Four-dimensional heteronuclear correlation experiments for chemical shift assignment of solid proteins

Aggarwal K, Delsuc M (1997) Triangular sampling of multidimensional NMR data sets. Magn Reson Chem 35:593–596 Baldus M, Geurts DG, Hediger S, Meier BH (1996) Efficient 15N-13C polarization transfer by adiabatic-passage Hartmann-Hahn cross polarization. J Magn Reson A 118:140–144 Baldus M, Petkova AT, Herzfeld JH, Griffin RG (1998) Cross polarization in the tilted frame: Assignment and spectral simplification in heteronuclear spin systems. Mol Phys 95:1197–1207 Barkhuijsen H, Debeer R, Vanormondt D (1987) Improved algorithm for noniterative time-domain model-fitting to exponentially damped magnetic-resonance signals. J Magn Reson 73:553–557 Bennett AE, Ok JH, Griffin RG, Vega S (1992) Chemical shift correlation spectroscopy in rotating solids: Radio-frequency dipolar recoupling and longitudinal exchange. J Chem Phys 96:8624–8627 Bennett AE, Rienstra CM, Auger M, Lakshmi KV, Griffin RG (1995) Heteronuclear decoupling in rotating solids. J Chem Phys 103:6951–6958 Bennett AE, Rienstra CM, Griffiths JM, Zhen W, Lansbury PT Jr, Griffin RG (1998) Homonuclear radio frequency-driven recoupling in rotating solids. J Chem Phys 108:9463–9479 Bloembergen N (1949) On the interaction of nuclear spins in a crystalline lattice. Physica 15:386 Bockmann A, Lange A, Galinier A, Luca S, Giraud N, Juy M, Heise H, Montserret R, Penin F, Baldus M (2003) Solid state NMR sequential resonance assignments and conformational analysis of the 2 × 10.4 kDa dimeric form of the bacillus subtilis protein crh. J Biomol NMR 27:323–339 Carravetta M, Eden M, Zhao X, Brinkmann A, Levitt MH (2000) Symmetry principles for the design of radiofrequency pulse sequences in the nuclear magnetic resonance of rotating solids. Chem Phys Lett 321:205–215 Carravetta M, Zhao X, Johannessen OG, Lai WC, Verhoeven MA, Bovee-Geurts PHM, Verdegem PJE, Kiihne S, Luthman H, De Groot HJM, DeGrip WJ, Lugtenburg J, Levitt MH (2004) Protein-induced bonding perturbation of the rhodopsin chromophore detected by double-quantum solid-state NMR. J Am Chem Soc 126:3948–3953 Castellani F, van Rossum B, Diehl A, Schubert M, Rehbein K, Oschkinat H (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 420:98–102 Castellani F, van Rossum BJ, Diehl A, Rehbein K, Oschkinat H (2003) Determination of solid-state NMR structures of proteins by means of three-dimensional 15N-13C-13C dipolar correlation spectroscopy and chemical shift analysis. Biochemistry 42:11476–11483 Cole HBR, Torchia DA (1991) An NMR-study of the backbone dynamics of staphylococcal nuclease in the crystalline state. Chem Phys 158:271–281 Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13:289–302 Costa PR, Sun BQ, Griffin RG (1997) Rotational resonance tickling: Accurate internuclear distance measurements in solids. J Am Chem Soc 119:10821–10830 Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRpipe - a multidimensional spectral processing system based on unix pipes. J Biomol NMR 6:277–293 Detken A, Hardy EH, Ernst M, Kainosho M, Kawakami T, Aimoto S, Meier BH (2001) Methods for sequential resonance assignment in solid, uniformly C-13, N-15 labelled peptides: Quantification and application to antamanide. J Biomol NMR 20:203–221 Etzkorn M, Martell S, Andronesi OC, Seidel K, Engelhard M, Baldus M (2007) Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angew Chem Int Ed 46:459–462 Flynn PF, Milton MJ, Babu CR, Wand AJ (2002) A simple and effective NMR cell for studies of encapsulated proteins dissolved in low viscosity solvents. J Biomol NMR 23:311–316 Franks WT, Wylie BJ, Stellfox SA, Rienstra CM (2006) Backbone conformational constraints in a microcrystalline U-15N-labeled protein by 3D dipolar-shift solid-state NMR spectroscopy. J Am Chem Soc 128:9992–9993 Franks WT, Zhou DH, Wylie BJ, Money BG, Graesser DT, Frericks HL, Sahota G, Rienstra CM (2005) Magic-angle spinning solid-state NMR spectroscopy of the beta 1 immunoglobulin binding domain of