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Modern Magnetic Resonance pp 879–910Cite as

Proton-Detection in Biological MAS Solid-State NMR Spectroscopy

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Abstract

In the last years, proton-detected experiments became more and more routine in MAS solid-state NMR. High-resolution proton spectra are obtained in MAS solid-state NMR in case samples are prepared using perdeuterated protein and D2O in the recrystallization buffer. Deuteration reduces drastically 1H, 1H dipolar interactions and allows to obtain amide proton line widths on the order of 20 Hz. Similarly, high-resolution proton spectra of aliphatic groups can be obtained if specifically labeled precursors for biosynthesis of methyl containing side chains are used, or if limited amounts of H2O in the bacterial growth medium is employed. This review summarizes recent spectroscopic developments to access structure and dynamics of biomacromolecules in the solid-state and shows a number of applications to amyloid fibrils, membrane proteins, and soluble protein complexes.

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References

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

    Article  CAS  Google Scholar 

  2. Colvin MT, Silvers R, Ni QZ, Can TV, Sergeyev I, Rosay M, Donovan KJ, Michael B, Wall J, Linse S, Griffin RG. Atomic resolution structure of monomorphic A beta(42) amyloid fibrils. J Am Chem Soc. 2016;138:9663–74.

    Article  CAS  Google Scholar 

  3. Loquet A, Sgourakis NG, Gupta R, Giller K, Riedel D, Goosmann C, Griesinger C, Kolbe M, Baker D, Becker S, Lange A. Atomic model of the type III secretion system needle. Nature. 2012;486:276–9.

    Article  CAS  Google Scholar 

  4. Mainz A, Peschek J, Stavropoulou M, Back K, Bardiaux B, Asami S, Prade E, Peters C, Weinkauf S, Buchner J, Reif B. The chaperone αB-crystallin deploys different interfaces to capture an amorphous and an amyloid client. Nat Struct Mol Biol. 2015;22:898–905.

    Article  CAS  Google Scholar 

  5. Tuttle MD, Comellas G, Nieuwkoop AJ, Covell DJ, Berthold DA, Kloepper KD, Courtney JM, Kim JK, Barclay AM, Kendall A, Wan W, Stubbs G, Schwieters CD, Lee VM, George JM, Rienstra CM. Solid-state NMR structure of a pathogenic fibril of full-length human α-synuclein. Nature Struct Mol Biol. 2016;23:409–415.

    Article  CAS  Google Scholar 

  6. Wälti MA, Ravotti F, Arai H, Glabe CG, Wall JS, Böckmann A, Güntert P, Meier BH, Riek R. Atomic-resolution structure of a disease-relevant Aβ(1-42) amyloid fibril. Proc Natl Acad Sci U S A. 2016;113:E4976–84.

    Article  CAS  Google Scholar 

  7. Wang S, Munro RA, Shi L, Kawamura I, Okitsu T, Wada A, Kim S-Y, Jung K-H, Brown LS, Ladizhansky V. Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nat Methods. 2013;10:1007.

    Article  CAS  Google Scholar 

  8. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH. Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science. 2008;319:1523–6.

    Article  CAS  Google Scholar 

  9. Samoson A, Tuherm T, Past J, Reinhold A, Anupold T, Heinmaa N. New horizons for magic-angle spinning NMR. Top Curr Chem. 2005;246:15–31.

    Article  CAS  Google Scholar 

  10. Agarwal V, Penzel S, Szekely K, Cadalbert R, Testori E, Oss A, Past J, Samoson A, Ernst M, Bockmann A, Meier BH. De Novo 3D structure determination from sub-milligram protein samples by solid-state 100 kHz MAS NMR spectroscopy. Angew Chem Int Ed. 2014;53:12253–6.

    Article  CAS  Google Scholar 

  11. Andreas LB, Jaudzems K, Stanek J, Lalli D, Bertarello A, Marchand TL, Cala-De Paepe D, Kotelovica S, Akopjana I, Knott B, Wegner S, Engelke F, Lesage A, Emsley L, Tars K, Herrmann T, Pintacuda G. Structure of fully protonated proteins by proton-detected magic-angle spinning NMR. Proc Natl Acad Sci U S A. 2016;113:9187–92.

    Article  CAS  Google Scholar 

  12. Stanek J, Andreas LB, Jaudzems K, Cala D, Lalli D, Bertarello A, Schubeis T, Akopjana I, Kotelovica S, Tars K, Pica A, Leone S, Picone D, Xu ZQ, Dixon NE, Martinez D, Berbon M, El Mammeri N, Noubhani A, Saupe S, Habenstein B, Loquet A, Pintacuda G. NMR spectroscopic assignment of backbone and side-chain protons in fully protonated proteins: microcrystals, sedimented assemblies, and amyloid fibrils. Angew Chem Int Ed Eng. 2016;55:15503–9.

    Google Scholar 

  13. Bockmann A, Ernst M, Meier BH. Spinning proteins, the faster, the better? J Magn Reson. 2015;253:71–9.

    Article  CAS  Google Scholar 

  14. Burum DP. Combined rotation and multiple pulse spectroscopy (CRAMPS). Concepts Magn Reson. 1990;2:213–27.

    Article  Google Scholar 

  15. Gerstein BC, Chow C, Pembleton RG, Wilson RC. Utility of pulse nuclear magnetic resonance in studying protons in coals. J Phys Chem. 1977;81:565–70.

    Article  CAS  Google Scholar 

  16. Schnabel B, Haubenreisser U, Scheler G, Müller R. Proc. 19th Congr. Ampere (Heidelberg) 1976, 441.

    Google Scholar 

  17. Waugh JS, Huber LM, Haeberlen U. Approach to high-resolution NMR in solids. Phys Rev Lett. 1968;20:180.

    Article  CAS  Google Scholar 

  18. Burum DP, Rhim WK. Analysis of multiple pulse NMR in solids .3. J Chem Phys. 1979;71:944–56.

    Article  CAS  Google Scholar 

  19. Hohwy M, Bower PV, Jakobsen HJ, Nielsen NC. A high-order and broadband CRAMPS experiment using z-rotational decoupling Chem. Phys Lett. 1997;273:297–303.

    CAS  Google Scholar 

  20. Bielecki A, Kolbert AC, Levitt MH. Frequency-switched pulse sequences – homonuclear decoupling and dilute spin NMR in solids. Chem Phys Lett. 1989;155:341–6.

    Article  CAS  Google Scholar 

  21. Vinogradov E, Madhu PK, Vega S. High-resolution proton solid-state NMR spectroscopy by phase-modulated Lee-Goldburg experiment. Chem Phys Lett. 1999;314:443–50.

    Article  CAS  Google Scholar 

  22. Vinogradov E, Madhu PK, Vega S. Proton spectroscopy in solid state nuclear magnetic resonance with windowed phase modulated Lee –Goldburg decoupling sequences. Chem Phys Lett. 2002;354:193–202.

