Advertisement

Journal of Biomolecular NMR

, Volume 59, Issue 1, pp 1–14 | Cite as

Dynamics in the solid-state: perspectives for the investigation of amyloid aggregates, membrane proteins and soluble protein complexes

  • Rasmus Linser
  • Riddhiman Sarkar
  • Alexey Krushelnitzky
  • Andi Mainz
  • Bernd ReifEmail author
Perspective

Abstract

Aggregates formed by amyloidogenic peptides and proteins and reconstituted membrane protein preparations differ significantly in terms of the spectral quality that they display in solid-state NMR experiments. Structural heterogeneity and dynamics can both in principle account for that observation. This perspectives article aims to point out challenges and limitations, but also potential opportunities in the investigation of these systems.

Keywords

MAS solid-state NMR Protein dynamics Amyloid fibrils Membrane proteins Soluble protein complexes 

Notes

Acknowledgments

This work was performed in the framework of SFB-1035/Project-B07 (German Research Foundation, DFG). This research was supported by the Helmholtz-Gemeinschaft, and the DFG (Re1435). We are grateful to the Center for Integrated Protein Science Munich (CIPS-M) for financial support. RL acknowledges the Australian Research Council for financial support in terms of a Discovery Early Career Researcher Award.

References

  1. Abramov E, Dolev I, Fogel H, Ciccotosto GD, Ruff E, Slutsky I (2009) Amyloid-beta as a positive endogenous regulator of release probability at hippocampal synapses. Nat Neurosci 12:U1120–U1567Google Scholar
  2. Agarwal V, Fink U, Schuldiner S, Reif B (2007) MAS solid-state NMR studies on the multidrug transporer EmrE. BBA—Biomembranes 1768:3036–3043Google Scholar
  3. Agarwal V, Faelber K, Schmieder P, Reif B (2009) High-resolution double-quantum deuterium magic angle spinning solid-state nmr spectroscopy of perdeuterated proteins. J Am Chem Soc 131:2–3Google Scholar
  4. Agarwal V, Linser R, Dasari M, Fink U, Lopez del Amo J-M, Reif B (2013) Hydrogen bonding involving side chain exchangeable groups stabilizes amyloid quarternary structure. Phys Chem Chem Phys 15:12551–12557Google Scholar
  5. Akasaka K, Ganapathy S, McDowell CA, Naito A (1983) Spin–spin and spin-lattice contributions to the rotating frame relaxation of C-13 in l-alanine. J Chem Phys 78:3567–3572ADSGoogle Scholar
  6. Akasaka K, Li H, Yamada H, Li RH, Thoresen T, Woodward CK (1999) Pressure response of protein backbone structure. Pressure-induced amide N-15 chemical shifts in BPTI. Protein Sci 8:1946–1953Google Scholar
  7. Akbey Ü, Lange S, Franks TW, Linser R, Diehl A, van Rossum BJ, Reif B, Oschkinat H (2010) Optimum levels of exchangeable protons in perdeuterated proteins for proton detection in MAS solid-state NMR spectroscopy. J Biomol NMR 46:67–73Google Scholar
  8. Alla M, Eckman R, Pines A (1980) Spin diffusion and spin-lattice relaxation of deuterium in rotating solids. Chem Phys Lett 71:148–151ADSGoogle Scholar
  9. Andrew ER, Bradbury A, Eades RG (1958) NMR spectra recorded from a crystal rotated at high speed. Nature 182:1659ADSGoogle Scholar
  10. Anfinsen CB (1973) Principles that govern folding of protein chains. Science 181:223–230ADSGoogle Scholar
