Sensitivity and resolution enhancement of oriented solid-state NMR: Application to membrane proteins

Progress in Nuclear Magnetic Resonance Spectroscopy

Volumn 75, Issue , 2013, Pages 50-68

  Gopinath, T ^a   Mote, Kaustubh R ^b   Veglia, Gianluigi ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b University of Minnesota   (United States)

Author keywords

Chemical shift anisotropy; Dipolar couplings; Oriented solid state NMR; Resolution enhancement; Sensitivity enhancement

Indexed keywords

ANISOTROPY; BIOLOGICAL MEMBRANES; CHEMICAL SHIFT; LIGHT POLARIZATION; LIPID BILAYERS; MAGIC ANGLE SPINNING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SPECTROMETERS;

CHEMICAL SHIFT ANISOTROPY; DIPOLAR COUPLINGS; RESOLUTION ENHANCEMENT; SENSITIVITY ENHANCEMENTS; SOLID STATE NMR;

PROTEINS;

MEMBRANE PROTEIN; PHOSPHOLAMBAN; SELENIUM;

4-PENTYL-4′-CYANOBIPHENYL; 5CB; ALGORITHM; ANIMAL; ARTICLE; BLEW; BURUM LINSER ERNST WINDOWLESS; CHEMICAL SHIFT ANISOTROPY; CHEMISTRY; CP; CROSS POLARIZATION; CRYSTALLIZATION; CSA; DC; DIPOLAR COUPLING; DIPOLAR COUPLINGS; DOUBLY TILTED ROTATING FRAME; DTRF; FREQUENCY-SWITCHED LEE-GOLDBERG; FSLG; HETCOR; HETERONUCLEAR CORRELATION; HETERONUCLEAR ISOTROPIC MIXING SEPARATED LOCAL FIELD; HIMSELF; HUMAN; LEE-GOLDBERG; LG; MAGIC ANGLE SPINNING; MAGIC SANDWICH HIGHER ORDER TRUNCATION; MALCOLM LEVITT DECOUPLING SEQUENCE; MAS; METHODOLOGY; MLEV; MSHOT; N-ACETYL-LEUCINE; N-ACETYL-VALINE-LEUCINE; NAL; NAVL; NUCLEAR MAGNETIC RESONANCE; O-SSNMR; ORIENTED SOLID-STATE NMR; PDSD; PELF; PI; PISEMA; PLN; POLARIZATION INVERSION; POLARIZATION INVERSION SPIN EXCHANGE AT THE MAGIC ANGLE; PROTON DRIVEN SPIN DIFFUSION; PROTON EVOLVED LOCAL FIELD; RESOLUTION ENHANCEMENT; RMS; ROOT MEAN SQUARE; SAMPI4; SARCOLIPIN; SELECTIVE AVERAGING MAGIC SANDWICH WITH POLARIZATION INVERSION; SENSITIVITY ENHANCEMENT; SIGNAL NOISE RATIO; SLN; SNR; WIM24; WINDOWLESS ISOTROPIC MIXING 24;

4-PENTYL-4′-CYANOBIPHENYL; 5CB; BLEW; BURUM LINSER ERNST WINDOWLESS; CHEMICAL SHIFT ANISOTROPY; CP; CROSS POLARIZATION; CSA; DC; DIPOLAR COUPLING; DIPOLAR COUPLINGS; DOUBLY TILTED ROTATING FRAME; DTRF; FREQUENCY-SWITCHED LEE-GOLDBERG; FSLG; HETCOR; HETERONUCLEAR CORRELATION; HETERONUCLEAR ISOTROPIC MIXING SEPARATED LOCAL FIELD; HIMSELF; LEE-GOLDBERG; LG; MAGIC ANGLE SPINNING; MAGIC SANDWICH HIGHER ORDER TRUNCATION; MALCOLM LEVITT DECOUPLING SEQUENCE; MAS; MLEV; MSHOT; N-ACETYL-LEUCINE; N-ACETYL-VALINE-LEUCINE; NAL; NAVL; O-SSNMR; ORIENTED SOLID-STATE NMR; PDSD; PELF; PHOSPHOLAMBAN; PI; PISEMA; PLN; POLARIZATION INVERSION; POLARIZATION INVERSION SPIN EXCHANGE AT THE MAGIC ANGLE; PROTON DRIVEN SPIN DIFFUSION; PROTON EVOLVED LOCAL FIELD; RESOLUTION ENHANCEMENT; RMS; ROOT MEAN SQUARE; SAMPI4; SARCOLIPIN; SE; SELECTIVE AVERAGING MAGIC SANDWICH WITH POLARIZATION INVERSION; SENSITIVITY ENHANCEMENT; SIGNAL TO NOISE RATIO; SLN; SNR; WIM24; WINDOWLESS ISOTROPIC MIXING 24;