protein G (GB1): N-15 and C-13 chemical shift assignments and conformational analysis. J Am Chem Soc 127:12291–12305 Frericks HL, Zhou DH, Yap L, Gennis RB, Rienstra CM (2006) Magic-angle spinning solid-state NMR of a 144 kda membrane protein complex: E. coli cytochrome bo3 oxidase. J Biomol NMR 36:55–71 Fung BM, Khitrin AK, Ermolaev K (2000) An improved broadband decoupling sequence for liquid crystals and solids. J Magn Reson 142:97–101 Gardner KH, Zhang XC, Gehring K, Kay LE (1998) Solution NMR studies of a 42 kda escherichia coli maltose binding protein beta-cyclodextrin complex: Chemical shift assignments and analysis. J Am Chem Soc 120:11738–11748 Goddard TD, Kneller DG (2006) Sparky 2.116. University of California, San Francisco Havlin RH, Tycko R (2005) Probing site-specific conformational distributions in protein folding with solid-state NMR. Proc Natl Acad Sci USA 102:3284–3289 Hediger S, Meier BH, Ernst RR (1995) Adiabatic passage Hartmann-Hahn cross-polarization in NMR under magic-angle sample-spinning. Chem Phys Lett 240:449–456 Heise H, Hoyer W, Becker S, Andronesi OC, Riedel D, Baldus M (2005) Molecular-level secondary structure, polymorphism, and dynamics of full-length alpha-synuclein fibrils studied by solid-state NMR. Proc Natl Acad Sci USA 102:15871–15876 Hiller M, Krabben L, Vinothkumar KR, Castellani F, Van Rossum B-J, Kühlbrandt W, Oschkinat H (2005) Solid-state magic-angle spinning NMR of outer-membrane protein g from Escherichia coli. ChemBioChem 6:1679–1684 Hing A, Vega S, Schaefer J (1992) Transferred-echo double-resonance NMR. J Magn Reson 96:205–209 Hoch JC, Stern AS (2001) Maximum entropy reconstruction, spectrum analysis and deconvolution in multidimensional nuclear magnetic resonance, Meth Enzym 338:159–178 Hohwy M, Jakobsen HJ, Edén M, Levitt MH, Nielsen NC (1998) Broadband dipolar recoupling in the nuclear magnetic resonance of rotating solids: A compensated C7 pulse sequence. J Chem Phys 108:2686–94 Hohwy M, Rienstra CM, Jaroniec CP, Griffin RG (1999) Fivefold symmetric homonuclear dipolar recoupling in rotating solids: Application to double quantum spectroscopy, J Chem Phys 110:7983–7992 Hong M (1999) Resonance assignment of C-13/N-15 labeled solid proteins by two- and three-dimensional magic-angle-spinning NMR. J Biomol NMR 15:1–14 Hu JG, Sun BQ, Griffin RG, Herzfeld J (1995) Solid state NMR detection of multiple m-intermediates in bacteriorhodopsin. Biophys J 68:A332 Igumenova TI, McDermott AE (2005) Homo-nuclear C-13 J-decoupling in uniformly C-13-enriched solid proteins. J Magn Reson 175:11–20 Igumenova TI, McDermott AE, Zilm KW, Martin RW, Paulson EK, Wand AJ (2004a) Assignments of carbon NMR resonances for microcrystalline ubiquitin. J Am Chem Soc 126:6720–6727 Igumenova TI, Wand AJ, McDermott AE (2004b) Assignment of the backbone resonances for microcrystalline ubiquitin. J Am Chem Soc 126:5323–5331 Ishii Y (2001) 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 Ishii Y, Ashida J, Terao T (1995) 13C-1H dipolar recoupling dynamics in 13C multiple-pulse solid-state NMR. Chem Phys Lett 246:439–445 Jovanovic T, Farid R, Friesner RA, McDermott AE (2005) Thermal equilibrium of high- and low-spin forms of cytochrome p450 bm-3: Repositioning of the substrate? J Am Chem Soc 127:13548–13552 Kim S, Szyperski T (2003) GFT NMR, a new approach to rapidly obtain precise high-dimensional NMR spectral information. J Am Chem Soc 125:1385–1393 Kloepper KD, Woods WS, Winter KA, George JM, Rienstra CM (2006) Preparation of alpha-synuclein fbrils for solid-state NMR: Expression, purification and incubation of wild type and mutant forms. Protein Expr Purif 48:112–117 Kumar A, Ernst RR, Wüthrich K (1980) A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem Biophys Res Commun 95:1–6 Kupce E, Freeman R (2004) Projection-reconstruction technique for speeding up multidimensional NMR spectroscopy. J Am Chem Soc 126:6429–6440 Lange A, Becker S, Seidel K, Giller K, Pongs O, Baldus M (2005) A concept for rapid protein-structure determination