  11. Arnold MR, Kremer W, Ludemann HD, Kalbitzer HR (2002) H-1-NMR parameters of common amino acid residues measured in aqueous solutions of the linear tetrapeptides Gly-Gly-X-Ala at pressures between 0.1 and 200 MPa. Biophys Chem 96:129–140Google Scholar
  12. Asami S, Reif B (2013) Proton-detected solid-state NMR at aliphatic sites: applications to crystalline systems. Acc Chem Res 46:2089–2097Google Scholar
  13. Asami S, Schmieder P, Reif B (2010) High resolution 1H-detected solid-state NMR spectroscopy of protein aliphatic resonances: access to tertiary structure information. J Am Chem Soc 132:15133–15135Google Scholar
  14. Austin RH, Chan SS, Jovin TM (1979) Rotational diffusion of cell-surface components by time-resolved phosphoresence anisotropy. Proc Natl Acad Sci USA 76:5650–5654ADSGoogle Scholar
  15. Bertini I, Luchinat C, Parigi G, Ravera E, Reif B, Turano P (2011) Solid-state NMR of proteins sedimented by ultracentrifugation. Proc Natl Acad Sci USA 108:10396–10399ADSGoogle Scholar
  16. Bocan J, Pileio G, Levitt MH (2012) Sensitivity enhancement and low-field spin relaxation in singlet NMR. Phys Chem Chem Phys 14:16032–16040Google Scholar
  17. Cady SD, Goodman C, Tatko CD, DeGrado WF, Hong M (2007) 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 129:5719–5729Google Scholar
  18. Carulla N, Caddy GL, Hall DR, Zurdo J, Gairi M, Feliz M, Giralt E, Robinson CV, Dobson CM (2005) Molecular recycling within amyloid fibrils. Nature 436:554–558ADSGoogle Scholar
  19. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, Normark S, Hultgren SJ (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851–855ADSGoogle Scholar
  20. Chen K-YM, Zhou F, Fryszczyn BG, Barth P (2012) Naturally evolved G protein-coupled receptors adopt metastable conformations. Proc Natl Acad Sci USA 109:13284–13289ADSGoogle Scholar
  21. Cherry RJ (1979) Rotational and lateral diffusion of membrane proteins. Biochim Biophys Acta 559:289–327Google Scholar
  22. Cherry RJ (2005) Membrane protein dynamics: rotational dynamics. In: Yeagle PL (ed) The structure of biological membranes. CRC Press, Boca RatonGoogle Scholar
  23. Chevelkov V, Rehbein K, Diehl A, Reif B (2006) Ultra-high resolution in proton solid-state NMR at high levels of deuteration. Angew Chem Int Ed 45:3878–3881Google Scholar
  24. Chevelkov V, Diehl A, Reif B (2007a) Quantitative measurement of differential 15N-Hα/β T2 relaxation times in a perdeuterated protein by MAS solid-state NMR spectroscopy. Magn Res Chem 45:S156–S160Google Scholar
  25. Chevelkov V, Faelber K, Schrey A, Rehbein K, Diehl A, Reif B (2007b) Differential line broadening in MAS solid-state NMR due to dynamic interference. J Am Chem Soc 129:10195–10200Google Scholar
  26. Chevelkov V, Zhuravleva AV, Xue Y, Reif B, Skrynnikov NR (2007c) Combined analysis of 15 N relaxation data from solid- and solution-state NMR spectroscopy. J Am Chem Soc 129:12594–12595Google Scholar
  27. Chevelkov V, Diehl A, Reif B (2008) Measurement of 15N–T1 relaxation rates in a perdeuterated protein by MAS solid-state NMR spectroscopy. J Chem Phys 128:052316ADSGoogle Scholar
  28. Chevelkov V, Fink U, Reif B (2009a) Accurate determination of order parameters from 1H,15N dipolar couplings in MAS solid-state NMR experiments. J Am Chem Soc 131:14018–14022Google Scholar
  29. Chevelkov V, Fink U, Reif B (2009b) Quantitative analysis of backbone motion in proteins using MAS solid-state NMR spectroscopy. J Biomol NMR 45:197–206Google Scholar