ALGORITHMS; ANIMALS; CRYSTALLIZATION; HUMANS; MEMBRANE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR;

EID: 84887104891     PISSN: 00796565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnmrs.2013.07.004     Document Type: Review

References (101)

1. D.T. Murray, N. Das, and T.A. Cross Solid state NMR strategy for characterizing native membrane protein structures Acc. Chem. Res. 2013 10.1021/ar3003442
2. T.A. Cross, M. Sharma, M. Yi, and H.-X. Zhou Influence of solubilizing environments on membrane protein structures Trends Biochem. Sci. 36 2011 117 125
3. D.E. Warschawski, A.A. Arnold, M. Beaugrand, A. Gravel, É. Chartrand, and I. Marcotte Choosing membrane mimetics for NMR structural studies of transmembrane proteins Biochim. Biophys. Acta 1808 2011 1957 1974
4. R. Verardi, N.J. Traaseth, L.R. Masterson, V.V. Vostrikov, and G. Veglia Isotope labeling for solution and solid-state NMR spectroscopy of membrane proteins Adv. Exp. Med. Biol. 992 2012 35 62
5. R.R. Ketchem, W. Hu, and T.A. Cross High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR Science 261 1993 1457 1460 (Pubitemid 23334269)
6. M. Sharma, M. Yi, H. Dong, H. Qin, E. Peterson, and D.D. Busath Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer Science 330 2010 509 512
7. N.J. Traaseth, L. Shi, R. Verardi, D.G. Mullen, G. Barany, and G. Veglia Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach Proc. Natl. Acad. Sci. USA 106 2009 10165 10170
8. R. Verardi, L. Shi, N.J. Traaseth, N. Walsh, and G. Veglia Structural topology of phospholamban pentamer in lipid bilayers by a hybrid solution and solid-state NMR method Proc. Natl. Acad. Sci. USA 108 2011 9101 9106
9. K.G. Valentine, S.F. Liu, F.M. Marassi, G. Veglia, S.J. Opella, and F.X. Ding Structure and topology of a peptide segment of the 6th transmembrane domain of the Saccharomyces cerevisae alpha-factor receptor in phospholipid bilayers Biopolymers 59 2001 243 256 (Pubitemid 32821743)
10. B.A. Buck-Koehntop, A. Mascioni, J.J. Buffy, and G. Veglia Structure, dynamics, and membrane topology of stannin: a mediator of neuronal cell apoptosis induced by trimethyltin chloride J. Mol. Biol. 354 2005 652 665 (Pubitemid 41628283)
11. J.J. Buffy, N.J. Traaseth, A. Mascioni, P.L. Gor'kov, E.Y. Chekmenev, and W.W. Brey Two-dimensional solid-state NMR reveals two topologies of sarcolipin in oriented lipid bilayers Biochemistry 45 2006 10939 10946 (Pubitemid 44360163)
12. 1H solid-state NMR data for determination of transmembrane peptide orientation and dynamics Biophys. J. 101 2011 2939 2947
13. V.V. Vostrikov, A.E. Daily, D.V. Greathouse, and R.E. Koeppe Charged or aromatic anchor residue dependence of transmembrane peptide tilt J. Biol. Chem. 285 2010 31723 31730
14. V.V. Vostrikov, B.A. Hall, D.V. Greathouse, R.E. Koeppe 2nd, and M.S. Sansom Changes in transmembrane helix alignment by arginine residues revealed by solid-state NMR experiments and coarse-grained MD simulations J. Am. Chem. Soc. 132 2010 5803 5811
15. C. Aisenbrey, M. Michalek, E.S. Salnikov, and B. Bechinger Solid-state NMR approaches to study protein structure and protein-lipid interactions Methods Mol. Biol. 974 2013 357 387
16. 15N solid-state NMR spectroscopy investigation Biophys. J. 81 2001 2251 2256 (Pubitemid 32917173)
17. C. Li, P. Gao, H. Qin, R. Chase, P.L. Gor'kov, and W.W. Brey Uniformly aligned full-length membrane proteins in liquid crystalline bilayers for structural characterization J. Am. Chem. Soc. 129 2007 5304 5305 (Pubitemid 46697586)
18. 15N-labeled membrane protein in phospholipid bilayers Proc. Natl. Acad. Sci. USA 94 1997 8551 8556
