 1H,15N dipolar couplings in MAS solid-state NMR experiments. J. Am. Chem. Soc. 131, 14018–14022 (2009).

    Article  Google Scholar 

  133. Schanda, P., Meier, B. H. & Ernst, M. Quantitative analysis of protein backbone dynamics in microcrystalline ubiquitin by solid-state NMR spectroscopy. J. Am. Chem. Soc. 132, 15957–15967 (2010).

    Article  Google Scholar 

  134. Ma, P. X. et al. Observing the overall rocking motion of a protein in a crystal. Nat. Commun. 6, e8361 (2015).

    Article  ADS  Google Scholar 

  135. Lewandowski, J. R., Sein, J., Blackledge, M. & Emsley, L. Anisotropic collective motion contributes to nuclear spin relaxation in crystalline proteins. J. Am. Chem. Soc. 132, 1246-+ (2010).

    Article  Google Scholar 

  136. Lewandowski, J. R., Halse, M. E., Blackledge, M. & Emsley, L. Protein dynamics. Direct observation of hierarchical protein dynamics. Science 348, 578–581 (2015). This study provides a quantitative analysis of the coupling of protein and solvent dynamics using relaxation NMR spectroscopy.

    Article  ADS  Google Scholar 

  137. Smith, A. A., Ernst, M., Riniker, S. & Meier, B. H. Localized and collective motions in HET-s(218–289) fibrils from combined NMR relaxation and MD simulation. Angew. Chem. Int. Ed. 58, 9383–9388 (2019).

    Article  Google Scholar 

  138. Shannon, M. D. et al. Conformational dynamics in the core of human Y145Stop prion protein amyloid probed by relaxation dispersion NMR. ChemPhysChem 20, 311–317 (2019).

    Article  Google Scholar 

  139. Gauto, D. F. et al. Aromatic ring dynamics, thermal activation, and transient conformations of a 468 kDa enzyme by specific H-1–C-13 labeling and fast magic-angle spinning NMR. J. Am. Chem. Soc. 141, 11183–11195 (2019).

    Article  Google Scholar 

  140. Wasylishen, R. E., Ashbrook, S. E. & Wimperis, S. NMR of Quadrupolar Nuclei in Solid Materials (Wiley, 2012).

  141. Massiot, D. et al. Modelling one- and two-dimensional solid-state NMR spectra. Magn. Reson. Chem. 40, 70–76 (2002).

    Article  Google Scholar 

  142. Bak, M., Rasmussen, J. T. & Nielsen, N. C. SIMPSON: a general simulation program for solid-state NMR spectroscopy. J. Magn. Res. 147, 296–330 (2000).

    Article  ADS  Google Scholar 

  143. Ashbrook, S. E., Berry, A. J. & Wimperis, S. O-17 multiple-quantum MAS NMR study of pyroxenes. J. Phys. Chem. B 106, 773–778 (2002).

    Article  Google Scholar 

  144. Frydman, L. & Harwood, J. S. Isotropic spectra of half-integer quadrupolar spins from bidimensional magic-angle-spinning NMR. J. Am. Chem. Soc. 117, 5367–5368 (1995).

    Article  Google Scholar 

  145. Goldbourt, A. & Madhu, P. K. Multiple-quantum magic-angle spinning: high-resolution solid-state NMR of half-integer spin quadrupolar nuclei. Annu. Rep. NMR Spec. 54, 81–153 (2005).

    Google Scholar 

  146. Moran, R. F., Dawson, D. M. & Ashbrook, S. E. Exploiting NMR spectroscopy for the study of disorder in solids. Int. Rev. Phys. Chem. 36, 39–115 (2017).

    Article  Google Scholar 

  147. Le Caer, G., Bureau, B. & Massiot, D. An extension of the Czjzek model for the distributions of electric field gradients in disordered solids and an application to NMR spectra of Ga-71 in chalcogenide glasses. J. Phys. Condens. Matter 22, 065402 (2010).

    Article  ADS  Google Scholar 

  148. Trease, N. M., Clark, T. M., Grandinetti, P. J., Stebbins, J. F. & Sen, S. Bond length-bond angle correlation in densified silica-results from O-17 NMR spectroscopy. J. Chem. Phys. 146, 184505 (2017).

    Article  ADS  Google Scholar 

  149. Ashbrook, S. E. & McKay, D. Combining solid-state NMR spectroscopy with first-principles calculations — a guide to NMR crystallography. Chem. Commun. 52, 7186–7204 (2016). This review describes how to use computational prediction of NMR interactions and NMR parameters alongside experiments to help interpret and assign complex spectral signals, thereby gaining more detailed structural insight.

    Article  Google Scholar 

  150. Bonhomme, C. et al. First-principles calculation of NMR parameters using the gauge including projector augmented wave method: a chemist’s point of view. Chem. Rev. 112, 5733–5779 (2012).

    Article  Google Scholar 

  151. Pickard, C. J. & Mauri, F. All-electron magnetic response with pseudopotentials: NMR chemical shifts. Phys. Rev. B 63, 245101 (2001). This paper establishes the framework for accurate calculation of chemical shifts in periodic solids.

    Article  ADS  Google Scholar 

  152. Caulkins, B. G. et al. NMR crystallography of a carbanionic intermediate in tryptophan synthase: chemical structure, tautomerization, and reaction specificity. J. Am. Chem. Soc. 138, 15214–15226 (2016).

    Article  Google Scholar 

  153. Baias, M. et al. De novo determination of the crystal structure of a large drug molecule by crystal structure prediction-based powder NMR crystallography. J. Am. Chem. Soc. 135, 17501–17507 (2013).

    Article  Google Scholar 

  154. Cadars, S. et al. Long- and short-range constraints for the structure determination of layered silicates with stacking disorder. Chem. Mater. 26, 6994–7008 (2014).

    Article  Google Scholar 

  155. Charpentier, T., Menziani, M. C. & Pedone, A. Computational simulations of solid state NMR spectra: a new era in structure determination of oxide glasses. RSC Adv. 3, 10550–10578 (2013).

    Article  Google Scholar 

  156. Cady, S. D. et al. Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463, 689–692 (2010). This study demonstrates the first determination of the structure and dynamics of a pharmaceutical drug bound to a membrane protein.