  30. Chevelkov V, Xue Y, Linser R, Skrynnikov NR, Reif B (2010) Comparison of solid-state dipolar couplings and solution relaxation data provides insight into protein backbone dynamics. J Am Chem Soc 132:5015–5017Google Scholar
  31. Cole R, Loria JP (2002) Evidence for flexibility in the function of ribonuclease A. Biochemistry 41:6072–6081Google Scholar
  32. Cowans BA, Grutzner JB (1993) Examination of homogeneous broadening in solids via rotationally synchronized spin-echo NMR-spectroscopy. J Magn Reson, Ser A 105:10–18ADSGoogle Scholar
  33. Fandrich M, Fletcher MA, Dobson CM (2001) Amyloid fibrils from muscle myoglobin—even an ordinary globular protein can assume a rogue guise if conditions are right. Nature 410:165–166ADSGoogle Scholar
  34. Fawzi NL, Ying JF, Torchia DA, Clore GM (2010) Kinetics of amyloid beta monomer-to-oligomer exchange by NMR relaxation. J Am Chem Soc 132:9948–9951Google Scholar
  35. Fawzi NL, Ying J, Ghirlando R, Torchia DA, Clore GM (2011) Atomic-resolution dynamics on the surface of amyloid-beta protofibrils probed by solution NMR. Nature 480:268–272ADSGoogle Scholar
  36. Ferella L, Luchinat C, Ravera E, Rosato A (2013) SedNMR: a web tool for optimizing sedimentation of macromolecular solutes for SSNMR. J Biomol NMR 57:319–326Google Scholar
  37. Fowler DM, Koulov AV, Alory-Jost C, Marks MS, Balch WE, Kelly JW (2006) Functional amyloid formation within mammalian tissue. PLoS Biol 4:100–107Google Scholar
  38. Gardiennet C, Schutz AK, Hunkeler A, Kunert B, Terradot L, Bockmann A, Meier BH (2012) A sedimented sample of a 59 kDa dodecameric helicase yields high-resolution solid-state NMR spectra. Angewandt Chem Int Edtk 51:7855–7858Google Scholar
  39. Garroway AN (1977) Homogeneous and inhomogeneous nuclear spin echoes in organic solids: adamantane. J Magn Reson 28:365–371ADSGoogle Scholar
  40. Gennis RB (1989) Biomembranes: molecular structure and function. Springer, New YorkGoogle Scholar
  41. Good DB, Wang S, Ward ME, Struppe J, Brown LS, Lewandowski JR, Ladizhansky V (2014) Conformational dynamics of a seven transmembrane helical protein anabaena sensory rhodopsin probed by solid-state NMR. J Am Chem Soc 136:2833–2842Google Scholar
  42. Greenwald J, Riek R (2012) On the possible amyloid origin of protein folds. J Mol Biol 421:417–426Google Scholar
  43. Halfmann R, Wright JR, Alberti S, Lindquist S, Rexach M (2012) Prion formation by a yeast GLFG nucleoporin. Prion 6:391–399Google Scholar
  44. Hall DA, Maus DC, Gerfen GJ, Inati SJ, Becerra LR, Dahlquist FW, Griffin RG (1997) Polarization-enhanced NMR spectroscopy of biomolecules in frozen solution. Science 276:930–932Google Scholar
  45. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, Fitzgerald KA, Latz E, Moore KJ, Golenbock DT (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 9:857–865Google Scholar
  46. Heck M, Hofmann KP (2001) Maximal rate and nucleotide dependence of rhodopsin-catalyzed transducin activation: initial rate analysis based on a double displacement mechanism. J Biol Chem 276:10000–10009Google Scholar
  47. Helmus JJ, Surewicz K, Nadaud PS, Surewicz WK, Jaroniec CP (2008) Molecular conformation and dynamics of the Y145Stop variant of human prion protein in amyloid fibrils. Proc Natl Acad Sci USA 105:6284–6289ADSGoogle Scholar