19. S.J. Opella, C. Ma, and F.M. Marassi Nuclear magnetic resonance of membrane-associated peptides and proteins Methods Enzymol. 339 2001 285 313 (Pubitemid 32666566)
20. A. Naito Structure elucidation of membrane-associated peptides and proteins in oriented bilayers by solid-state NMR spectroscopy Solid State Nucl. Magn. Reson. 36 2009 67 76
21. S.J. Opella, and F.M. Marassi Structure determination of membrane proteins by NMR spectroscopy Chem. Rev. 104 2004 3587 3606
22. S. Ozdirekcan, C. Etchebest, J.A. Killian, and P.F.J. Fuchs On the orientation of a designed transmembrane peptide: toward the right tilt angle? J. Am. Chem. Soc. 129 2007 15174 15181 (Pubitemid 350247801)
23. I. Marcotte, and M. Auger Bicelles as model membranes for solid- and solution-state NMR studies of membrane peptides and proteins Concepts Magn. Reson. Part A 24A 2005 17 37
24. U.H.N. Dürr, M. Gildenberg, and A. Ramamoorthy The magic of bicelles lights up membrane protein structure Chem. Rev. 112 2012 6054 6074
25. A.A. De Angelis, and S.J. Opella Bicelle samples for solid-state NMR of membrane proteins Nat. Protocols 2 2007 2332 2338
26. A.A. Nevzorov, and S.J. Opella Selective averaging for high-resolution solid-state NMR spectroscopy of aligned samples J. Magn. Reson. 185 2007 59 70 (Pubitemid 46484391)
27. 15N solid-state NMR spectroscopy J. Am. Chem. Soc. 126 2004 16676 16683 (Pubitemid 40081970)
28. S.H. Park, F. Casagrande, B.B. Das, L. Albrecht, M. Chu, and S.J. Opella Local and global dynamics of the G protein-coupled receptor CXCR1 Biochemistry 50 2011 2371 2380
29. S.H. Park, and S.J. Opella Triton x-100 as the "short-chain lipid" improves the magnetic alignment and stability of membrane proteins in phosphatidylcholine bilayers for oriented-sample solid-state NMR spectroscopy J. Am. Chem. Soc. 132 2010 12552 12553
30. 2H solid-state NMR spectroscopy Biochemistry 43 2004 10502 10512 (Pubitemid 39079321)
31. M.F. Mesleh, G. Veglia, T.M. DeSilva, F.M. Marassi, and S.J. Opella Dipolar waves as NMR maps of protein structure J. Am. Chem. Soc. 124 2002 4206 4207 (Pubitemid 34441543)
32. T. Gopinath, and G. Veglia Sensitivity enhancement in static solid-state NMR experiments via single- and multiple-quantum dipolar coherences J. Am. Chem. Soc. 131 2009 5754 5756
33. T. Gopinath, N.J. Traaseth, K. Mote, and G. Veglia Sensitivity enhanced heteronuclear correlation spectroscopy in multidimensional solid-state NMR of oriented systems via chemical shift coherences J. Am. Chem. Soc. 132 2010 5357 5363
34. T. Gopinath, R. Verardi, N.J. Traaseth, and G. Veglia Sensitivity enhancement of separated local field experiments: application to membrane proteins J. Phys. Chem. B 114 2010 5089 5095
35. T. Gopinath, K.R. Mote, and G. Veglia Proton evolved local field solid-state nuclear magnetic resonance using Hadamard encoding: theory and application to membrane proteins J. Chem. Phys. 135 2011 074503
36. T. Gopinath, and G. Veglia Improved resolution in dipolar NMR spectra using constant time evolution PISEMA experiment Chem. Phys. Lett. 494 2010 104 110
37. L. Müller, A. Kumar, T. Baumann, and R. Ernst Transient oscillations in NMR cross-polarization experiments in solids Phys. Rev. Lett. 32 1974 1402 1406
38. N. Sinha, and K. Ramanathan Use of polarization inversion for resolution of small dipolar couplings in SLF-2D NMR experiments - an application to liquid crystals Chem. Phys. Lett. 332 2000 125 130
39. H. Kim, T.A. Cross, and R. Fu Cross-polarization schemes for peptide samples oriented in hydrated phospholipid bilayers J. Magn. Reson. 168 2004 147 152
40. J.S. Waugh Uncoupling of local field spectra in nuclear magnetic resonance: determination of atomic positions in solids Proc. Natl. Acad. Sci. USA 73 1976 1394 1397