by solid-state NMR spectroscopy. Angew Chem Int Ed 44:2089–2092 Lange A, Giller K, Hornig S, Martin-Eauclaire M-F, Pongs O, Becker S, Baldus M (2006) Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440:959–962 Lee YK, Kurur ND, Helmle M, Johannessen OG, Nielsen NC, Levitt MH (1995) Efficient dipolar recoupling in the NMR of rotating solids - a sevenfold symmetrical radiofrequency pulse sequence. Chem Phys Lett 242:304–309 Li Y, Berthold DA, Frericks HL, Gennis RB, Rienstra CM (2007) Partial 13C and 15N chemical shift assignments of the disulfide bond forming enzyme DsbB by 3D magic-angle spinning NMR spectroscopy. ChemBioChem 8:434–442 Li Y, Wylie BJ, Rienstra CM (2006) Selective refocusing pulses in magic-angle spinning NMR: Characterization and applications to multidimensional protein spectroscopy. J Magn Reson 179:206–216 Marion D, Wüthrich K (1983) Application of phase sensitive two-dimensional correlated spectroscopy (cosy) for measurements of H-1-H-1 spin-spin coupling-constants in proteins. Biochem Biophys Res Commun 113:967–974 Markley JL, Bax A, Arata Y, Hilbers CW, Kaptein R, Sykes BD, Wright PE, Wüthrich K (1998) Recommendations for the presentation of NMR structures of proteins and nucleic acids – (IUPAC Recommendations 1998). Pure Appl Chem 70:117–142 Martin RW, Paulson EK, Zilm KW (2003) Design of a triple resonance magic angle sample spinning probe for high field solid state nuclear magnetic resonance. Rev Sci Instrum 74:3045–3061 Martin RW, Zilm KW (2003) Preparation of protein nanocrystals and their characterization by solid state NMR. J Magn Reson 165:162–174 Marulanda D, Tasayco ML, Cataldi M, Arriaran V, Polenova T (2005) Resonance assignments and secondary structure analysis of e. Coli thioredoxin by magic angle spinning solid-state NMR spectroscopy. J Phys Chem B 109:18135–18145 Marulanda D, Tasayco ML, McDermott A, Cataldi M, Arriaran V, Polenova T (2004) Magic angle spinning solid-state NMR spectroscopy for structural studies of protein interfaces. Resonance assignments of differentially enriched escherichia coli thioredoxin reassembled by fragment complementation. J Am Chem Soc 126:16608–16620 McDermott A, Polenova T, Bockmann A, Zilm KW, Paulsen EK, Martin RW, Montelione GT (2000) Partial NMR assignments for uniformly (C-13, N-15)-enriched BPTI in the solid state. J Biomol NMR 16:209–219 McDowell LM, Klug CA, Beusen DD, Schaefer J (1996a) Ligand geometry of the ternary complex of 5-enolpyruvylshikimate-3-phosphate synthase from rotational-echo double-resonance NMR. Biochemistry 35:5395–5403 McDowell LM, Lee MS, McKay RA, Anderson KS, Schaefer J (1996b) Intersubunit communication in tryptophan synthase by carbon-13 and flourine-19 REDOR NMR. Biochemistry 35:3328–3334 McDowell LM, Poliks B, Studelska DR, O’Connor RD, Beusen DD, Schaefer J (2004) Rotational-echo double-resonance NMR-restrained model of the ternary complex of 5-enolpyruvylshikimate-3-phosphate synthase. J Biomol NMR 28:11–29 Morcombe CR, Gaponenko V, Byrd RA, Zilm KW (2004) Diluting abundant spins by isotope edited radio frequency field assisted diffusion. J Am Chem Soc 126:7196–7197 Morcombe CR, Zilm KW (2003) Chemical shift referencing in mas solid state NMR. J Magn Reson 162:479–486 Pauli J, Baldus M, van Rossum B, de Groot H, Oschkinat H (2001) Backbone and side-chain 13C and 15N resonance assignments of the alpha-spectrin SH3 domain by magic angle spinning solid state NMR at 17.6 tesla. ChemBioChem 2:272–281 Pauli J, van Rossum B, Forster H, de Groot HJM, Oschkinat H (2000) Sample optimization and identification of signal patterns of amino acid side chains in 2D RFDR spectra of the alpha-spectrin SH3 domain. J Magn Reson 143:411–416 Paulson EK, Martin RW, Zilm KW (2004) Cross polarization, radio frequency field homogeneity, and circuit balancing in high field solid state NMR probes. J Magn Reson 171:314–323 Petkova AT, Leapman RD, Guo ZH, Yau WM, Mattson MP, Tycko R (2005) Self-propagating, molecular-level polymorphism in Alzheimer’s beta-amyloid