  48. Helmus JJ, Surewicz K, Surewicz WK, Jaroniec CP (2010) Conformational flexibility of Y145Stop human prion protein amyloid fibrils probed by solid-state nuclear magnetic resonance spectroscopy. J Am Chem Soc 132:2393–2403Google Scholar
  49. Henzler-Wildman KA, Lei M, Thai V, Kerns SJ, Karplus M, Kern D (2007a) A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450:913–916ADSGoogle Scholar
  50. Henzler-Wildman KA, Thai V, Lei M, Ott M, Wolf-Watz M, Fenn T, Pozharski E, Wilson MA, Petsko GA, Karplus M, Huebner CG, Kern D (2007b) Intrinsic motions along an enzymatic reaction trajectory. Nature 450:838–844ADSGoogle Scholar
  51. Hiller M, Krabben L, Vinothkumar KR, Castellani F, Van Rossum B, Kühlbrandt W, Oschkinat H (2005) Solid-state magic-angle spinning nmr of outer-membrane protein G from Escherichia coli. ChemBioChem 6:1679–1684Google Scholar
  52. Hologne M, Faelber K, Diehl A, Reif B (2005) Characterization of dynamics of perdeuterated proteins by MAS solid-state NMR. J Am Chem Soc 127:11208–11209Google Scholar
  53. Hologne M, Chevelkov V, Reif B (2006) Deuteration of peptides and proteins in MAS solid-state NMR. Prog NMR Spect 48:211–232Google Scholar
  54. Hong M, Doherty T (2006) Orientation determination of membrane-disruptive proteins using powder samples and rotational diffusion: a simple solid-state NMR approach. Chem Phys Lett 432:296–300ADSGoogle Scholar
  55. Jacso T, Franks WT, Rose H, Fink U, Broecker J, Keller S, Oschkinat H, Reif B (2012) 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 51:432–435Google Scholar
  56. Kato M, Han TNW, Xie S, Shi K, Du X, Wu LC, Mirzaei H, Goldsmith EJ, Longgood J, Pei J, Grishin NV, Frantz DE, Schneider JW, Chen S, Li L, Sawaya MR, Eisenberg D, Tycko R, McKnight SL (2012) Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149:753–767Google Scholar
  57. Kim HJ, Kim NC, Wang Y-D, Scarborough EA, Moore J, Diaz Z, MacLea KS, Freibaum B, Li S, Molliex A, Kanagaraj AP, Carter R, Boylan KB, Wojtas AM, Rademakers R, Pinkus JL, Greenberg SA, Trojanowski JQ, Traynor BJ, Smith BN, Topp S, Gkazi A-S, Miller J, Shaw CE, Kottlors M, Kirschner J, Pestronk A, Li YR, Ford AF, Gitler AD, Benatar M, King OD, Kimonis VE, Ross ED, Weihl CC, Shorter J, Taylor JP (2013) Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495–473: 467Google Scholar
  58. Kitahara R, Hata K, Li H, Williamson MP, Akasaka K (2013) Pressure-induced chemical shifts as probes for conformational fluctuations in proteins. Prog NMR Spect 71:35–58Google Scholar
  59. Klyszejko AL, Shastri S, Mari SA, Grubmuller H, Muller DJ, Glaubitz C (2008) Folding and assembly of proteorhodopsin. J Mol Biol 376:35–41Google Scholar
  60. Knight MJ, Pell AJ, Bertini I, Felli IC, Gonnelli L, Pierattelli R, Herrmann T, Emsley L, Pintacuda G (2012) Structure and backbone dynamics of a microcrystalline metalloprotein by solid-state NMR. Proc Natl Acad Sci USA 109:11095–11100ADSGoogle Scholar
  61. Krushelnitsky A, Zinkevich T, Reichert D, Chevelkov V, Reif B (2010) 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 132:11850–11853Google Scholar
  62. Labokha AA, Gradmann S, Frey S, Hulsmann BB, Urlaub H, Baldus M, Gorlich D (2013) Systematic analysis of barrier-forming FG hydrogels from Xenopus nuclear pore complexes. EMBO J 32:204–218Google Scholar