    Article  CAS  Google Scholar 

  23. Lesage A, Sakellariou D, Hediger S, Elena B, Charmont P, Steuernagel S, Emsley L. Experimental aspects of proton NMR spectroscopy in solids using phase-modulated homonuclear dipolar decoupling. J Magn Reson. 2003;163:105–13.

    Article  CAS  Google Scholar 

  24. Madhu PK, Zhao X, Levitt MH. High-resolution H-1 NMR in the solid state using symmetry-based pulse sequences. Chem Phys Lett. 2001;346:142–8.

    Article  CAS  Google Scholar 

  25. Morcombe CR, Paulson EK, Gaponenko V, Byrd RA, Zilm KW. H-1-N-15 correlation spectroscopy of nanocrystalline proteins. J Biomol NMR. 2005;31:217–30.

    Article  CAS  Google Scholar 

  26. Kay LE, Gardner KH. Solution NMR spectroscopy beyond 25 kDa. Curr Opin Struct Biol. 1997;7:722–31.

    Article  CAS  Google Scholar 

  27. LeMaster DM, Richards FM. NMR sequential assignment of Escherichia coli thioredoxin utilizing random fractional deuteration. Biochemist. 1988;27:142–50.

    Article  CAS  Google Scholar 

  28. LeMaster DM. Deuteration in protein proton magnetic resonance. Methods Enzymol. 1989;177:23–43.

    Article  CAS  Google Scholar 

  29. McDermott AE, Creuzet FJ, Kolbert AC, Griffin RG. High-resolution magic-angle-spinning NMR spectra of protons in deuterated solids. J Magn Reson. 1992;98:408–13.

    CAS  Google Scholar 

  30. Zheng L, Fishbein KW, Griffin RG, Herzfeld J. Two-dimensional solid-state 1H NMR and proton exchange. J Am Chem Soc. 1993;115:6254–61.

    Article  CAS  Google Scholar 

  31. Zorin VE, Brown SP, Hodgkinson P. Origins of linewidth in 1H magic-angle spinning NMR. J Chem Phys. 2006;125:144508.

    Article  CAS  Google Scholar 

  32. Reif B, Jaroniec CP, Rienstra CM, Hohwy M, Griffin RG. 1H-1H MAS correlation spectroscopy and distance measurements in a deuterated peptide. J Magn Reson. 2001;151:320–7.

    Article  CAS  Google Scholar 

  33. Reif B, Griffin RG. 1H detected 1H,15N correlation spectroscopy in rotating solids. J Magn Reson. 2003;160:78–83.

    Article  CAS  Google Scholar 

  34. Zhou DH, Graesser DT, Franks WT, Rienstra CM. Sensitivity and resolution in proton solid-state NMR at intermediate deuteration levels: quantitative linewidth analysis and applications to correlation spectroscopy. J Magn Reson. 2006;178:297–307.

    Article  CAS  Google Scholar 

  35. Chevelkov V, van Rossum BJ, Castellani F, Rehbein K, Diehl A, Hohwy M, Steuernagel S, Engelke F, Oschkinat H, Reif B. 1H detection in MAS solid state NMR spectroscopy employing pulsed field gradients for residual solvent suppression. J Am Chem Soc. 2003;125:7788–9.

    Article  CAS  Google Scholar 

  36. Paulson EK, Morcombe CR, Gaponenko V, Dancheck B, Byrd RA, Zilm KW. Sensitive high resolution inverse detection NMR spectroscopy of proteins in the solid state. J Am Chem Soc. 2003;125:15831–6.

    Article  CAS  Google Scholar 

  37. Paulson EK, Morcombe CR, Gaponenko V, Dancheck B, Byrd RA, Zilm KW. High-sensitivity observation of dipolar exchange and NOEs between exchangeable protons in proteins by 3D solid-state NMR spectroscopy. J Am Chem Soc. 2003;125:14222–3.

    Article  CAS  Google Scholar 

  38. Reif B, van Rossum BJ, Castellani F, Rehbein K, Diehl A, Oschkinat H. Characterization of 1H 1H distances in a uniformly 2H,15N labeled SH3 domain by MAS solid state NMR spectroscopy. J Am Chem Soc. 2003;125:1488–9.

    Article  CAS  Google Scholar 

  39. Chevelkov V, Faelber K, Diehl A, Heinemann U, Oschkinat H, Reif B. Detection of dynamic water molecules in a microcrystalline sample of the SH3 domain of alpha-spectrin by MAS solid-state NMR. J Biomol NMR. 2005;31:295–310.

    Article  CAS  Google Scholar 

  40. 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. 2006;45:3878–81.

    Article  CAS  Google Scholar 

  41. Akbey Ü, Lange S, Franks TW, Linser R, Diehl A, van Rossum BJ, Reif B, Oschkinat H. Optimum levels of exchangeable protons in perdeuterated proteins for proton detection in MAS solid-state NMR spectroscopy. J Biomol NMR. 2010;46:67–73.

    Article  CAS  Google Scholar 

  42. Zhou DH, Rienstra CM. High-performance solvent suppression for proton-detected solid-state NMR. J Magn Reson. 2008;192:167–72.

    Article  CAS  Google Scholar 

  43. Barbet-Massin E, Felletti M, Schneider R, Jehle S, Communie G, Martinez N, Jensen MR, Ruigrok RWH, Emsley L, Lesage A, Blackledge M, Pintacuda G. Insights into the structure and dynamics of measles virus nucleocapsids by H-1-detected solid-state NMR. Biophys J. 2014;107:941–6.

    Article  CAS  Google Scholar 

  44. Knight MJ, Webber AL, Pell AJ, Guerry P, Barbet-Massin E, Bertini I, Felli IC, Gonnelli L, Pierattelli R, Emsley L, Lesage A, Herrmann T, Pintacuda G. Fast resonance assignment and fold determination of human superoxide dismutase by high-resolution proton-detected solid-state MAS NMR spectroscopy. Angew Chem Int Ed. 2011;50:11697–701.

    Article  CAS  Google Scholar 

  45. Lewandowski JR, Dumez JN, Akbey U, Lange S, Emsley L, Oschkinat H. Enhanced resolution and coherence lifetimes in the solid-state NMR spectroscopy of perdeuterated proteins under ultrafast magic-angle spinning. J Phys Chem Lett. 2011;2:2205–11.

    Article  CAS  Google Scholar 

  46. Penzel S, Smith AA, Agarwal V, Hunkeler A, Org ML, Samoson A, Bockmann A, Ernst M, Meier BH. Protein resonance assignment at MAS frequencies approaching 100 kHz: a quantitative comparison of J-coupling and dipolar-coupling-based transfer methods. J Biomol NMR. 2015;63:165–86.