41. C.H. Wu, A. Ramamoorthy, and S.J. Opella High-resolution heteronuclear dipolar solid-state NMR spectroscopy J. Magn. Reson. A 109 1994 270 272
42. M. Lee, and W. Goldburg Nuclear-magnetic-resonance line narrowing by a rotating rf field Phys. Rev. 140 1965 A1261 A1271
43. M.H. Levitt, D. Suter, and R.R. Ernst Spin dynamics and thermodynamics in solid-state NMR cross polarization J. Chem. Phys. 84 1986 4243
44. F.M. Marassi, and S.J. Opella NMR structural studies of membrane proteins Curr. Opin. Struct. Biol. 8 1998 640 648 (Pubitemid 28486393)
45. K. Yamamoto, S.V. Dvinskikh, and A. Ramamoorthy Measurement of heteronuclear dipolar couplings using a rotating frame solid-state NMR experiment Chem. Phys. Lett. 419 2006 533 536
46. K. Yamamoto, D.K. Lee, and A. Ramamoorthy Broadband-PISEMA solid-state NMR spectroscopy Chem. Phys. Lett. 407 2005 289 293 (Pubitemid 40626589)
47. S. Jayanthi, and K.V. Ramanathan 2(n)-SEMA-a robust solid state nuclear magnetic resonance experiment for measuring heteronuclear dipolar couplings in static oriented systems using effective transverse spin-lock J. Chem. Phys. 132 2010 134501
48. D.K. Lee, T. Narasimhaswamy, and A. Ramamoorthy PITANSEMA, a low-power PISEMA solid-state NMR experiment Chem. Phys. Lett. 399 2004 359 362 (Pubitemid 40017537)
49. S.V. Dvinskikh, and D. Sandstrom Frequency offset refocused PISEMA-type sequences J. Magn. Reson. 175 2005 163 169 (Pubitemid 40753516)
50. A. Ramamoorthy, Y. Wei, and D.K. Lee PISEMA solid state NMR spectroscopy Advances in Solid State NMR Studies of Materials and Polymers 2004 Elsevier Acad. Pr pp. 1-52
51. M. Hohwy, and N.C. Nielsen Elimination of high order terms in multiple pulse nuclear magnetic resonance spectroscopy: application to homonuclear decoupling in solids J. Chem. Phys. 106 1997 7571
52. P. Caravatti, L. Braunschweiler, and R.R. Ernst Heteronuclear correlation spectroscopy in rotating solids Chem. Phys. Lett. 100 1983 305 310
53. J. Cavanagh, A.G. Palmer, P.E. Wright, and M. Rance Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy J. Magn. Reson. 91 1991 151 170
54. L. Kay, P. Keifer, and T. Saarinen Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J. Am. Chem. Soc. 114 1992 10663 10665
55. 15N labeled integral membrane proteins in magnetically aligned lipid bilayers J. Biomol. NMR 51 2011 339 346
56. N.J. Traaseth, T. Gopinath, and G. Veglia On the performance of spin diffusion NMR techniques in oriented solids: prospects for resonance assignments and distance measurements from separated local field experiments J. Phys. Chem. B 114 2010 13872 13880
57. R.S. Prosser, V.B. Volkov, and I.V. Shiyanovskaya Solid-state NMR studies of magnetically aligned phospholipid membranes: taming lanthanides for membrane protein studies Biochem. Cell Biol. 76 1998 443 451 (Pubitemid 29102029)
58. R.S. Prosser, V.B. Volkov, and I.V. Shiyanovskaya Novel chelate-induced magnetic alignment of biological membranes Biophys. J. 75 1998 2163 2169 (Pubitemid 28492098)
59. G. Veglia, and S.J. Opella Lanthanide ion binding to adventitious sites aligns membrane proteins in micelles for solution NMR spectroscopy J. Am. Chem. Soc. 122 2000 11733 11734
60. C. Loudet, S. Manet, S. Gineste, R. Oda, M.F. Achard, and E.J. Dufourc Biphenyl bicelle disks align perpendicular to magnetic fields on large temperature scales: a study combining synthesis, solid-state NMR, TEM, and SAXS Biophys. J. 92 2007 3949 3959 (Pubitemid 46910581)
61. S.H. Park, C. Loudet, F.M. Marassi, E.J. Dufourc, and S.J. Opella Solid-state NMR spectroscopy of a membrane protein in biphenyl phospholipid bicelles with the bilayer normal parallel to the magnetic field J. Magn. Reson. 193 2008 133 138