  63. Lange OF, Lakomek N-A, Fares C, Schroeder GF, Walter KFA, Becker S, Meiler J, Grubmueller H, Griesinger C, de Groot BL (2008) Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320:1471–1475ADSGoogle Scholar
  64. Le YY, Gong WH, Tiffany HL, Tumanov A, Nedospasov S, Shen WP, Dunlop NM, Gao JL, Murphy PM, Oppenheim JJ, Wang JM (2001) Amyloid beta(42) activates a G-protein-coupled chemoattractant receptor, FPR-Like-1. J Neurosci 21:RC123Google Scholar
  65. Lewandowski JR, Dumez JN, Akbey U, Lange S, Emsley L, Oschkinat H (2011a) Enhanced resolution and coherence lifetimes in the solid-state NMR spectroscopy of perdeuterated proteins under ultrafast magic-angle spinning. J Phys Chem Lett 2:2205–2211Google Scholar
  66. Lewandowski JR, Sass HJ, Grzesiek S, Blackledge M, Emsley L (2011b) Site-specific measurement of slow motions in proteins. J Am Chem Soc 133:16762–16765Google Scholar
  67. Linser R, Chevelkov V, Diehl A, Reif B (2007) Sensitivity enhancement using paramagnetic relaxation in MAS solid state NMR of perdeuterated proteins. J Magn Reson 189:209–216ADSGoogle Scholar
  68. Linser R, Fink U, Reif B (2010) Detection of dynamic regions in biological solids enabled by spin-state selective NMR experiments. J Am Chem Soc 132:8891–8893Google Scholar
  69. 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 (2011) Proton detected solid-state NMR of fibrillar and membrane proteins. Angew Chem Int Ed 50:4508–4512Google Scholar
  70. Lopez del Amo J-M, Dasari M, Fink U, Grelle G, Wanker EE, Bieschke J, Reif B (2012a) Structural properties of EGCG induced, non-toxic Alzheimer’s disease Aβ oligomers. J Mol Biol 421:517–524Google Scholar
  71. Lopez del Amo JM, Schmidt M, Fink U, Dasari M, Fändrich M, Reif B (2012b) The basic subunit in Alzheimer’s disease beta-amyloid fibrils can be an asymmetric dimer. Angew Chem Int Ed 51:6136–6139Google Scholar
  72. Lopez del Amo J-M, Schneider D, Loquet A, Lange A, Reif B (2013) Cryogenic solid state NMR studies of fibrils of the Alzheimer’s disease amyloid-β peptide: perspectives for DNP. J Biomol NMR 56:359–363Google Scholar
  73. Lu GJ, Park SH, Opella SJ (2012) Improved H-1 amide resonance line narrowing in oriented sample solid-state NMR of membrane proteins in phospholipid bilayers. J Magn Reson 220:54–61ADSGoogle Scholar
  74. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK (1999) Structure of bacteriorhodopsin at 1.55 angstrom resolution. J Mol Biol 291:899–911Google Scholar
  75. Maddelein ML, Dos Reis S, Duvezin-Caubet S, Coulary-Salin B, Saupe SJ (2002) Amyloid aggregates of the HET-s prion protein are infectious. Proc Natl Acad Sci USA 99:7402–7407ADSGoogle Scholar
  76. Mainz A, Jehle S, van Rossum BJ, Oschkinat H, Reif B (2009) Large protein complexes with extreme rotational correlation times investigated in solution by magic-angle-spinning NMR spectroscopy. J Am Chem Soc 131:15968–15969Google Scholar
  77. Mainz A, Bardiaux B, Kuppler F, Multhaup G, Felli IC, Pierattelli R, Reif B (2012) Structural and mechanistic implications of metal-binding in the small heat-shock protein αB-crystallin. J Biol Chem 287:1128–1138Google Scholar