fibrils. Science 307:262–265 Petkova AT, Leapman RD, Yau WM, Tycko R (2004) Structural investigations of alzheimer’s beta-amyloid fibrils by solid state NMR. Biophys J 86:506A-506A Pintacuda G, Giraud N, Pierattelli R, Böckmann A, Bertini I, Emsley L (2006) Solid-state NMR spectroscopy of a paramagnetic protein: assignment and study of human dimeric oxidized Cu(II)-Zn(II) superoxide dismutase (SOD). Angew Chem Int Ed 46:1079–1082 Raleigh DP, Levitt MH, Griffin RG (1988) Rotational resonance in solid state NMR. Chem Phys Lett 146:71–76 Ravindranathan KP, Gallicchio E, McDermott AE, Levy RM (2007) Conformational dynamics of substrate in the active site of cytochrome p450 bm-3/npg complex: Insights from NMR order parameters. J Am Chem Soc 129:474–475 Rienstra CM, Hohwy M, Hong M, Griffin RG (2000) 2D and 3D N-15-C-13-C-13 NMR chemical shift correlation spectroscopy of solids: Assignment of mas spectra of peptides. J Am Chem Soc 122:10979–10990 Ritter C, Maddelein M-L, Siemer AB, Luhrs T, Ernst M, Meier BH, Saupe SJ, Riek R (2005) Correlation of structural elements and infectivity of the HET-s prion. Nature 435:844–848 Schaefer J, Stejskal EO (1979) Double cross polarization NMR of solids. J Magn Reson 34:443–447 Seidel K, Lange A, Becker S, Hughes CE, Heise H, Baldus M (2004) Protein solid-state NMR resonance assignments from (C-13, C-13) correlation spectroscopy. Phys Chem Chem Phys 6:5090–5093 Siemar AB, Ritter C, Ernst M, Riek R, Meier BH (2005) High-resolution solid-state NMR spectroscopy of the prion protein HET-s in its amyloid conformation. Angew Chem Int Ed 44:2441–2444 Siemer AB, Ritter C, Steinmetz MO, Ernst M, Riek R, Meier BH (2006) 13C, 15N resonance assignment of the het-s prion protein in its amyloid form. J Biomol NMR 34:75–87 Sonnenberg L, Luca S, Baldus M (2004) Multiple-spin analysis of chemical-shift-selective (C-13, C-13) transfer in uniformly labeled biomolecules. J Magn Reson 166:100–110 Stringer JA, Bronnimann CE, Mullen CG, Zhou DHH, Stellfox SA, Li Y, Williams EH, Rienstra CM (2005) Reduction of rf-induced sample heating with a scroll coil resonator structure for solid-state NMR probes. J Magn Reson 173:40–48 Stueber D, Mehta AK, Chen ZY, Wooley KL, Schaefer J (2006) Local order in polycarbonate glasses by C-13{F-19} rotational-echo double-resonance NMR. J Polym Sci Part B: Polym Phys 44:2760–2775 Suter D, Ernst RR (1985) Spin diffusion in resolved solid state NMR spectra. Phys Rev B 32:5608–5627 Szyperski T, Yeh D, Sukumaran D, Moseley H, Montelione G (2002) Reduced-dimensionality NMR spectroscopy for high-throughput protein resonance assignment. Proc Natl Acad Sci USA 99:8009–8014 Takegoshi K, Nakamura S, Terao T (2003) C-13-H-1 dipolar-driven C-13-C-13 recoupling without C-13 rf irradiation in nuclear magnetic resonance of rotating solids. J Chem Phys 118:2325–2341 Takegoshi K, Nomura K, Terao T (1995) Rotational resonance in the tilted rotating frame. Chem Phys Lett 232:424–428 Tugarinov V, Muhandiram R, Ayed A, Kay L (2002) Four-dimensional NMR spectroscopy of a 723-residue protein: Chemical shift assignments and secondary structure of malate synthase g. J Am Chem Soc 124:10025–10035 Tycko R (1996) Prospects for resonance assignments in multidimensional solid-state NMR spectra of uniformly labeled proteins. J Biomol NMR 8:239–251 Tycko R (2004) Progress towards a molecular-level structural understanding of amyloid fibrils. Curr Opin Struct Biol 14:96–103 Van Geet AL (1968) Calibration of the methanol and glycol nuclear magnetic resonance thermometers with a static thermistor probe. Anal Chem 40:2227–2229 Wylie BJ, Franks WT, Rienstra CM (2006) Determinations of 15N chemical shift anisotropy magnitudes in a uniformly 15N,13C-labeled microcrystalline proteins by three-dimensional magic-angle spinning NMR spectroscopy. J Phys Chem B 110:10926–10936 Zech SG, Wand AJ, McDermott AE (2005) Protein structure determination by high-resolution solid-state NMR spectroscopy: application to microcrystalline ubiquitin. J Am Chem Soc 127:8618–8626