    Article  CAS  Google Scholar 

  47. Agarwal V, Reif B. Residual methyl protonation in perdeuterated proteins for multidimensional correlation experiments in MAS solid-state NMR spectroscopy. J Magn Reson. 2008;194:16–24.

    Article  CAS  Google Scholar 

  48. Agarwal V, Diehl A, Skrynnikov N, Reif B. High resolution 1H detected 1H,13C correlation spectra in MAS solid-state NMR using deuterated proteins with selective 1H,2H isotopic labeling of methyl groups. J Am Chem Soc. 2006;128:12620–1.

    Article  CAS  Google Scholar 

  49. Agarwal V, Xue Y, Reif B, Skrynnikov NR. Protein side-chain dynamics as observed by solution- and solid-state NMR: a similarity revealed. J Am Chem Soc. 2008;130:16611–21.

    Article  CAS  Google Scholar 

  50. Huber M, Hiller S, Schanda P, Ernst M, Bockmann A, Verel R, Meier BH. A proton-detected 4D solid-state NMR experiment for protein structure determination. Chem Phys Chem. 2011;12:915–8.

    Article  CAS  Google Scholar 

  51. Goto N, Kay LE. New developments in isotope strategies for protein solution NMR spectroscopy. Curr Opin Cell Biol. 2000;10:585–92.

    CAS  Google Scholar 

  52. Asami S, Schmieder P, Reif B. High resolution 1H-detected solid-state NMR spectroscopy of protein aliphatic resonances: access to tertiary structure information. J Am Chem Soc. 2010;132:15133–5.

    Article  CAS  Google Scholar 

  53. Asami S, Reif B. Assignment strategies for aliphatic protons in the solid-state in randomly protonated proteins. J Biomol NMR. 2012;52:31–9.

    Article  CAS  Google Scholar 

  54. Asami S, Reif B. Proton-detected solid-state NMR at aliphatic sites: applications to crystalline systems. Acc Chem Res. 2013;46:2089–97.

    Article  CAS  Google Scholar 

  55. Mance D, Sinnige T, Kaplan M, Narasimhan S, Daniels M, Houben K, Baldus M, Weingarth M. An efficient labelling approach to harness backbone and side-chain protons in H-1-detected solid-state NMR spectroscopy. Angew Chem Int Ed Eng. 2015;54:15799–803.

    Article  CAS  Google Scholar 

  56. Sinnige T, Daniels M, Baldus M, Weingarth M. Proton clouds to measure long-range contacts between nonexchangeable side chain protons in solid-state NMR. J Am Chem Soc. 2014;136:4452–5.

    Article  CAS  Google Scholar 

  57. Agarwal V, Linser R, Fink U, Faelber K, Reif B. Identification of hydroxyl protons, determination of their exchange dynamics, and characterization of hydrogen bonding by MAS solid-state NMR spectroscopy in a microcrystalline protein. J Am Chem Soc. 2010;132:3187–95.

    Article  CAS  Google Scholar 

  58. Agarwal V, Faelber K, Schmieder P, Reif B. High-resolution double-quantum deuterium magic angle spinning solid-state NMR spectroscopy of perdeuterated proteins. J Am Chem Soc. 2009;131:2–3.

    Article  CAS  Google Scholar 

  59. Lalli D, Schanda P, Chowdhury A, Retel J, Hiller M, Higman VA, Handel L, Agarwal V, Reif B, van Rossum B-J, Akbey Ü, Oschkinat H. Three-dimensional deuterium-carbon correlation experiments for high-resolution solid-state MAS NMR spectroscopy of large proteins. J Biomol NMR. 2011;51:477–85.

    Article  CAS  Google Scholar 

  60. Shi XY, Rienstra CM. Site-specific internal motions in GB1 protein microcrystals revealed by 3D H-2-C-13-C-13 solid-state NMR spectroscopy. J Am Chem Soc. 2016;138:4105–19.

    Article  CAS  Google Scholar 

  61. Wei D, Akbey Ü, Paaske B, Oschkinat H, Reif B, Bjerring M, Nielsen NC. Optimal 2H Rf pulses and 2H-13C cross-polarization methods for solid-state 2H MAS NMR of perdeuterated proteins. J Phys Chem Lett. 2011;2:1289–94.

    Article  CAS  Google Scholar 

  62. Hologne M, Faelber K, Diehl A, Reif B. Characterization of dynamics of perdeuterated proteins by MAS solid-state NMR. J Am Chem Soc. 2005;127:11208–9.

    Article  CAS  Google Scholar 

  63. Bjerring M, Paaske B, Oschkinat H, Akbey U, Nielsen NC. Rapid solid-state NMR of deuterated proteins by interleaved cross-polarization from H-1 and H-2 nuclei. J Magn Reson. 2012;214:324–8.

    Article  CAS  Google Scholar 

  64. Jain SK, Nielsen AB, Hiller M, Handel L, Ernst M, Oschkinat H, Akbey U, Nielsen NC. Low-power polarization transfer between deuterons and spin-1/2 nuclei using adiabatic (CP)-C-RESPIRATION in solid-state NMR. Phys Chem Chem Phys. 2014;16:2827–30.

    Article  CAS  Google Scholar 

  65. Akbey U, Nieuwkoop AJ, Wegner S, Voreck A, Kunert B, Bandara P, Engelke F, Nielsen NC, Oschkinat H. Quadruple-resonance magic-angle spinning NMR spectroscopy of deuterated solid proteins. Angew Chem Int Ed. 2014;53:2438–42.

    Article  CAS  Google Scholar 

  66. Linser R, Chevelkov V, Diehl A, Reif B. Sensitivity enhancement using paramagnetic relaxation in MAS solid state NMR of perdeuterated proteins. J Magn Reson. 2007;189:209–16.

    Article  CAS  Google Scholar 

  67. Wickramasinghe NP, Kotecha M, Samoson A, Past J, Ishii Y. Sensitivity enhancement in C-13 solid-state NMR of protein microcrystals by use of paramagnetic metal ions for optimizing H-1 T-1 relaxation. J Magn Reson. 2007;184:350–6.

    Article  CAS  Google Scholar 

  68. Wickramasinghe NP, Parthasarathy S, Jones CR, Bhardwaj C, Long F, Kotecha M, Mehboob S, Fung LW, Past J, Samoson A, Ishii Y. Nanomole-scale protein solid-state NMR by breaking intrinsic H-1 T-1 boundaries. Nat Methods. 2009;6:215–8.

    Article  CAS  Google Scholar 

  69. Doty FD, Kulkarni J, Turner C, Entzminger G, Bielecki A. Using a cross-coil to reduce RF heating by an order of magnitude in triple-resonance multinuclear MAS at high fields. J Magn Reson. 2006;182:239–53.