  78. Mainz A, Religa T, Sprangers R, Linser R, Kay LE, Reif B (2013) NMR spectroscopy of soluble protein complexes at one mega-dalton and beyond. Angewandt Chem Int Edt 52:8746–8751Google Scholar
  79. Maji SK, Perrin MH, Sawaya MR, Jessberger S, Vadodaria K, Rissman RA, Singru PS, Nilsson KPR, Simon R, Schubert D, Eisenberg D, Rivier J, Sawchenko P, Vale W, Riek R (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325:328–332ADSGoogle Scholar
  80. Mollica L, Baias M, Lewandowski JR, Wylie BJ, Sperling LJ, Rienstra CM, Emsley L, Blackledge M (2012) Atomic-resolution structural dynamics in crystalline proteins from NMR and molecular simulation. J Phys Chem Lett 3:3657–3662Google Scholar
  81. Morris VK, Linser R, Wilde KL, Duff AP, Sunde M, Kwan AH (2012) Solid-state NMR spectroscopy of functional amyloid from a fungal hydrophobin: a well-ordered beta-sheet core amidst structural heterogeneity. Angewandt Chem Int Edt 51:12621–12625Google Scholar
  82. Narayanan S, Reif B (2005) Characterization of chemical exchange between soluble and aggregated states of beta-amyloid by solution state NMR upon variation of the salt conditions. Biochemistry 44:1444–1452Google Scholar
  83. Paravastu AK, Leapman RD, Yau W-M, Tycko R (2008) Molecular structural basis for polymorphism in Alzheimer’s beta-amyloid fibrils. Proc Natl Acad Sci USA 105:18349–18354ADSGoogle Scholar
  84. Park SH, Mrse AA, Nevzorov AA, De Angelis AA, Opella SJ (2006) Rotational diffusion of membrane proteins in aligned phospholipid bilayers by solid-state NMR spectroscopy. J Magn Reson 178:162–165ADSGoogle Scholar
  85. Park SH, Das BB, Casagrande F, Tian Y, Nothnagel HJ, Chu M, Kiefer H, Maier K, De Angelis AA, Marassi FM, Opella SJ (2012) Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491:779ADSGoogle Scholar
  86. Patzelt H, Ulrich AS, Egbringhoff H, Dux P, Ashurst J, Simon B, Oschkinat H, Oesterhelt D (1997) Towards structural investigations on isotope labelled native bacteriorhodopsin in detergent micelles by solution-state NMR spectroscopy. J Biomol NMR 10:95–106Google Scholar
  87. Petkova AT, Yau W-M, Tycko R (2006) Experimental constraints on quaternary structure in Alzheimer’s β-amyloid fibrils. Biochemistry 45:498–512Google Scholar
  88. Qiang W, Kelley K, Tycko R (2013) Polymorph-specific kinetics and thermodynamics of beta-amyloid fibril growth. J Am Chem Soc 135:6860–6871Google Scholar
  89. Quillin ML, Matthews BW (2000) Accurate calculation of the density of proteins. Acta Crystallogr Sect D: Biol Crystallogr 56:791–794Google Scholar
  90. Rasmussen SGF, Choi H-J, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC, Burghammer M, Ratnala VRP, Sanishvili R, Fischetti RF, Schertler GFX, Weis WI, Kobilka BK (2007) Crystal structure of the human ß2 adrenergic G-protein-coupled receptor. Nature 450:383–388ADSGoogle Scholar
  91. Ravera E, Parigi G, Mainz A, Religa TL, Reif B, Luchinat C (2013) Experimental determination of microsecond reorientation correlation times in protein solutions. J Phys Chem B 117:3548–3553Google Scholar
  92. Renault M, Pawsey S, Bos MP, Koers EJ, Nand D, Tommassen-van Boxtel R, Rosay M, Tommassen J, Maas WE, Baldus M (2011) Solid-state NMR spectroscopy on cellular preparations Enhanced by dynamic nuclear polarization. Angew Chem Int Ed Engl 51:2998–3001Google Scholar