62. R.C. Page, and T.A. Cross Transmembrane helix uniformity examined by spectral mapping of torsion angles Structure 16 2008 787 797 (Pubitemid 351626899)
63. S. Kim, and T.A. Cross Uniformity, ideality, and hydrogen bonds in transmembrane alpha-helices Biophys. J. 83 2002 2084 2095
64. A. Mascioni, B.L. Eggimann, and G. Veglia Determination of helical membrane protein topology using residual dipolar couplings and exhaustive search algorithm: application to phospholamban Chem. Phys. Lipids 132 2004 133 144 (Pubitemid 39461993)
65. G. Metz, X.L. Wu, and S.O. Smith Ramped-amplitude cross-polarization in magic-angle-spinning NMR J. Magn. Reson. A 110 1994 219 227
66. O.B. Peersen, X.L. Wu, I. Kustanovich, and S.O. Smith Variable-amplitude cross-polarization MAS NMR J. Magn. Reson. A 104 1993 334 339
67. T. Nakai, and T. Terao Measurements of heteronuclear dipolar powder patterns due only to directly bonded couplings Magn. Reson. Chem. 30 1992 42 44
68. M. Hong, K. Schmidt-Rohr, and D. Nanz Study of phospholipid structure by H-1, C-13, P-31 dipolar couplings from two-dimensional NMR Biophys. J. 69 1995 1939 1950
69. K. Schmidt-Rohr, D. Nanz, L. Emsley, and A. Pines NMR measurement of resolved heteronuclear dipole couplings in liquid crystals and lipids J. Phys. Chem. 98 1994 6668 6670
70. S. Dvinskikh, U.H. Durr, K. Yamamoto, and A. Ramamoorthy A high-resolution solid-state NMR approach for the structural studies of bicelles J. Am. Chem. Soc. 128 2006 6326 6327 (Pubitemid 43727264)
71. J.W. Emsley, P. Lesot, G. De Luca, A. Lesage, D. Merlet, and G. Pileio A comparison of proton-detected 13C local field experiments with deuterium NMR at natural abundance for studying liquid crystals Liq. Cryst. 35 2008 443 464
72. S. Jayanthi, P.K. Madhu, N.D. Kurur, and K.V. Ramanathan Heteronuclear polarization transfer in static oriented systems using a windowless multiple-pulse sequence Chem. Phys. Lett. 439 2007 407 411 (Pubitemid 46635409)
73. S.V. Dvinskikh, K. Yamamoto, U.H. Durr, and A. Ramamoorthy Sensitivity and resolution enhancement in solid-state NMR spectroscopy of bicelles J. Magn. Reson. 184 2007 228 235 (Pubitemid 46177668)
74. R. Soong, P.E. Smith, J. Xu, K. Yamamoto, S.C. Im, and L. Waskell Proton-evolved local-field solid-state NMR studies of cytochrome b5 embedded in bicelles, revealing both structural and dynamical information J. Am. Chem. Soc. 132 2010 5779 5788
75. J.S. Waugh, M. Huber, and U. Haeberlen Approach to high resolution NMR in solids Phys. Rev. Lett. 20 1968 180 183
76. U. Haeberlen, and J.S. Waugh Coherent averaging effects in magnetic resonance Phys. Rev. 175 1968 453 467
77. P. Mansfield Symmetrized pulse sequences in high resolution NMR in solids J. Phys. C: Solid State Phys. 4 1971 1444 1452
78. W.K. Rhim, D.D. Elleman, and R.W. Vaughan Analysis of multiple pulse NMR in solids J. Chem. Phys. 59 1973 3740 3749
79. D.P. Burum, and W.K. Rhim Analysis of multiple pulse NMR in solids J. Chem. Phys. 71 1979 944
80. E. Vinogradov, P.K. Madhu, and S. Vega Phase modulated Lee-Goldburg magic angle spinning proton nuclear magnetic resonance experiments in the solid state: a bimodal Floquet theoretical treatment J. Chem. Phys. 115 2001 8983
81. D.P. Burum, M. Linder, and R.R. Ernst Low-power multipulse line narrowing in solid-state J. Magn. Reson. 44 1981 173 188
82. G.J. Lu, S.H. Park, and S.J. Opella Improved 1H amide resonance line narrowing in oriented sample solid-state NMR of membrane proteins in phospholipid bilayers J. Magn. Reson. 220 2012 54 61