    Article  CAS  Google Scholar 

  70. Krahn A, Priller U, Emsley L, Engelke F. Resonator with reduced sample heating and increased homogeneity for solid-state NMR. J Magn Reson. 2008;191:78–92.

    Article  CAS  Google Scholar 

  71. Stringer JA, Bronnimann CE, Mullen CG, Zhou DHH, Stellfox SA, Li Y, Williams EH, Rienstra CM. Reduction of RF-induced sample heating with a scroll coil resonator structure for solid-state NMR probes. J Magn Reson. 2005;173:40–8.

    Article  CAS  Google Scholar 

  72. Linser R, Fink U, Reif B. Probing surface accessibility of proteins using paramagnetic relaxation in solid-state NMR spectroscopy. J Am Chem Soc. 2009;131:13703–8.

    Article  CAS  Google Scholar 

  73. Tang M, Comellas G, Mueller LJ, Rienstra CM. High resolution C-13-detected solid-state NMR spectroscopy of a deuterated protein. J Biomol NMR. 2010;48:103–11.

    Article  CAS  Google Scholar 

  74. Linser R, Fink U, Reif B. Proton-detected scalar coupling based assignment strategies in MAS solid-state NMR spectroscopy applied to perdeuterated proteins. J Magn Reson. 2008;193:89–93.

    Article  CAS  Google Scholar 

  75. Linser R, Fink U, Reif B. Narrow carbonyl resonances in proton-diluted proteins facilitate NMR assignments in the solid-state. J Biomol NMR. 2010;47:1–6.

    Article  CAS  Google Scholar 

  76. Schanda P, Huber M, Verel R, Ernst M, Meier BH. Direct detection of 3hJNC hydrogen-bond scalar couplings in proteins by solid-state NMR spectroscopy. Angew Chem Int Ed. 2009;48:9322–5.

    Article  CAS  Google Scholar 

  77. Linser R. Side-chain to backbone correlations from solid-state NMR of perdeuterated proteins through combined excitation and long-range magnetization transfers. J Biomol NMR. 2011;51:221–6.

    Article  CAS  Google Scholar 

  78. 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 micro-crystalline protein with MAS solid-state NMR spectroscopy. J Am Chem Soc. 2011;133:5905–12.

    Article  CAS  Google Scholar 

  79. Barbet-Massin E, Pell AJ, Jaudzems K, Franks WT, Retel JS, Kotelovica S, Akopjana I, Tars K, Emsley L, Oschkinat H, Lesage A, Pintacuda G. Out-and-back C-13-C-13 scalar transfers in protein resonance assignment by proton-detected solid-state NMR under ultra-fast MAS. J Biomol NMR. 2013;56:379–86.

    Article  CAS  Google Scholar 

  80. Barbet-Massin E, Pell AJ, Retel JS, Andreas LB, Jaudzems K, Franks WT, Nieuwkoop AJ, Hiller M, Higman V, Guerry P, Bertarello A, Knight MJ, Felletti M, Le Marchand T, Kotelovica S, Akopjana I, Tars K, Stoppini M, Bellotti V, Bolognesi M, Ricagno S, Chou JJ, Griffin RG, Oschkinat H, Lesage A, Emsley L, Herrmann T, Pintacuda G. Rapid proton-detected NMR assignment for proteins with fast magic angle spinning. J Am Chem Soc. 2014;136:12489–97.

    Article  CAS  Google Scholar 

  81. Andreas LB, Stanek J, Marchand TL, Bertarello A, Cala-De Paepe D, Lalli D, Krejčíková M, Doyen C, Öster C, Knott B, Wegner S, Engelke F, Felli IC, Pierattelli R, Dixon NE, Emsley L, Herrmann T, Pintacuda G. Protein residue linking in a single spectrum for magic-angle spinning NMR assignment. J Biomol NMR. 2015;62:253–61.

    Article  CAS  Google Scholar 

  82. Xiang S, Grohe K, Rovó P, Vasa SK, Giller K, Becker S, Linser R. Sequential backbone assignment based on dipolar amide-to-amide correlation experiments. J Biomol NMR. 2015;62:303–11.

    Article  CAS  Google Scholar 

  83. Chevelkov V, Habenstein B, Loquet A, Giller K, Becker S, Lange A. Proton-detected MAS NMR experiments based on dipolar transfers for backbone assignment of highly deuterated proteins. J Magn Reson. 2014;242:180–8.

    Article  CAS  Google Scholar 

  84. Cole HBR, Torchia DA. An NMR-study of the backbone dynamics of staphylococcal nuclease in the crystalline state. Chem Phys. 1991;158:271–81.

    Article  CAS  Google Scholar 

  85. Giraud N, Böckmann A, Lesage A, Penin F, Blackledge M, Emsley L. Site-specific backbone dynamics from a crystalline protein by solid-state NMR spectroscopy. J Am Chem Soc. 2004;126:11422–3.

    Article  CAS  Google Scholar 

  86. Giraud N, Blackledge M, Goldman M, Böckmann A, Lesage A, Penin F, Emsley L. Quantitative analysis of backbone dynamics in a crystalline protein from nitrogen-15 spin-lattice relaxation. J Am Chem Soc. 2005;127:18190–201.

    Article  CAS  Google Scholar 

  87. 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. 2007;184:51–61.

    Article  CAS  Google Scholar 

  88. Schanda P, Meier BH, Ernst M. Quantitative analysis of protein backbone dynamics in microcrystalline ubiquitin by solid-state NMR spectroscopy. J Am Chem Soc. 2010;132:15957–67.

    Article  CAS  Google Scholar 

  89. 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. 2008;128:052316.

    Article  CAS  Google Scholar 

  90. Reif B, Xue Y, Agarwal V, Pavlova MS, Hologne M, Diehl A, Ryabov YE, Skrynnikov NR. Protein side-chain dynamics observed by solution- and solid-state NMR: comparative analysis of methyl 2H relaxation data. J Am Chem Soc. 2006;128:12354–5.

    Article  CAS  Google Scholar 

  91. Chevelkov V, Zhuravleva AV, Xue Y, Reif B, Skrynnikov NR. Combined analysis of 15N relaxation data from solid- and solution-state NMR spectroscopy. J Am Chem Soc. 2007;129:12594–5.

    Article  CAS  Google Scholar 

  92. Chevelkov V, Xue Y, Linser R, Skrynnikov NR, Reif B. Comparison of solid-state dipolar couplings and solution relaxation data provides insight into protein backbone dynamics. J Am Chem Soc. 2010;132:5015–7.

    Article  CAS  Google Scholar 

  93. Cavanagh J, Fairbrother WJ, Palmer AG, Skelton NJ. Protein NMR spectroscopy: principles and practice, in. San Diego: Academic; 1996.