    Article  ADS  Google Scholar 

  157. Sharma, M. et al. Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer. Science 330, 509–512 (2010).

    Article  ADS  Google Scholar 

  158. Lange, A. et al. Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440, 959–962 (2006). This study shows how high-affinity binding of the scorpion toxin to a chimeric K+ channel is associated with significant structural rearrangements in both molecules, which explains the high specificity of toxin–K+ channel interactions.

    Article  ADS  Google Scholar 

  159. Wylie, B. J., Bhate, M. P. & McDermott, A. E. Transmembrane allosteric coupling of the gates in a potassium channel. Proc. Natl Acad. Sci. USA 111, 185–190 (2014).

    Article  ADS  Google Scholar 

  160. Öster, C. et al. The conduction pathway of potassium channels is water free under physiological conditions. Sci. Adv. 5, eaaw6756 (2019).

    Article  ADS  Google Scholar 

  161. Gayen, A., Leninger, M. & Traaseth, N. J. Protonation of a glutamate residue modulates the dynamics of the drug transporter EmrE. Nat. Chem. Biol. 12, 141–145 (2016).

    Article  Google Scholar 

  162. Lehnert, E. et al. Antigenic peptide recognition on the human ABC transporter TAP resolved by DNP-enhanced solid-state NMR spectroscopy. J. Am. Chem. Soc. 138, 13967–13974 (2016).

    Article  Google Scholar 

  163. Lalli, D. et al. Proton-based structural analysis of a heptahelical transmembrane protein in lipid bilayers. J. Am. Chem. Soc. 139, 13006–13012 (2017).

    Article  Google Scholar 

  164. Wang, S. L. et al. Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nat. Methods 10, 1007-–1012 (2013).

    Article  Google Scholar 

  165. Retel, J. S. et al. Structure of outer membrane protein G in lipid bilayers. Nat. Commun. 8, 2073 (2017).

    Article  ADS  Google Scholar 

  166. Medeiros-Silva, J. et al. High-resolution NMR studies of antibiotics in cellular membranes. Nat. Commun. 9, 3963 (2018).

    Article  ADS  Google Scholar 

  167. Amani, R. et al. Conformational changes upon gating of KirBac1.1 into an open-activated state revealed by solid-state NMR and functional assays. Proc. Natl Acad. Sci. USA 117, 2938–2947 (2020).

    Article  Google Scholar 

  168. Mandala, V. S., Gelenter, M. D. & Hong, M. Transport-relevant protein conformational dynamics and water dynamics on multiple time scales in an Archetypal proton channel: insights from solid-state NMR. J. Am. Chem. Soc. 140, 1514–1524 (2018).

    Article  Google Scholar 

  169. Spadaccini, R., Kaur, H., Becker-Baldus, J. & Glaubitz, C. The effect of drug binding on specific sites in transmembrane helices 4 and 6 of the ABC exporter MsbA studied by DNP-enhanced solid-state NMR. Biochim. Biophys. Acta 1860, 833–840 (2018).

    Article  Google Scholar 

  170. Maciejko, J., Kaur, J., Becker-Baldus, J. & Glaubitz, C. Photocycle-dependent conformational changes in the proteorhodopsin cross-protomer Asp-His-Trp triad revealed by DNP-enhanced MAS-NMR. Proc. Natl Acad. Sci. USA 116, 8342–8349 (2019).

    Article  Google Scholar 

  171. Becker-Baldus, J. et al. Enlightening the photoactive site of channelrhodopsin-2 by DNP-enhanced solid-state NMR spectroscopy. Proc. Natl Acad. Sci. USA 112, 9896–9901 (2015).

    Article  ADS  Google Scholar 

  172. Ni, Q. Z. et al. Primary transfer step in the light-driven ion pump bacteriorhodopsin: an irreversible U-turn revealed by dynamic nuclear polarization-enhanced magic angle spinning NMR. J. Am. Chem. Soc. 140, 4085–4091 (2018).

    Article  Google Scholar 

  173. Good, D., Pham, C., Jagas, J., Lewandowski, J. R. & Ladizhansky, V. Solid-state NMR provides evidence for small-amplitude slow domain motions in a multispanning transmembrane α-helical protein. J. Am. Chem. Soc. 139, 9246–9258 (2017).

    Article  Google Scholar 

  174. Tycko, R. Amyloid polymorphism: structural basis and neurobiological relevance. Neuron 86, 632–645 (2015).

    Article  Google Scholar 

  175. Xiao, Y. L. et al. A β 1–42 fibril structure illuminates self-recognition and replication of amyloid in Alzheimer’s disease. Nat. Struct. Mol. Biol. 22, 499–505 (2015).

    Article  Google Scholar 

  176. Colvin, M. T. et al. Atomic resolution structure of monomorphic Aβ42 amyloid fibrils. J. Am. Chem. Soc. 138, 9663–9674 (2016). This paper determines an atomic resolution structure of a monomorphic form of Aβ42 amyloid fibrils, which is essential to the aetiology of Alzheimer disease.

    Article  Google Scholar 

  177. Wälti, M. A. et al. Atomic-resolution structure of a disease-relevant Aβ1–42 amyloid fibril. Proc. Natl Acad. Sci. USA 113, E4976–E4984 (2016).

    Article  Google Scholar 

  178. Bousset, L. et al. Structural and functional characterization of two α-synuclein strains. Nat. Commun. 4, 2575 (2013).

    Article  ADS  Google Scholar 

  179. Tuttle, M. D. et al. Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein. Nat. Struct. Mol. Biol. 23, 409–415 (2016).

    Article  Google Scholar 

  180. Fitzpatrick, A. W. et al. Atomic structure and hierarchical assembly of a cross-β amyloid fibril. Proc. Natl Acad. Sci. USA 110, 5468–5473 (2013).

    Article  ADS  Google Scholar 

  181. Iadanza, M. G. et al. The structure of a β2-microglobulin fibril suggests a molecular basis for its amyloid polymorphism. Nat. Commun. 9, 1–10 (2018).

    Article  Google Scholar 

  182. Murray, D. T. et al. Structure of FUS protein fibrils and its relevance to self-assembly and phase separation of low-complexity domains. Cell 171, 615–627 (2017).

    Article  Google Scholar 

  183. Dregni, A. J. et al. In vitro 0N4R tau fibrils contain a monomorphic b-sheet core enclosed by dynamically heterogeneous fuzzy coat segments. Proc. Natl Acad. Sci. USA 116, 16357–16366 (2019).