  93. Rose A, Theune D, Goede A, Hildebrand PW (2013) MP:PD—a data base of internal packing densities, internal packing defects and internal waters of helical membrane proteins. Nucl Acids Res (in press)Google Scholar
  94. Rosenbaum DM, Cherezov V, Hanson MA, Rasmussen SGF, Thian FS, Kobilka TS, Choi H-J, Yao X-J, Weis WI, Stevens RC, Kobilka BK (2007) GPCR engineering yields high-resolution structural insights into ß2-adrenergic receptor function. Science 318:1266–1273ADSGoogle Scholar
  95. Saffman PG, Delbruck M (1975) Brownian motion in biological membranes. Proc Natl Acad Sci USA 72:3111–3113ADSGoogle Scholar
  96. Samoson A, Tuherm T, Gan Z (2001) High-field high-speed mas resolution enhancement in 1H NMR spectroscopy of solids. Solid State NMR 20:130–136Google Scholar
  97. Sapra KT, Besir S, Oesterhelt D, Muller DJ (2006) Characterizing molecular interactions in different bacteriorhodopsin assemblies by single-molecule force spectroscopy. J Mol Biol 355:640–650Google Scholar
  98. Sarkar CA, Dodevski I, Kenig M, Dudli S, Mohr A, Hermans E, Plückthun A (2008) Directed evolution of a G protein-coupled receptor for expression, stability, and binding selectivity. Proc Natl Acad Sci USA 105:14808–14813ADSGoogle Scholar
  99. Schanda P, Meier BH, Ernst M (2010) Quantitative analysis of protein backbone dynamics in microcrystalline ubiquitin by solid-state NMR spectroscopy. J Am Chem Soc 132:15957–15967Google Scholar
  100. Schanda P, Huber M, Boisbouvier J, Meier BH, Ernst M (2011) Solid-state NMR measurements of asymmetric dipolar couplings provide insight into protein side-chain motion. Angewandt Chem Int Edt 50:11005–11009Google Scholar
  101. Schlinkmann KM, Honegger A, Tureci E, Robison KE, Lipovsek D, Pluckthun A (2012) Critical features for biosynthesis, stability, and functionality of a G protein-coupled receptor uncovered by all-versus-all mutations. Proc Natl Acad Sci USA 109:9810–9815ADSGoogle Scholar
  102. Shahid SA, Bardiaux B, Franks WT, Krabben L, Habeck M, van Rossum B-J, Linke D (2012) Membrane-protein structure determination by solid-state NMR spectroscopy of microcrystals. Nat Methods 9:U1119–U1212Google Scholar
  103. Skrynnikov NR (2007) Asymmetric doublets in MAS NMR: coherent and incoherent mechanisms. Magn Res Chem 45:S161–S173Google Scholar
  104. Soscia SJ, Kirby JE, Washicosky KJ, Tucker SM, Ingelsson M, Hyman B, Burton MA, Goldstein LE, Duong S, Tanzi RE, Moir RD (2010) The Alzheimer’s disease-associated amyloid beta-protein is an antimicrobial peptide. PloS One 5:e9505ADSGoogle Scholar
  105. Stein WD (1990) Channels, carriers and pumps. An introduction to membrane transport. Academic Press, San DiegoGoogle Scholar
  106. Takahashi H, Ayala I, Bardet M, De Paepe G, Simorre J-P, Hediger S (2013) Solid-state NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization. J Am Chem Soc 135:5105–5110Google Scholar
  107. Tanzi RE, Moir RD, Wagner SL (2004) Clearance of Alzheimer’s A beta peptide: the many roads to perdition. Neuron 43:605–608Google Scholar
  108. Tollinger M, Sivertsen AC, Meier BH, Ernst M, Schanda P (2012) Site-resolved measurement of microsecond-to-millisecond conformational-exchange processes in proteins by solid-state NMR spectroscopy. J Am Chem Soc 134:14800–14807Google Scholar
  109. Tycko R (2006) Molecular structure of amyloid fibrils: insights from solid-state NMR. Quart Rev Biophys 39:1–55Google Scholar