    Google Scholar 

  94. Torchia DA, Szabo A. Spin-lattice relaxation in solids. J Magn Reson. 1982;49:107–21.

    CAS  Google Scholar 

  95. Chekmenev EY, Zhang Q, Waddell KW, Mashuta MS, Wittebort RJ. 15N chemical shielding in glycyl tripeptides: measurement by solid-state NMR and correlation with X-ray structure. J Am Chem Soc. 2004;126:379–84.

    Article  CAS  Google Scholar 

  96. Franks WT, Zhou DH, Wylie BJ, Money BG, Graesser DT, Frericks HL, Gurmukh S, Rienstra CM. Magic-angle spinning solid-state NMR spectroscopy of the beta 1 immunoglobulin binding domain of protein G (GB1): 15N and 13C chemical shift assignments and conformational analysis. J Am Chem Soc. 2005;127:12291–305.

    Article  CAS  Google Scholar 

  97. Hall JB, Fushman D. Variability of the N-15 chemical shielding tensors in the B3 domain of protein G from N-15 relaxation measurements at several fields. Implications for backbone order parameters. J Am Chem Soc. 2006;128:7855–70.

    Article  CAS  Google Scholar 

  98. Wylie BJ, Franks WT, Rienstra CM. Determinations of N-15 chemical shift anisotropy magnitudes in a uniformly N-15, C-13-labeled microcrystalline protein by three-dimensional magic-angle spinning nuclear magnetic resonance spectroscopy. J Phys Chem B. 2006;110:10926–36.

    Article  CAS  Google Scholar 

  99. Wylie BJ, Sperling LJ, Frericks HL, Shah GJ, Franks WT, Rienstra CM. Chemical-shift anisotropy measurements of amide and carbonyl resonances in a microcrystalline protein with slow magic-angle spinning NMR spectroscopy. J Am Chem Soc. 2007;129:5318–9.

    Article  CAS  Google Scholar 

  100. Yao L, Vögeli B, Ying J, Bax A. NMR determination of amide N–H equilibrium bond length from concerted dipolar coupling measurements. J Am Chem Soc. 2008;130:16518–20.

    Article  CAS  Google Scholar 

  101. Lopez del Amo J-M, Fink U, Reif B. Quantification of protein backbone hydrogen-deuterium exchange rates by MAS solid-state NMR spectroscopy. J Biomol NMR. 2010;48:203–12.

    Article  CAS  Google Scholar 

  102. Chevelkov V, Faelber K, Schrey A, Rehbein K, Diehl A, Reif B. Differential line broadening in MAS solid-state NMR due to dynamic interference. J Am Chem Soc. 2007;129:10195–200.

    Article  CAS  Google Scholar 

  103. Duma L, Hediger S, Lesage A, Sakellariou D, Emsley L. Carbon-13 lineshapes in solid-state NMR of labeled compounds. Effects of coherent CSA-dipolar cross-correlation. J Magn Reson. 2003;162:90–101.

    Article  CAS  Google Scholar 

  104. Griffey D, Redfield A. Proton-deteceted heteronuclear edited and correlated nuclear-magnetic-resonance and nuclear Overhauser effect in solution. Q Rev Biophys. 1987;19:51–82.

    Article  CAS  Google Scholar 

  105. Harris RK, Packer KJ, Thayer AM. Slow magic-angle rotation 13C NMR studies of solid phosphonium iodides. The interplay of dipolar, shielding and indirect coupling tensors. J Magn Reson. 1985;62:284–97.

    CAS  Google Scholar 

  106. Igumenova TI, McDermott AE. Improvement of resolution in solid state NMR spectra with J-decoupling: an analysis of lineshape contributions in uniformly 13C-enriched amino acids and proteins. J Magn Reson. 2003;164:270–85.

    Article  CAS  Google Scholar 

  107. Wu G, Sun B, Wasylishen RE, Griffin RG. Spinning sidebands in slow-magic-angle-spinning NMR spectra arising from tightly J-coupled spin pairs. J Magn Reson. 1997;124:366–71.

    Article  CAS  Google Scholar 

  108. Zilm KW, Grant DM. Carbon-13 dipolar spectroscopy of small organic molecules in argon matrices. J Am Chem Soc. 1981;103:2913–22.

    Article  CAS  Google Scholar 

  109. Maricq MM, Waugh JS. NMR in rotating solids. J Chem Phys. 1979;70:3300–16.

    Article  CAS  Google Scholar 

  110. Skrynnikov NR. Asymmetric doublets in MAS NMR: coherent and incoherent mechanisms. Magn Reson Chem. 2007;45:S161–73.

    Article  CAS  Google Scholar 

  111. Pervushin K, Riek R, Wider G, Wüthrich K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci U S A. 1997;94:12366–71.

    Article  CAS  Google Scholar 

  112. Reif B, Hennig M, Griesinger C. Direct measurement of angles between bond vectors in high-resolution NMR. Science. 1997;276:1230–3.

    Article  CAS  Google Scholar 

  113. Reif B, Diener A, Hennig M, Maurer M, Griesinger C. Cross correlated relaxation for the measurement of angles between tensorial interactions. J Magn Reson. 2000;143:45–68.

    Article  CAS  Google Scholar 

  114. Tjandra N, Szabo A, Bax A. Protein backbone dynamics and 15N chemical shift anisotropy from quantitative measurement of relaxation interference effects. J Am Chem Soc. 1996;118:6986–91.

    Article  CAS  Google Scholar 

  115. Chevelkov V, Diehl A, Reif B. Quantitative measurement of differential 15N-Hα/β T2 relaxation times in a perdeuterated protein by MAS solid-state NMR spectroscopy. Magn Reson Chem. 2007;45:S156–60.

    Article  CAS  Google Scholar 

  116. Linser R, Fink U, Reif B. Assignment of dynamic regions in biological solids enabled by spin-state selective NMR experiments. J Am Chem Soc. 2010;132:8891–3.

    Article  CAS  Google Scholar 

  117. Chevelkov V, Reif B. TROSY effects in MAS solid-state NMR. Concepts NMR. 2008;32A:143–56.

    CAS  Google Scholar 

  118. Kurauskas V, Weber E, Hessel A, Ayala I, Marion D, Schanda P. Cross-correlated relaxation of dipolar coupling and chemical-shift anisotropy in magic-angle spinning R-1 rho NMR measurements: application to protein backbone dynamics measurements. J Phys Chem B. 2016;120:8905–13.

    Article  CAS  Google Scholar 

  119. Cady SD, Hong M. Effects of amantadine on the dynamics of membrane-bound influenza A M2 transmembrane peptide studied by NMR relaxation. J Biomol NMR. 2009;45:185–96.

    Article  CAS  Google Scholar 

  120. Krushelnitsky A, Zinkevich T, Reichert D, Chevelkov V, Reif B. Microsecond time scale mobility in a solid protein as studied by the N-15 R-1 rho site-specific NMR relaxation rates. J Am Chem Soc. 2010;132:11850–3.