    Article  Google Scholar 

  184. Piehl, D. W. et al. Immunoglobulin light chains form an extensive and highly ordered fibril involving the N- and C-termini. ACS Omega 2, 712–720 (2017).

    Article  Google Scholar 

  185. Hora, M. et al. Antibody light chain fibrils are similar to oligomeric precursors. PLoS ONE 12, e0181799 (2017).

    Article  Google Scholar 

  186. Prade, E. et al. Structural mechanism of the interaction of Alzheimer’s disease Aβ fibrils with the non-steroidal anti-inflammatory drug (NSAID) sulindac sulfide. J. Biol. Chem. 290, 28737–28745 (2015).

    Article  Google Scholar 

  187. Lopez del Amo, J.-M. et al. Structural properties of EGCG induced, non-toxic Alzheimer’s disease Aβ oligomers. J. Mol. Biol. 421, 517–524 (2012).

    Article  Google Scholar 

  188. Chimon, S. et al. Evidence of fibril-like β-sheet structures in a neurotoxic amyloid intermediate of Alzheimer’s β-amyloid. Nat. Struct. Mol. Biol. 14, 1157–1164 (2007).

    Article  Google Scholar 

  189. Qiang, W., Yau, W. M. & Schulte, J. Fibrillation of β amyloid peptides in the presence of phospholipid bilayers and the consequent membrane disruption. Biochim. Biophys. Acta 1848, 266–276 (2015).

    Article  Google Scholar 

  190. Fusco, G. et al. Direct observation of the three regions in α-synuclein that determine its membrane-bound behaviour. Nat. Commun. 5, 3827 (2014).

    Article  ADS  Google Scholar 

  191. Wang, T., Jo, H., DeGrado, W. F. & Hong, M. Water distribution, dynamics, and interactions with Alzheimer’s β-amyloid fibrils investigated by solid-state NMR. J. Am. Chem. Soc. 139, 6242–6252 (2017).

    Article  Google Scholar 

  192. Murray, D. T. & Tycko, R. Side chain hydrogen-bonding interactions within amyloid-like fibrils formed by the low-complexity domain of FUS: evidence from solid state nuclear magnetic resonance spectroscopy. Biochemistry 59, 364–378 (2020).

    Article  Google Scholar 

  193. Dregni, A. J., Duan, P. & Hong, M. Hydration and dynamics of full-length tau amyloid fibrils investigated by solid-state nuclear magnetic resonance. Biochemistry 59, 2237–2248 (2020).

    Article  Google Scholar 

  194. Wasmer, C. et al. Amyloid fibrils of the HET-s(218–289) prion form a β solenoid with a triangular hydrophobic core. Science 319, 1523–1526 (2008).

    Article  ADS  Google Scholar 

  195. Gelenter, M. D. et al. The peptide hormone glucagon forms amyloid fibrils with two coexisting β-strand conformations. Nat. Struct. Mol. Biol. 26, 592–598 (2019).

    Article  Google Scholar 

  196. Nespovitaya, N. et al. Dynamic assembly and disassembly of functional β-endorphin amyloid fibrils. J. Am. Chem. Soc. 138, 846–856 (2016).

    Article  Google Scholar 

  197. Bertini, I. et al. Solid-state NMR of proteins sedimented by ultracentrifugation. Proc. Natl Acad. Sci. USA 108, 10396–10399 (2011).

    Article  ADS  Google Scholar 

  198. Yan, S. et al. Atomic-resolution structure of the CAP-Gly domain of dynactin on polymeric microtubules determined by magic angle spinning NMR spectroscopy. Proc. Natl Acad. Sci. USA 112, 14611–14616 (2015).

    Article  ADS  Google Scholar 

  199. Lu, M. et al. Dynamic allostery governs cyclophilin A-HIV capsid interplay. Proc. Natl Acad. Sci. USA 112, 14617–14622 (2015).

    Article  ADS  Google Scholar 

  200. Mainz, A. et al. NMR spectroscopy of soluble protein complexes at one mega-dalton and beyond. Angew. Chem. Int. Ed. 52, 8746–8751 (2013).

    Article  Google Scholar 

  201. Kurauskas, V. et al. Sensitive proton-detected solid-state NMR spectroscopy of large proteins with selective CH3 labelling: application to the 50S ribosome subunit. Chem. Commun. 52, 9558–9561 (2016).

    Article  Google Scholar 

  202. Mainz, A. et al. The chaperone αB-crystallin uses different interfaces to capture an amorphous and an amyloid client. Nat. Struct. Mol. Biol. 22, 898–905 (2015).

    Article  Google Scholar 

  203. Felix, J. et al. Mechanism of the allosteric activation of the ClpP protease machinery by substrates and active-site inhibitors. Sci. Adv. 5, eaaw3818 (2019).

    Article  ADS  Google Scholar 

  204. Knight, M. J. et al. Rapid measurement of pseudocontact shifts in metalloproteins by proton-detected solid-state NMR spectroscopy. J. Am. Chem. Soc. 134, 14730–14733 (2012).

    Article  Google Scholar 

  205. Bertini, I. et al. High-resolution solid-state NMR structure of a 17.6 kDa protein. J. Am. Chem. Soc. 132, 1032–1040 (2010).

    Article  Google Scholar 

  206. Damman, R. et al. Atomic-level insight into mRNA processing bodies by combining solid and solution-state NMR spectroscopy. Nat. Commun. 10, 4536 (2019).

    Article  ADS  Google Scholar 

  207. Bertarello, A. et al. Picometer resolution structure of the coordination sphere in the metal-binding site in a metalloprotein by NMR. J. Am. Chem. Soc. 142, 16757–16765 (2020).

    Article  Google Scholar 

  208. Wang, T., Phyo, P. & Hong, M. Multidimensional solid-state NMR spectroscopy of plant cell walls. Solid State Nucl. Magn. Reson. 78, 56–63 (2016).

    Article  Google Scholar 

  209. Takahashi, H. et al. Solid-state NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization. J. Am. Chem. Soc. 135, 5105–5110 (2013).

    Article  Google Scholar 

  210. Wang, T. & Hong, M. Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls. J. Exp. Botany 67, 503–514 (2016).

    Article  Google Scholar 

  211. Dick-Pérez, M. et al. Structure and interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry 50, 989–1000 (2011).