  110. Ueno H, Suzuki T, Kinosita KJ, Yoshida M (2005) ATP-driven stepwise rotation of FoF1-ATP synthase. Proc Natl Acad Sci USA 102:1333–1338ADSGoogle Scholar
  111. Vanderhart DL, Earl WL, Garroway AN (1981) Resolution in C-13 NMR of organic-solids using high-power proton decoupling and magic-angle sample spinning. J Magn Reson 44:361–401ADSGoogle Scholar
  112. Wang S, Munro RA, Shi L, Kawamura I, Okitsu T, Wada A, Kim S-Y, Jung K-H, Brown LS, Ladizhansky V (2013a) Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nat Methods 10:1007Google Scholar
  113. Wang T, Park YB, Caporini MA, Rosay M, Zhong L, Cosgrove DJ, Hong M (2013b) Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc Natl Acad Sci USA 110:16444–16449ADSGoogle Scholar
  114. Ward ME, Shi L, Lake E, Krishnamurthy S, Hutchins H, Brown LS, Ladizhansky V (2011) Proton-detected solid-state NMR reveals intramembrane polar networks in a seven-helical transmembrane protein proteorhodopsin. J Am Chem Soc 133:17434–17443Google Scholar
  115. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319:1523–1526ADSGoogle Scholar
  116. Wiench JW, Lin VS-Y, Pruski M (2008) Si-29 NMR in solid state with CPMG acquisition under MAS. J Magn Reson 193:233–242ADSGoogle Scholar
  117. Williams JC, McDermott AE (1995) Dynamics of the flexible loop of triosephosphate isomerase—the loop motion is not ligand-gated. Biochemistry 34:8309–8319Google Scholar
  118. Yang J, Tasayco ML, Polenova T (2009) Dynamics of reassembled thioredoxin studied by magic angle spinning NMR: snapshots from Different Time Scales. J Am Chem Soc 131:13690–13702Google Scholar
  119. Zhou DH, Shah G, Cormos M, Mullen C, Sandoz D, Rienstra CM (2007a) Proton-detected solid-state NMR Spectroscopy of fully protonated proteins at 40 kHz magic-angle spinning. J Am Chem Soc 129:11791–11801Google Scholar
  120. Zhou DH, Shea JJ, Nieuwkoop AJ, Franks WT, Wylie BJ, Mullen C, Sandoz D, Rienstra CM (2007b) Solid-state protein-structure determination with proton-detected triple-resonance 3D magic-angle-spinning NMR spectroscopy. Angew Chemie Int Edt 46:8380–8383Google Scholar
  121. Zhou DH, Nieuwkoop AJ, Berthold DA, Comellas G, Sperling LJ, Tang M, Shah GJ, Brea EJ, Lemkau LR, Rienstra CM (2012) Solid-state NMR analysis of membrane proteins and protein aggregates by proton detected spectroscopy. J Biomol NMR 54:291–305Google Scholar
  122. Zinkevich T, Chevelkov V, Reif B, Saalwachter K, Krushelnitsky A (2013) Internal protein dynamics on ps to μs timescales as studied by multi-frequency 15 N solid-state NMR relaxation. J Biomol NMR 57:219–235Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Rasmus Linser
    • 1
  • Riddhiman Sarkar
    • 2
    • 3
  • Alexey Krushelnitzky
    • 4
  • Andi Mainz
    • 2
    • 3
  • Bernd Reif
    • 2
    • 3
    Email author
  1. 1.Department of Biological Chemistry and Molecular PharmacologyHarvard Medical SchoolBostonUSA
  2. 2.Department of Chemie, Munich Center for Integrated Protein Science (CIPSM)Technische Universität München (TUM)GarchingGermany
  3. 3.Deutsches Forschungszentrum für Gesundheit und Umwelt (HMGU)Helmholtz-Zentrum MünchenNeuherbergGermany
  4. 4.Institut für Physik – NMRMartin-Luther-Universität Halle-WittenbergHalle (Saale)Germany

Personalised recommendations