    Article  CAS  Google Scholar 

  121. Ma PX, Haller JD, Zajakala J, Macek P, Sivertsen AC, Willbold D, Boisbouvier J, Schanda P. Probing transient conformational states of proteins by solid-state R11 relaxation- dispersion NMR spectroscopy. Angew Chem Int Ed. 2014;53:4312–7.

    Article  CAS  Google Scholar 

  122. Ma PX, Xue Y, Coquelle N, Haller JD, Yuwen TR, Ayala I, Mikhailovskii O, Willbold D, Colletier JP, Skrynnikov NR, Schanda P. Observing the overall rocking motion of a protein in a crystal. Nat Commun. 2015;6:8361.

    Article  CAS  Google Scholar 

  123. Quinn CM, McDermott AE. Monitoring conformational dynamics with solid-state R (1 rho) experiments. J Biomol NMR. 2009;45:5–8.

    Article  CAS  Google Scholar 

  124. Krushelnitsky A, de Azevedo E, Linser R, Reif B, Saalwächter K, Reichert D. Direct observation of millisecond to second motions in proteins by dipolar CODEX NMR. J Am Chem Soc. 2009;131:12097–9.

    Article  CAS  Google Scholar 

  125. Lorieau JL, McDermott AE. Conformational flexibility of a microcrystalline globular protein: order parameters by solid-state NMR spectroscopy. J Am Chem Soc. 2006;128:11505–12.

    Article  CAS  Google Scholar 

  126. Lorieau JL, McDermott AE. Order parameters based on (CH)–C-13-H-1, (CH2)–C-13-H-1 and (CH3)–C-13-H-1 heteronuclear dipolar powder patterns: a comparison of MAS-based solid-state NMR sequences. Magn Reson Chem. 2006;44:334–47.

    Article  CAS  Google Scholar 

  127. Lorieau JL, Day LA, McDermott AE. Conformational dynamics of an intact virus: order parameters for the coat protein of Pf1 bacteriophage. Proc Natl Acad Sci U S A. 2008;105:10366–71.

    Article  Google Scholar 

  128. 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. 2009;131:14018–22.

    Article  CAS  Google Scholar 

  129. Dvinskikh SV, Zimmermann H, Maliniak A, Sandstrom D. Heteronuclear dipolar recoupling in liquid crystals and solids by PISEMA-type pulse sequences. J Magn Reson. 2003;164:165–70.

    Article  CAS  Google Scholar 

  130. Dvinskikh SV, Zimmermann H, Maliniak A, Sandström D. Heteronuclear dipolar recoupling in solid-state nuclear magnetic resonance by amplitude-, phase-, and frequency-modulated Lee–Goldburg cross-polarization. J Chem Phys. 2005;122:044512.

    Article  CAS  Google Scholar 

  131. Wu XL, Zilm KW. Cross-polarization with high-speed magic-angle spinning. J Magn Reson A. 1993;104:154–65.

    Article  CAS  Google Scholar 

  132. Schanda P, Meier BH, Ernst M. Accurate measurement of one-bond H-X heteronuclear dipolar couplings in MAS solid-state NMR. J Magn Reson. 2011;210:246–59.

    Article  CAS  Google Scholar 

  133. Schanda P, Huber M, Boisbouvier J, Meier BH, Ernst M. Solid-state NMR measurements of asymmetric dipolar couplings provide insight into protein side-chain motion. Angew Chem Int Ed. 2011;50:11005–9.

    Article  CAS  Google Scholar 

  134. Chevelkov V, Fink U, Reif B. Quantitative analysis of backbone motion in proteins using MAS solid-state NMR spectroscopy. J Biomol NMR. 2009;45:197–206.

    Article  CAS  Google Scholar 

  135. Clore GM, Szabo A, Bax A, Kay LE, Driscoll PC, Gronenborn AM. Deviations from the simple 2-parameter model-free approach to the interpretation of N-15 nuclear magnetic relaxation of proteins. J Am Chem Soc. 1990;112:4989–91.

    Article  CAS  Google Scholar 

  136. Lipari G, Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc. 1982;104:4546–59.

    Article  CAS  Google Scholar 

  137. Schanda P, Ernst M. Studying dynamics by magic-angle spinning solid-state NMR spectroscopy: principles and applications to biomolecules. Prog NMR Spect. 2016;96:1–46.

    Article  CAS  Google Scholar 

  138. Klement K, Wieligmann K, Meinhardt J, Hortschansky P, Richter W, Fandrich M. Effect of different salt ions on the propensity of aggregation and on the structure of Alzheimer’s abeta(1–40) amyloid fibrils. J Mol Biol. 2007;373:1321–33.

    Article  CAS  Google Scholar 

  139. Paravastu AK, Leapman RD, Yau W-M, Tycko R. Molecular structural basis for polymorphism in Alzheimer’s beta-amyloid fibrils. Proc Natl Acad Sci U S A. 2008;105:18349–54.

    Article  Google Scholar 

  140. Petkova AT, Leapman RD, Guo ZH, Yau WM, Mattson MP, Tycko R. Self-propagating, molecular-level polymorphism in Alzheimer’s β-amyloid fibrils. Science. 2005;307:262–5.

    Article  CAS  Google Scholar 

  141. Linser R, Dasari M, Hiller M, Higman V, Fink U, Lopez del Amo J-M, Handel L, Kessler B, Schmieder P, Oesterhelt D, Oschkinat H, Reif B. Proton detected solid-state NMR of fibrillar and membrane proteins. Angew Chem Int Ed. 2011;50:4508–12.

    Article  CAS  Google Scholar 

  142. Dasari M, Espargaro A, Sabate R, Lopez del Amo JM, Fink U, Grelle G, Bieschke J, Ventura S, Reif B. Bacterial inclusion bodies of the Alzheimer disease beta-amyloid peptides can be employed to study native like aggregation intermediate states. ChemBioChem. 2011;12:407–23.

    Article  CAS  Google Scholar 

  143. Carulla N, Caddy GL, Hall DR, Zurdo J, Gairi M, Feliz M, Giralt E, Robinson CV, Dobson CM. Molecular recycling within amyloid fibrils. Nature. 2005;436:554–8.

    Article  CAS  Google Scholar 

  144. Fawzi NL, Ying JF, Torchia DA, Clore GM. Kinetics of amyloid beta monomer-to-oligomer exchange by NMR relaxation. J Am Chem Soc. 2010;132:9948–51.

    Article  CAS  Google Scholar 

  145. Fawzi NL, Ying J, Ghirlando R, Torchia DA, Clore GM. Atomic-resolution dynamics on the surface of amyloid-beta protofibrils probed by solution NMR. Nature. 2011;480:268–72.