    Article  Google Scholar 

  212. Wang, T., Yang, H., Kubicki, J. D. & Hong, M. Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2D solid-state NMR spectroscopy and density functional theory calculations. Biomacromolecules 17, 2210–2222 (2016).

    Article  Google Scholar 

  213. Simmons, T. J. et al. Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR. Nat. Commun. 7, 13902 (2016).

    Article  ADS  Google Scholar 

  214. Phyo, P., Wang, T., Yang, Y., O’Neill, H. & Hong, M. Direct determination of hydroxymethyl conformations of plant cell wall cellulose using 1H polarization transfer solid-state NMR. Biomacromolecules 19, 1485–1497 (2018).

    Article  Google Scholar 

  215. Wang, T. et al. Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc. Natl Acad. Sci. USA 110, 16444–16449 (2013).

    Article  ADS  Google Scholar 

  216. Kang, X. et al. Lignin–polysaccharide interactions in plant secondary cell walls revealed by solid-state NMR. Nat. Commun. 10, 347 (2019). This solid-state NMR study provides the first comprehensive molecular-level structural insights into lignin–polysaccharide interactions in plant secondary cell walls.

    Article  ADS  Google Scholar 

  217. Kang, X. et al. Molecular architecture of fungal cell walls revealed by solid-state NMR. Nat. Commun. 9, 2747 (2018).

    Article  ADS  Google Scholar 

  218. Bougault, C., Ayala, I., Vollmer, W., Simorre, J. P. & Schanda, P. Studying intact bacterial peptidoglycan by proton-detected NMR spectroscopy at 100 kHz MAS frequency. J. Struct. Biol. 206, 66–72 (2019).

    Article  Google Scholar 

  219. McCrate, O. A., Zhou, X., Reichhardt, C. & Cegelski, L. Sum of the parts: composition and architecture of the bacterial extracellular matrix. J. Mol. Biol. 425, 4286–4294 (2013).

    Article  Google Scholar 

  220. Thongsomboon, W. et al. Phosphoethanolamine cellulose: a naturally produced chemically modified cellulose. Science 359, 334–338 (2018).

    Article  ADS  Google Scholar 

  221. Rossini, A. J. et al. Dynamic nuclear polarization NMR spectroscopy of microcrystalline solids. J. Am. Chem. Soc. 134, 16899–16908 (2012).

    Article  Google Scholar 

  222. Hartman, J. D., Day, G. M. & Beran, G. J. Enhanced NMR discrimination of pharmaceutically relevant molecular crystal forms through fragment-based ab initio chemical shift predictions. Cryst. Growth Des. 16, 6479–6493 (2016).

    Article  Google Scholar 

  223. Lu, X. et al. Molecular interactions in posaconazole amorphous solid dispersions from two-dimensional solid-state NMR spectroscopy. Mol. Pharm. 16, 2579–2589 (2019).

    Article  Google Scholar 

  224. Nilsson Lill, S. O. et al. Elucidating an amorphous form stabilization mechanism for tenapanor hydrochloride: crystal structure analysis using X-ray diffraction, NMR crystallography, and molecular modeling. Mol. Pharm. 15, 1476–1487 (2018).

    Article  Google Scholar 

  225. Leclaire, J. et al. Structure elucidation of a complex CO2-based organic framework material by NMR crystallography. Chem. Sci. 7, 4379–4390 (2016).

    Article  Google Scholar 

  226. Hofstetter, A. et al. Rapid structure determination of molecular solids using chemical shifts directed by unambiguous prior constraints. J. Am. Chem. Soc. 141, 16624–16634 (2019).

    Article  Google Scholar 

  227. Engel, E. A. et al. A Bayesian approach to NMR crystal structure determination. Phys. Chem. Chem. Phys. 21, 23385–23400 (2019).

    Article  Google Scholar 

  228. Ni, Q. Z. et al. In situ characterization of pharmaceutical formulations by dynamic nuclear polarization enhanced MAS NMR. J. Phys. Chem. B 121, 8132–8141 (2017).

    Article  Google Scholar 

  229. Walder, B. J. et al. One- and two-dimensional high-resolution NMR from flat surfaces. ACS Cent. Sci. 5, 515–523 (2019).

    Article  Google Scholar 

  230. Webber, A. L. et al. Identifying guanosine self assembly at natural isotopic abundance by high-resolution H-1 and C-13 solid-state NMR spectroscopy. J. Am. Chem. Soc. 133, 19777–19795 (2011).

    Article  Google Scholar 

  231. Mann, S. K., Pham, T. N., McQueen, L. L., Lewandowski, J. R. & Brown, S. P. Revealing intermolecular hydrogen bonding structure and dynamics in a deep eutectic pharmaceutical by magic-angle spinning NMR spectroscopy. Mol. Pharm. 17, 622–631 (2020).

    Article  Google Scholar 

  232. Jiang, X. et al. Thermally activated transient dipoles and rotational dynamics of hydrogen-bonded and charge-transferred diazabicyclo 2.2.2 octane molecular rotors. J. Am. Chem. Soc. 141, 16802–16809 (2019).

    Article  Google Scholar 

  233. Tracht, U. et al. Length scale of dynamic heterogeneities at the glass transition determined by multidimensional nuclear magnetic resonance. Phys. Rev. Lett. 81, 2727–2730 (1998).

    Article  ADS  Google Scholar 

  234. Viger-Gravel, J. et al. Structure of lipid nanoparticles containing siRNA or mRNA by dynamic nuclear polarization-enhanced NMR spectroscopy. J. Phys. Chem. B 122, 2073–2081 (2018).

    Article  Google Scholar 

  235. Pinon, A. C., Skantze, U., Viger-Gravel, J., Schantz, S. & Emsley, L. Core-shell structure of organic crystalline nanoparticles determined by relayed dynamic nuclear polarization NMR. J. Phys. Chem. A 122, 8802–8807 (2018).

    Article  Google Scholar 

  236. Johnson, R. L. & Schmidt-Rohr, K. Quantitative solid-state 13C NMR with signal enhancement by multiple cross polarization. J. Magn. Reson. 239, 44–49 (2014).