83. R. Fu, E.D. Gordon, D.J. Hibbard, and M. Cotten High resolution heteronuclear correlation NMR spectroscopy of an antimicrobial peptide in aligned lipid bilayers: peptide-water interactions at the water-bilayer interface J. Am. Chem. Soc. 131 2009 10830 10831
84. A.A. Nevzorov Orientational and motional narrowing of solid-state NMR lineshapes of uniaxially aligned membrane proteins J. Phys. Chem. B 115 2011 15406 15414
85. A.A. Maudsley, and R.R. Ernst Indirect detection of magnetic resonance by heteronuclear two-dimensional spectroscopy Chem. Phys. Lett. 50 1977 368 372
86. G.J. Lu, W.S. Son, and S.J. Opella A general assignment method for oriented sample (OS) solid-state NMR of proteins based on the correlation of resonances through heteronuclear dipolar couplings in samples aligned parallel and perpendicular to the magnetic field J. Magn. Reson. 209 2011 195 206
87. D.J. States, R.A. Haberkorn, and D.J. Ruben A two-dimensional nuclear overhauser experiment with pure absorption phase in 4 quadrants J. Magn. Reson. 48 1982 286 292
88. K.R. Mote, T. Gopinath, G. Veglia, Determination of structural topology of a membrane protein in lipid-bilayers using polarization optimized experiments (POE) for static and MAS solid state NMR spectroscopy, J. Biomol. NMR (2013), http://dx.doi.org/10.1007/s10858-013-9766-2.
89. T. Asbury, J.R. Quine, S. Achuthan, J. Hu, M.S. Chapman, and T.A. Cross PIPATH: an optimized algorithm for generating alpha-helical structures from PISEMA data J. Magn. Reson. 183 2006 87 95 (Pubitemid 44692524)
90. F.M. Marassi, and S.J. Opella Simultaneous assignment and structure determination of a membrane protein from NMR orientational restraints Protein Sci. 12 2003 403 411 (Pubitemid 36241100)
91. L. Shi, N.J. Traaseth, R. Verardi, A. Cembran, J. Gao, and G. Veglia A refinement protocol to determine structure, topology, and depth of insertion of membrane proteins using hybrid solution and solid-state NMR restraints J. Biomol. NMR 44 2009 195 205
92. F.M. Marassi, J.J. Gesell, A.P. Valente, Y. Kim, M. Oblatt-Montal, and M. Montal Dilute spin-exchange assignment of solid-state NMR spectra of oriented proteins: acetylcholine M2 in bilayers J. Biomol. NMR 14 1999 141 148 (Pubitemid 29322968)
93. K. Takegoshi, S. Nakamura, and T. Terao Dipolar-assisted rotational resonance in magic-angle spinning NMR Chem. Phys. Lett. 344 2001 631 637 (Pubitemid 33628408)
94. S. Caldarelli, M. Hong, L. Emsley, and A. Pines Measurement of carbon-proton dipolar couplings in liquid crystals by local dipolar field NMR spectroscopy J. Phys. Chem. 100 1996 18696 18701 (Pubitemid 126834476)
95. D. Suter, and R. Ernst Spin diffusion in resolved solid-state NMR spectra Phys. Rev. B: Condens. Matter Mater. Phys. 32 1985 5608 5627
96. J. Xu, J. Struppe, and A. Ramamoorthy Two-dimensional homonuclear chemical shift correlation established by the cross-relaxation driven spin diffusion in solids J. Chem. Phys. 128 2008 52308
97. A.A. Nevzorov Mismatched Hartmann-Hahn conditions cause proton-mediated intermolecular magnetization transfer between dilute low-spin nuclei in NMR of static solids J. Am. Chem. Soc. 130 2008 11282 11283
98. R.W. Knox, G.J. Lu, S.J. Opella, and A.A. Nevzorov A resonance assignment method for oriented-sample solid-state NMR of proteins J. Am. Chem. Soc. 132 2010 8255 8257
99. W. Tang, R.W. Knox, and A.A. Nevzorov A spectroscopic assignment technique for membrane proteins reconstituted in magnetically aligned bicelles J. Biomol. NMR 54 2012 307 316
100. A.K. Khitrin, J. Xu, and A. Ramamoorthy Cross-correlations between low-gamma nuclei in solids via a common dipolar bath J. Magn. Reson. 212 2011 95 101
101. 13C spin diffusion of adamantane J. Chem. Phys. 79 1983 3694