    Article  CAS  Google Scholar 

  146. Narayanan S, Reif B. Characterization of chemical exchange between soluble and aggregated states of beta-amyloid by solution state NMR upon variation of the salt conditions. Biochemistry. 2005;44:1444–52.

    Article  CAS  Google Scholar 

  147. Qiang W, Kelley K, Tycko R. Polymorph-specific kinetics and thermodynamics of beta-amyloid fibril growth. J Am Chem Soc. 2013;135:6860–71.

    Article  CAS  Google Scholar 

  148. Helmus JJ, Surewicz K, Nadaud PS, Surewicz WK, Jaroniec CP. Molecular conformation and dynamics of the Y145Stop variant of human prion protein in amyloid fibrils. Proc Natl Acad Sci U S A. 2008;105:6284–9.

    Article  Google Scholar 

  149. Helmus JJ, Surewicz K, Surewicz WK, Jaroniec CP. Conformational flexibility of Y145Stop human prion protein amyloid fibrils probed by solid-state nuclear magnetic resonance spectroscopy. J Am Chem Soc. 2010;132:2393–403.

    Article  CAS  Google Scholar 

  150. Zhou DH, Nieuwkoop AJ, Berthold DA, Comellas G, Sperling LJ, Tang M, Shah GJ, Brea EJ, Lemkau LR, Rienstra CM. Solid-state NMR analysis of membrane proteins and protein aggregates by proton detected spectroscopy. J Biomol NMR. 2012;54:291–305.

    Article  CAS  Google Scholar 

  151. Morris VK, Linser R, Wilde KL, Duff AP, Sunde M, Kwan AH. Solid-state NMR spectroscopy of functional amyloid from a fungal hydrophobin: a well-ordered beta-sheet core amidst structural heterogeneity. Angew Chem Int Ed. 2012;51:12621–5.

    Article  CAS  Google Scholar 

  152. Linser R, Sarkar R, Krushelnitzky A, Mainz A, Reif B. Dynamics in the solid-state: perspectives for the investigation of amyloid aggregates, membrane proteins and soluble protein complexes. J Biomol NMR. 2014;59:1–14.

    Article  CAS  Google Scholar 

  153. Lopez del Amo J-M, Dasari M, Fink U, Grelle G, Wanker EE, Bieschke J, Reif B. Structural properties of EGCG induced, non-toxic Alzheimer’s disease Aβ oligomers. J Mol Biol. 2012;421:517–24.

    Article  CAS  Google Scholar 

  154. Lopez del Amo JM, Schmidt M, Fink U, Dasari M, Fändrich M, Reif B. The basic subunit in Alzheimer’s disease beta-amyloid fibrils can be an asymmetric dimer. Angew Chem Int Ed Eng. 2012;51:6136–9.

    Article  CAS  Google Scholar 

  155. Agarwal V, Linser R, Dasari M, Fink U, Lopez del Amo J-M, Reif B. Hydrogen bonding involving side chain exchangeable groups stabilizes amyloid quarternary structure. Phys Chem Chem Phys. 2013;15:12551–7.

    Article  CAS  Google Scholar 

  156. Park SH, Das BB, Casagrande F, Tian Y, Nothnagel HJ, Chu M, Kiefer H, Maier K, De Angelis AA, Marassi FM, Opella SJ. Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature. 2012;491:779.

    Article  CAS  Google Scholar 

  157. Shahid SA, Bardiaux B, Franks WT, Krabben L, Habeck M, van Rossum B-J, Linke D. Membrane-protein structure determination by solid-state NMR spectroscopy of microcrystals. Nat Methods. 2012;9:1212–U1119.

    Article  CAS  Google Scholar 

  158. Agarwal V, Fink U, Schuldiner S, Reif B. MAS solid-state NMR studies on the multidrug transporer EmrE. BBA-Bioenergetics. 2007;1768:3036–43.

    CAS  Google Scholar 

  159. Jacso T, Franks WT, Rose H, Fink U, Broecker J, Keller S, Oschkinat H, Reif B. 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. 2012;51:432–5.

    Article  CAS  Google Scholar 

  160. Renault M, Pawsey S, Bos MP, Koers EJ, Nand D, Tommassen-van Boxtel R, Rosay M, Tommassen J, Maas WE, Baldus M. Solid-state NMR spectroscopy on cellular preparations enhanced by dynamic nuclear polarization. Angew Chem Int Ed Eng. 2011;51:2998–3001.

    Article  CAS  Google Scholar 

  161. Takahashi H, Ayala I, Bardet M, De Paepe G, Simorre J-P, Hediger S. Solid-state NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization. J Am Chem Soc. 2013;135:5105–10.

    Article  CAS  Google Scholar 

  162. Wang T, Park YB, Caporini MA, Rosay M, Zhong L, Cosgrove DJ, Hong M. Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc Natl Acad Sci U S A. 2013;110:16444–9.

    Article  Google Scholar 

  163. Hall DA, Maus DC, Gerfen GJ, Inati SJ, Becerra LR, Dahlquist FW, Griffin RG. Polarization-enhanced NMR spectroscopy of biomolecules in frozen solution. Science. 1997;276:930–2.

    Article  CAS  Google Scholar 

  164. Patzelt H, Ulrich AS, Egbringhoff H, Dux P, Ashurst J, Simon B, Oschkinat H, Oesterhelt D. Towards structural investigations on isotope labelled native bacteriorhodopsin in detergent micelles by solution-state NMR spectroscopy. J Biomol NMR. 1997;10:95–106.

    Article  CAS  Google Scholar 

  165. Hiller M, Krabben L, Vinothkumar KR, Castellani F, Van Rossum B, Kühlbrandt W, Oschkinat H. Solid-state magic-angle spinning NMR of outer-membrane protein G from Escherichia coli. ChemBioChem. 2005;6:1679–84.

    Article  CAS  Google Scholar 

  166. Ward ME, Shi L, Lake E, Krishnamurthy S, Hutchins H, Brown LS, Ladizhansky V. Proton-detected solid-state NMR reveals intramembrane polar networks in a seven-helical transmembrane protein proteorhodopsin. J Am Chem Soc. 2011;133:17434–43.

    Article  CAS  Google Scholar 

  167. Saurel O, Iordanov I, Nars G, Demange P, Marchand TL, Andreas LB, Pintacuda G, Milon A. Local and global dynamics in Klebsiella pneumoniae outer membrane protein a in lipid bilayers probed at atomic resolution. J Am Chem Soc. 2017;139:1590–1597.

    Article  CAS  Google Scholar 

  168. Andreas LB, Reese M, Eddy MT, Gelev V, Ni QZ, Miller EA, Emsley L, Pintacuda G, Chou JJ, Griffin RG. Structure and mechanism of the influenza A M2(18-60) dimer of dimers. J Am Chem Soc. 2015;137:14877–86.