    Article  ADS  Google Scholar 

  237. Mao, J. D., Cao, X. Y., Olk, D. C., Chu, W. Y. & Schmidt-Rohr, K. Advanced solid-state NMR spectroscopy of natural organic matter. Prog. Nucl. Magn. Reson. Spect. 100, 17–51 (2017).

    Article  Google Scholar 

  238. Mao, J. D. et al. Abundant and stable char residues in soils: implications for soil fertility and carbon sequestration. Environ. Sci. Technol. 46, 9571–9576 (2012).

    Article  ADS  Google Scholar 

  239. Duan, P. et al. The chemical structure of carbon nanothreads analyzed by advanced solid-state NMR. J. Am. Chem. Soc. 140, 7658–7666 (2018).

    Article  Google Scholar 

  240. Hu, Y. Y., Rawal, A. & Schmidt-Rohr, K. Strongly bound citrate stabilizes the apatite nanocrystals in bone. Proc. Natl Acad. Sci. USA 107, 22425–22429 (2010). This study employs 13C chemical shifts and 13C–31P distance NMR spectroscopy experiments to show that the calcium phosphate surfaces in bone are studded with citrate molecules, which stabilize the apatite nanocrystals in bone.

    Article  ADS  Google Scholar 

  241. Davies, E. et al. Citrate bridges between mineral platelets in bone. Proc. Natl Acad. Sci. USA 111, E1354–E1363 (2014).

    Article  Google Scholar 

  242. Moran, R. F. et al. Ensemble-based modeling of the NMR spectra of solid solutions: cation disorder in Y2(Sn,Ti)2O7. J. Am. Chem. Soc. 141, 17838–17846 (2019).

    Article  Google Scholar 

  243. Ashbrook, S. E. et al. New insights into phase distribution, phase composition and disorder in Y2(Zr,Sn)2O7 ceramics from NMR spectroscopy. Phys. Chem. Chem. Phys. 17, 9049–9059 (2015).

    Article  Google Scholar 

  244. Valla, M. et al. Atomic description of the interface between silica and alumina in aluminosilicates through dynamic nuclear polarization surface-enhanced NMR spectroscopy and first-principles calculations. J. Am. Chem. Soc. 137, 10710–10719 (2015).

    Article  Google Scholar 

  245. Playford, H. Y. et al. Characterization of structural disorder in γ-Ga2O3. J. Phys. Chem. C 118, 16188–16198 (2014).

    Article  Google Scholar 

  246. Jaegers, N. R., Mueller, K. T., Wang, Y. & Hu, J. Z. Variable temperature and pressure operando MAS NMR for catalysis science and related materials. Acc. Chem. Res. 53, 611–619 (2020).

    Article  Google Scholar 

  247. Buannic, L., Blanc, F., Middlemiss, D. S. & Grey, C. P. Probing cation and vacancy ordering in the dry and hydrated yttrium-substituted BaSnO3 perovskite by NMR spectroscopy and first principles calculations: implications for proton mobility. J. Am. Chem. Soc. 134, 14483–14498 (2012).

    Article  Google Scholar 

  248. Alharbi, E. A. et al. Atomic-level passivation mechanism of ammonium salts enabling highly efficient perovskite solar cells. Nat. Commun. 10, 3008 (2019).

    Article  ADS  Google Scholar 

  249. Kubicki, D. J. et al. Phase segregation in Cs-, Rb- and K-doped mixed-cation (MA)x(FA)1 − xPbl3 hybrid perovskites from solid-state NMR. J. Am. Chem. Soc. 139, 14173–14180 (2017).

    Article  Google Scholar 

  250. Soleilhavoup, A., Hampson, M. R., Clark, S. J., Evans, J. S. O. & Hodgkinson, P. Using O-17 solid-state NMR and first principles calculation to characterise structure and dynamics in inorganic framework materials. Magn. Reson. Chem. 45, S144–S155 (2007).

    Article  Google Scholar 

  251. Pecher, O., Carretero-Gonzalez, J., Griffith, K. J. & Grey, C. P. Materials’ methods: NMR in battery research. Chem. Mater. 29, 213–242 (2017).

    Article  Google Scholar 

  252. Liu, T. et al. Cycling Li-O2 batteries via LiOH formation and decomposition. Science 350, 530–533 (2015). This paper describes how to overcome key challenges in engineering of lithium–air batteries and the use of 7Li and 1H NMR spectroscopy to determine the discharge products and elucidate the origin of protons in the formed LiOH.

    Article  ADS  Google Scholar 

  253. Chen, J. et al. Polar surface structure of oxide nanocrystals revealed with solid-state NMR spectroscopy. Nat. Commun. 10, 5420 (2019).

    Article  ADS  Google Scholar 

  254. Stebbins, J. F. & Xue, X. Y. in Spectroscopic Methods in Mineralology and Materials Sciences Vol. 78 (eds. Henderson, G. S., Neuville, D. R. & Downs, R. T.) 605–653 (Mineralogical Society of America, 2014).

  255. Griffin, J. M. & Ashbrook, S. E. Solid-state NMR of high-pressure silicates in the earth’s mantle. Annu. Rep. NMR Spec. 79, 241–332 (2013).

    Google Scholar 

  256. Langner, R., Fechtelkord, M., Garcia, A., Palin, E. J. & Lopez-Solano, J. Aluminum ordering and clustering in Al-rich synthetic phlogopite: {H-1}→Si-29 CPMAS HETCOR spectroscopy and atomistic calculations. Am. Mineral. 97, 341–352 (2012).

    Article  ADS  Google Scholar 

  257. Florian, P., Veron, E., Green, T. F. G., Yates, J. R. & Massiot, D. Elucidation of the Al/Si ordering in gehlenite Ca2Al2SiO7 by combined Si-29 and Al-27 NMR spectroscopy/quantum chemical calculations. Chem. Mater. 24, 4068–4079 (2012).

    Article  Google Scholar 

  258. Palke, A. C., Stebbins, J. F., Geiger, C. A. & Tippelt, G. Cation order–disorder in Fe-bearing pyrope and grossular garnets: a Al-27 and Si-29 MAS NMR and Fe-57 Mossbauer spectroscopy study. Am. Mineral. 100, 536–547 (2015).

    Article  ADS  Google Scholar 

  259. Gan, Z. H. Isotropic NMR spectra of half-integer quadrupolar nuclei using satellite transitions and magic-angle spinning. J. Am. Chem. Soc. 122, 3242–3243 (2000).