    Article  CAS  Google Scholar 

  169. Medeiros-Silva J, Mance D, Daniels M, Jekhmane S, Houben K, Baldus M, Weingarth M. H-1-detected solid-state NMR studies of water-inaccessible proteins invitro and insitu. Angew Chem Int Ed Eng. 2016;55:13606–10.

    Article  CAS  Google Scholar 

  170. Austin RH, Chan SS, Jovin TM. Rotational diffusion of cell-surface components by time-resolved phosphoresence anisotropy. Proc Natl Acad Sci U S A. 1979;76:5650–4.

    Article  CAS  Google Scholar 

  171. Cherry RJ. Rotational and lateral diffusion of membrane proteins. Biochim Biophys Acta. 1979;559:289–327.

    Article  CAS  Google Scholar 

  172. Cherry RJ. Membrane protein dynamics: rotational dynamics. In: Yeagle PL, editor. The structure of biological membranes. Boca Raton: CRC Press; 2005.

    Google Scholar 

  173. Saffman PG, Delbruck M. Brownian motion in biological membranes. Proc Natl Acad Sci U S A. 1975;72:3111–3.

    Article  CAS  Google Scholar 

  174. Park SH, Mrse AA, Nevzorov AA, De Angelis AA, Opella SJ. Rotational diffusion of membrane proteins in aligned phospholipid bilayers by solid-state NMR spectroscopy. J Magn Reson. 2006;178:162–5.

    Article  CAS  Google Scholar 

  175. Lu GJ, Park SH, Opella SJ. Improved H-1 amide resonance line narrowing in oriented sample solid-state NMR of membrane proteins in phospholipid bilayers. J Magn Reson. 2012;220:54–61.

    Article  CAS  Google Scholar 

  176. Cady SD, Goodman C, Tatko CD, DeGrado WF, Hong M. Determining the orientation of uniaxially rotating membrane proteins using unoriented samples: a (2)H, (13)C, and (15)N solid-state NMR investigation of the dynamics and orientation of a transmembrane helical bundle. J Am Chem Soc. 2007;129:5719–29.

    Article  CAS  Google Scholar 

  177. Hong M, Doherty T. Orientation determination of membrane-disruptive proteins using powder samples and rotational diffusion: a simple solid-state NMR approach. Chem Phys Lett. 2006;432:296–300.

    Article  CAS  Google Scholar 

  178. Good DB, Wang S, Ward ME, Struppe J, Brown LS, Lewandowski JR, Ladizhansky V. Conformational dynamics of a seven transmembrane helical protein anabaena sensory rhodopsin probed by solid-state NMR. J Am Chem Soc. 2014;136:2833–42.

    Article  CAS  Google Scholar 

  179. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK. Structure of bacteriorhodopsin at 1.55 angstrom resolution. J Mol Biol. 1999;291:899–911.

    Article  CAS  Google Scholar 

  180. Sapra KT, Besir S, Oesterhelt D, Muller DJ. Characterizing molecular interactions in different bacteriorhodopsin assemblies by single-molecule force spectroscopy. J Mol Biol. 2006;355:640–50.

    Article  CAS  Google Scholar 

  181. Klyszejko AL, Shastri S, Mari SA, Grubmuller H, Muller DJ, Glaubitz C. Folding and assembly of proteorhodopsin. J Mol Biol. 2008;376:35–41.

    Article  CAS  Google Scholar 

  182. Andrew ER, Bradbury A, Eades RG. NMR spectra recorded from a crystal rotated at high speed. Nature. 1958;182:1659.

    Article  CAS  Google Scholar 

  183. Mainz A, Jehle S, van Rossum BJ, Oschkinat H, Reif B. Large protein complexes with extreme rotational correlation times investigated in solution by magic-angle-spinning NMR spectroscopy. J Am Chem Soc. 2009;131:15968–9.

    Article  CAS  Google Scholar 

  184. Mainz A, Bardiaux B, Kuppler F, Multhaup G, Felli IC, Pierattelli R, Reif B. Structural and mechanistic implications of metal-binding in the small heat-shock protein αB-crystallin. J Biol Chem. 2012;287:1128–38.

    Article  CAS  Google Scholar 

  185. Bertini I, Luchinat C, Parigi G, Ravera E, Reif B, Turano P. Solid-state NMR of proteins sedimented by ultracentrifugation. Proc Natl Acad Sci U S A. 2011;108:10396–9.

    Article  Google Scholar 

  186. Ravera E, Parigi G, Mainz A, Religa TL, Reif B, Luchinat C. Experimental determination of microsecond reorientation correlation times in protein solutions. J Phys Chem B. 2013;117:3548–53.

    Article  CAS  Google Scholar 

  187. Linser R. Backbone assignment of perdeuterated proteins using long-range H/C-dipolar transfers. J Biomol NMR. 2012;52:151–8.

    Article  CAS  Google Scholar 

  188. Mainz A, Religa T, Sprangers R, Linser R, Kay LE, Reif B. NMR spectroscopy of soluble protein complexes at one mega-dalton and beyond. Angew Chem Int Ed Eng. 2013;52:8746–51.

    Article  CAS  Google Scholar 

  189. Aquilina JA, Benesch JLP, Bateman OA, Slingsby C, Robinson CV. Polydispersity of a mammalian chaperone: mass spectrometry reveals the population of oligomers in alpha B-crystallin. Proc Natl Acad Sci U S A. 2003;100:10611–6.

    Article  CAS  Google Scholar 

  190. Horwitz J. Alpha crystallin: the quest for a homogeneous quaternary structure. Exp Eye Res. 2009;88:190–4.

    Article  CAS  Google Scholar 

  191. Barbet-Massin E, Huang C-T, Daebel V, Hsu S-TD, Reif B. Site-specific solid-state NMR studies of “trigger factor” in complex with the large ribosomal subunit 50S. Angew Chem Int Ed Eng. 2015;54:4367–9.

    Article  CAS  Google Scholar 

  192. Kurauskas V, Crublet E, Macek P, Kerfah R, Gauto DF, Boisbouvier J, Schanda P. Sensitive proton-detected solid-state NMR spectroscopy of large proteins with selective CH3 labelling: application to the 50S ribosome subunit. Chem Commun. 2016;52:9558–61.

    Article  CAS  Google Scholar 

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  1. Munich Center for Integrated Protein Science (CIPSM) at Department Chemie, Technische Universität München, Lichtenbergstr. 4, 85747, Garching, Germany

    Bernd Reif

  2. Helmholtz-Zentrum München (HMGU), German Research Center for Environmental Health, Ingolstädter Landstr. 1, 85764, Neuherberg, Germany

    Bernd Reif

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    Graham A. Webb

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Reif, B. (2018). Proton-Detection in Biological MAS Solid-State NMR Spectroscopy. In: Webb, G. (eds) Modern Magnetic Resonance. Springer, Cham. https://doi.org/10.1007/978-3-319-28388-3_69

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