    Article  Google Scholar 

  260. Ashbrook, S. E. & Wimperis, S. High-resolution NMR of quadrupolar nuclei in solids: the satellite-transition magic angle spinning (STMAS) experiment. Prog. Nucl. Magn. Reson. Spectrosc. 45, 53–108 (2004).

    Article  Google Scholar 

  261. McKay, D. et al. A picture of disorder in hydrous wadsleyite — under the combined microscope of solid-state NMR spectroscopy and Ab initio random structure searching. J. Am. Chem. Soc. 141, 3024–3036 (2019).

    Article  Google Scholar 

  262. Griffin, J. M., Berry, A. J., Frost, D. J., Wimperis, S. & Ashbrook, S. E. Water in the earth’s mantle: a solid-state NMR study of hydrous wadsleyite. Chem. Sci. 4, 1523–1538 (2013).

    Article  Google Scholar 

  263. Ashbrook, S. E., Dawson, D. M. & Seymour, V. R. Recent developments in solid-state NMR spectroscopy of crystalline microporous materials. Phys. Chem. Chem. Phys. 16, 8223–8242 (2014).

    Article  Google Scholar 

  264. Pugh, S. M., Wright, P. A., Law, D. J., Thompson, N. & Ashbrook, S. E. Facile, room-temperature O-17 enrichment of zeolite frameworks revealed by solid-state NMR spectroscopy. J. Am. Chem. Soc. 142, 900–906 (2020).

    Article  Google Scholar 

  265. Bignami, G. P. M. et al. Synthesis, isotopic enrichment, and solid-state NMR characterization of zeolites derived from the assembly, disassembly, organization, reassembly process. J. Am. Chem. Soc. 139, 5140–5148 (2017).

    Article  Google Scholar 

  266. Nagashima, H. et al. Recent developments in NMR studies of aluminophosphates. Annu. Rep. NMR Spectrosc. 94, 113–185 (2018).

    Article  Google Scholar 

  267. Dawson, D. M. et al. A multinuclear NMR study of six forms of AlPO-34: structure and motional broadening. J. Phys. Chem. C 121, 1781–1793 (2017).

    Article  Google Scholar 

  268. Lucier, B. E. G., Chen, S. S. & Huang, Y. N. Characterization of metal–organic frameworks: unlocking the potential of solid-state NMR. Acc. Chem. Res. 51, 319–330 (2018).

    Article  Google Scholar 

  269. Witherspoon, V. J., Xu, J. & Reimer, J. A. Solid-state NMR investigations of carbon dioxide gas in metal–organic frameworks: insights into molecular motion and adsorptive behavior. Chem. Rev. 118, 10033–10048 (2018).

    Article  Google Scholar 

  270. Kong, X. Q. et al. Mapping of functional groups in metal–organic frameworks. Science 341, 882–885 (2013). This paper shows how solid-state NMR combined with molecular simulations can map the spatial distributions of linkers in multivariate metal–organic framework materials as random, well-mixed or clustered.

    Article  ADS  Google Scholar 

  271. Bonhomme, C., Gervais, C. & Laurencin, D. Recent NMR developments applied to organic–inorganic materials. Prog. Nucl. Magn. Reson. Spectrosc. 77, 1–48 (2014).

    Article  Google Scholar 

  272. Eden, M. 27Al NMR studies of aluminosilicate glasses. Annu. Rep. NMR Spectrosc. 86, 237–331 (2015).

    Article  Google Scholar 

  273. Pustovgar, E. et al. Understanding silicate hydration from quantitative analyses of hydrating tricalcium silicates. Nat. Commun. 7, 10952 (2016).

    Article  ADS  Google Scholar 

  274. Kunhi Mohamed, A. et al. The atomic-level structure of cementitious calcium aluminate silicate hydrate. J. Am. Chem. Soc. 142, 11060–11071 (2020).

    Article  Google Scholar 

  275. Gervais, C., Bonhomme, C. & Laurencin, D. Recent directions in the solid-state NMR study of synthetic and natural calcium phosphates. Solid State Nucl. Magn. Reson. 107, 101663 (2020).

    Article  Google Scholar 

  276. Casabianca, L. B. Solid-state nuclear magnetic resonance studies of nanoparticles. Solid State Nucl. Magn. Reson. 107, 101664 (2020).

    Article  Google Scholar 

  277. Al-Johani, H. et al. The structure and binding mode of citrate in the stabilization of gold nanoparticles. Nat. Chem. 9, 890–895 (2017).

    Article  Google Scholar 

  278. Berrettini, M. G., Braun, G., Hu, J. G. & Strouse, G. F. NMR analysis of surfaces and interfaces in 2-nm CdSe. J. Am. Chem. Soc. 126, 7063–7070 (2004).

    Article  Google Scholar 

  279. Avenier, P. et al. Dinitrogen dissociation on an isolated surface tantalum atom. Science 317, 1056–1060 (2007).

    Article  ADS  Google Scholar 

  280. Trebosc, J., Wiench, J. W., Huh, S., Lin, V. S. Y. & Pruski, M. Studies of organically functionalized mesoporous silicas using heteronuclear solid-state correlation NMR spectroscopy under fast magic angle spinning. J. Am. Chem. Soc. 127, 7587–7593 (2005).

    Article  Google Scholar 

  281. Wang, M. et al. Identification of different oxygen species in oxide nanostructures with 17O solid-state NMR spectroscopy. Sci. Adv. 1, e1400133 (2015).

    Article  ADS  Google Scholar 

  282. Berruyer, P. et al. Three-dimensional structure determination of surface sites. J. Am. Chem. Soc. 139, 849–855 (2017).

    Article  Google Scholar 

  283. Kobayashi, T., Perras, F. A., Slowing, I. I., Sadow, A. D. & Pruski, M. Dynamic nuclear polarization solid-state NMR in heterogeneous catalysis research. ACS Catal. 5, 7055–7062 (2015).

    Article  Google Scholar 

  284. Perras, F. A., Wang, Z. R., Naik, P., Slowing, I. I. & Pruski, M. Natural abundance O-17 DNP NMR provides precise O–H distances and insights into the bronsted acidity of heterogeneous catalysts. Angew. Chem. Int. Ed. 56, 9165–9169 (2017).

    Article  Google Scholar 

  285. Tošner, Z. et al. Overcoming volume selectivity of dipolar recoupling in biological solid-state NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 57, 14514–14518 (2018).

    Article  Google Scholar 

  286. Lewandowski, J. R., De Paëpe, G. & Griffin, R. G. Proton assisted insensitive nuclei cross polarization. J. Am. Chem. Soc. 129, 728–729 (2007).

    Article  Google Scholar 

  287. Samoson, A. H-MAS. J. Magn. Res. 306, 167–172 (2019).

    Article  ADS  Google Scholar 

  288. Wang, Z. et al. Combining fast magic angle spinning dynamic nuclear polarization with indirect detection to further enhance the sensitivity of solid-state NMR spectroscopy. Solid State Nucl. Magn. Reson. 109, 101685 (2020).

    Article  Google Scholar 

  289. Tycko, R. & Hu, K. N. A Monte Carlo/simulated annealing algorithm for sequential resonance assignment in solid state NMR of uniformly labeled proteins with magic-angle spinning. J. Magn. Reson. 205, 304–314 (2010).

    Article  ADS  Google Scholar 

  290. Fritzsching, K. J., Yang, Y., Schmidt-Rohr, K. & Hong, M. Practical use of chemical shift databases for protein solid-state NMR: 2D chemical shift maps and amino-acid assignment with secondary-structure information. J. Biomol. NMR 56, 155–167 (2013).

    Article  Google Scholar 

  291. Fritzsching, K. J., Hong, M. & Schmidt-Rohr, K. Conformationally selective multidimensional chemical shift ranges in proteins from a PACSY database purged using intrinsic quality criteria. J. Biomol. NMR 64, 115–130 (2016).

    Article  Google Scholar 

  292. Yang, Y., Fritzsching, K. J. & Hong, M. Resonance assignment of disordered proteins using a multi-objective non-dominated sorting genetic algorithm. J. Biomol. NMR 57, 281–296 (2013).

    Article  Google Scholar 

  293. Bartok, A. P. & Yates, J. R. Regularized SCAN functional. J. Chem. Phys. 150, 207101 (2019).

    Article  Google Scholar 

  294. Hartman, J. D., Kudla, R. A., Day, G. M., Mueller, L. J. & Beran, G. J. Benchmark fragment-based 1H, 13C, 15N and 17O chemical shift predictions in molecular crystals. Phys. Chem. Chem. Phys. 18, 21686–21709 (2016).

    Article  Google Scholar 

  295. Paruzzo, F. M. et al. Chemical shifts in molecular solids by machine learning. Nat. Commun. 9, 4501 (2018).

    Article  ADS  Google Scholar 

  296. Iwasa, Y. et al. A high-resolution 1.3-GHz/54-mm LTS/HTS NMR magnet. IEEE Trans. Appl. Supercond. 25, 1–5 (2015).

    Article  Google Scholar 

  297. Gan, Z. et al. NMR spectroscopy up to 35.2 T using a series-connected hybrid magnet. J. Magn. Reson. 284, 125–136 (2017).

    Article  ADS  Google Scholar 

  298. Xue, K. et al. Impact of magnetic field strength on resolution and sensitivity of proton resonances in biological solids. J. Phys. Chem. C. 124, 22631–22637 (2020).

    Article  Google Scholar 

  299. Keeler, E. G. et al. 17O MAS NMR correlation spectroscopy at high magnetic fields. J. Am. Chem. Soc. 139, 17953–17963 (2017).

    Article  Google Scholar 

  300. Chen, P. H. et al. Magic angle spinning spheres. Sci. Adv. 4, eaau1540 (2018).

    Article  ADS  Google Scholar 

  301. Agarwal, V. et al. De novo 3D structure determination from sub-milligram protein samples by solid-state 100 kHz MAS NMR spectroscopy. Angew. Chem. Int. Ed. 53, 12253–12256 (2014).

    Article  Google Scholar 

  302. Xue, K. et al. Magic angle spinning frequencies beyond 300 kHz are necessary to yield maximum sensitivity in selectively methyl protonated protein samples in solid state NMR. J. Phys. Chem. C 122, 16437–16442 (2018).

    Article  Google Scholar 

  303. Gao, C. et al. Four millimeter spherical rotors spinning at 28 kHz with double-saddle coils for cross polarization NMR. J. Magn. Reson. 303, 1–6 (2019).

    Article  ADS  Google Scholar 

  304. Berruyer, P. et al. Dynamic nuclear polarization enhancement of 200 at 21.15 T enabled by 65 kHz magic angle spinning. J. Phys. Chem. Lett. 11, 8386–8391 (2020).

    Article  Google Scholar 

  305. Can, T. V., Walish, J. J., Swager, T. M. & Griffin, R. G. Time domain DNP with the NOVEL sequence. J. Chem. Phys. 143, 054201 (2015).

    Article  ADS  Google Scholar 

  306. Jaudzems, K. et al. Dynamic nuclear polarization-enhanced biomolecular NMR spectroscopy at high magnetic field with fast magic-angle spinning. Angew. Chem. Int. Ed. 57, 7458–7462 (2018).

    Article  Google Scholar 

  307. Tosner, Z. et al. Optimal control in NMR spectroscopy: numerical implementation in SIMPSON. J. Magn. Res. 197, 120–134 (2009).

    Article  ADS  Google Scholar 

  308. Concistrè, M., Johannessen, O. G., Carignani, E., Geppi, M. & Levitt, M. H. Magic-angle spinning NMR of cold samples. Acc. Chem. Res. 46, 1914–1922 (2013).

    Article  Google Scholar 

  309. Jeon, J., Thurber, K. R., Ghirlando, R., Yau, W. M. & Tycko, R. Application of millisecond time-resolved solid state NMR to the kinetics and mechanism of melittin self-assembly. Proc. Natl Acad. Sci. USA 116, 16717–16722 (2019).

    Article  Google Scholar 

  310. Freedberg, D. I. & Selenko, P. Live cell NMR. Annu. Rev. Biophys. 43, 171–192 (2014).

    Article  Google Scholar 

  311. Chow, W. Y. et al. NMR spectroscopy of native and in vitro tissues implicates polyADP ribose in biomineralization. Science 344, 742–746 (2014).

    Article  ADS  Google Scholar 

  312. Narasimhan, S. et al. DNP-supported solid-state NMR spectroscopy of proteins inside mammalian cells. Angew. Chem. Int. Ed. 58, 12969–12973 (2019).

    Article  Google Scholar 

  313. Jacso, T. et al. Characterization of membrane proteins in isolated native cellular membranes by dynamic nuclear polarization solid-state NMR spectroscopy without purification and reconstitution. Angew. Chem. Int. Ed. 51, 432–435 (2012).

    Article  Google Scholar 

  314. Kaplan, M. et al. EGFR dynamics change during activation in native membranes as revealed by NMR. Cell 167, 1241–1251 (2016).

    Article  Google Scholar 

  315. Yusa, G., Muraki, K., Takashina, K., Hashimoto, K. & Hirayama, Y. Controlled multiple quantum coherences of nuclear spins in a nanometre-scale device. Nature 434, 1001–1005 (2005).

    Article  ADS  Google Scholar 

  316. Meriles, C. A. et al. High-resolution NMR of static samples by rotation of the magnetic field. J. Magn. Reson. 169, 13–18 (2004).

    Article  ADS  Google Scholar 

  317. Sakellariou, D. et al. Permanent magnet assembly producing a strong tilted homogeneous magnetic field: towards magic angle field spinning NMR and MRI. Magn. Reson. Chem. 48, 903–908 (2010).

    Article  Google Scholar 

  318. Niu, Z. et al. Mapping of the binding interface of PET tracer molecules and Alzheimer disease Aβ fibrils using MAS solid-state NMR. ChemBioChem 21, 2495–2502 (2020).

    Article  Google Scholar 

  319. Reichert, D. & Krushelnitsky, A. in Modern Methods in Solid-state NMR: A Practitioner’s Guide (ed. Hodgkinson, P.) (RSC, 2018).

  320. Ashbrook, S. E. et al. 17O and 29Si NMR parameters of MgSiO3 phases from high-resolution solid-state NMR spectroscopy and first-principles calculations. J. Am. Chem. Soc. 129, 13213–13224 (2007).

    Article  Google Scholar 

  321. Haw, J. F., Song, W., Marcus, D. M. & Nicholas, J. B. The mechanism of methanol to hydrocarbon catalysis. Acc. Chem. Res. 36, 317–326 (2003).

    Article  Google Scholar 

  322. Alanazi, A. Q. et al. Atomic-level microstructure of efficient formamidinium-based perovskite solar cells stabilized by 5-ammonium valeric acid iodide revealed by multinuclear and two-dimensional solid-state NMR. J. Am. Chem. Soc. 141, 17659–17669 (2019).

    Article  Google Scholar 

  323. Martins, V. et al. Higher magnetic fields, finer MOF structural information: 17O solid-state NMR at 35.2 T. J. Am. Chem. Soc. 142, 14877–14889 (2020).

    Article  Google Scholar 

  324. Paravastu, A.K. Leapman, R.D., Yau, W.M, Tycko, R. Molecular structural basis for polymorphism in Alzheimer’s beta-amyloid fibrils. Proc. Natl Acad. Sci. USA 105, 18349–18354 (2008).

    Article  ADS  Google Scholar 

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Acknowledgements

M.H. acknowledges support by National Institutes of Health (NIH) grant GM066976.

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Authors and Affiliations

  1. Technische Universität München, Department Chemie, Garching, Germany

    Bernd Reif

  2. School of Chemistry, University of St Andrews, St Andrews, UK

    Sharon E. Ashbrook

  3. École Polytechnique Fédérale de Lausanne (EPFL), Institut des sciences et ingénierie chimiques, Lausanne, Switzerland

    Lyndon Emsley

  4. Department of Chemistry and Francis Bitter Magnet Laboratory, Massachusetts Institute of Technology, Cambridge, MA, USA

    Mei Hong

Authors
  1. Bernd Reif
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  2. Sharon E. Ashbrook
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  3. Lyndon Emsley
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  4. Mei Hong
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Contributions

Introduction (B.R., S.E.A., L.E. and M.H.); Experimentation (B.R., S.E.A., L.E. and M.H.); Results (B.R., S.E.A., L.E. and M.H.); Applications (B.R., S.E.A., L.E. and M.H.); Reproducibility and data deposition (B.R., S.E.A., L.E. and M.H.); Limitations and optimizations (B.R., S.E.A., L.E. and M.H.); Outlook (B.R., S.E.A., L.E. and M.H.); overview of the Primer (M.H.).

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Correspondence to Mei Hong.

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Related links

Biological Magnetic Resonance Data Bank (BRMB): https://bmrb.io/

Cambridge Structural Database (CSD): https://www.ccdc.cam.ac.uk/solutions/csd-system/components/csd/

Inorganic Crystal Structure Database (ICSD): https://icsd.products.fiz-karlsruhe.de

Protein Databank (PDB): https://www.rcsb.org/

Glossary

Non-zero nuclear spins

Nuclear isotopes with a non-zero spin angular momentum.

Gyromagnetic ratio

The ratio of the magnetic moment of a particle to its angular momentum.

Anisotropic

Orientation-dependent.

Fourier transformation

A mathematical transformation that decomposes a function (usually of time) into its constituent frequencies.

Ionothermal synthesis

The use of ionic liquids as both the solvent and the potential template in the formation of solids.

Chemical shift anisotropies

(CSAs). The orientation-dependent component of the chemical shielding interaction.

Paramagnetic

Weakly attracted by an externally applied magnetic field, typically as a result of the presence of unpaired electrons.

Molecular dynamics

A computer-simulation method for characterizing the dynamics of atoms and molecules, providing an overview of how they move over a period of time.

Density functional theory

(DFT). A computational quantum-mechanical modelling approach used to investigate electronic structure in many-body systems.

Cryo-electron microscopy

A technique used to determine the 3D structure of samples frozen at cryogenic temperatures, which are not in a crystalline form.

Extended X-ray absorption fine structure

An X-ray absorption spectroscopy technique that is amenable for non-uniform crystalline samples.

Generalized gradient approximation

A type of exchange correlation functional used in density functional theory that considers the density and the gradient of the density

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Reif, B., Ashbrook, S.E., Emsley, L. et al. Solid-state NMR spectroscopy. Nat Rev Methods Primers 1, 2 (2021). https://doi.org/10.1038/s43586-020-00002-1

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