Solid-state nuclear magnetic resonance investigation of protein and polypeptide structure

Annual Review of Biophysics and Biomolecular Structure

Volumn 28, Issue , 1999, Pages 235-268

  Fu, Riqiang ^a   Cross, Timothy A ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Distance constraints; Magic angle spinning; Orientational constraints; Oriented samples; Torsional constraints

Indexed keywords

ARTICLE; ISOTOPE LABELING; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SOLID STATE; STRUCTURE ANALYSIS;

ANISOTROPY; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PROTEIN CONFORMATION; PROTEINS;

EID: 0032986388     PISSN: 10568700     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.biophys.28.1.235     Document Type: Article

References (114)

1. 13C-enriched chlorosomes and isolated bacteriochlorophyll c aggregates of Chlorobium tepidum: the self-organization of pigments is the main structural feature of Chlorosomes. Biochemistry 34:15259-66
2. 2. Bennett AE, Ok JH, Griffin RG. 1992. Chemical shift correlation spectroscopy in rotating solids: radio frequency-driven dipolar recoupling and longitudinal exchange. J. Chem. Phys. 96:8624-27
3. 3. Blumich B, Hegemeyer A, Schaefer D, Schmidt-Rohr K, Spiess HW. 1990. Solid state NMR spectroscopy in polymer science. Adv. Mat. 2:72-81
4. 4. Brenneman MT, Cross TA. 1990. A method for the analytic determination of polypeptide structure using solid state nuclear magnetic resonance: the "metric method". J. Chem. Phys. 92:1483-94
5. 4a. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. 1983. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comp. Chem. 4: 187-217
6. 5. Busath DD, Thulin CD, Hendershot RW, Phillips LR, Maughan P, et al. 1998. Non-contact dipole effects on channel permeation. I. Experiments with (5F-Indole) Trp-13 gramicidin A channels. Biophys. J. 75:2830-44
7. 6. Costa PR, Kocosko DA, Sun BQ, Lansbury PTJ, Griffin RG. 1997. Determination of peptide amide configuration in a model amyloid fibril by solid-state NMR. J. Am. Chem. Soc. 119:10487-95
8. 7. Costa PR, Sun B, Griffin RG. 1997. Rotational resonance tickling: accurate internuclear distance measurement in solids. J. Am. Chem. Soc. 119:10821-30
9. 8. Cotten M, Feng X, Cross TA. 1997. Protein stability and conformational rearrangements in lipid bilayers: linear gramicidin, a model system. Biophys. J. 73:614-23
10. 9. Cotten M, Fu R, Cross TA. 1999. Solid state NMR and hydrogen-deuterium exchange in a bilayer solubilized peplide: structural and mechanistic implications. Biophys. J. In press
11. 10. Cotten M, Soghomonian VG, Hu W, Cross TA. 1997. High resolution and high fields in biological solid-state NMR. Solid State Nucl. Magn. Reson. 9:77-80
12. 11. Crippen GM. 1977. A novel approach to calculation of conformation: distance geometry. J. Comp. Phys. 24:96-107
13. 12. Cross TA. 1994. Structural biology of peptides and proteins in synthetic membrane environments by solid-state NMR spectroscopy. Ann. Rep. NMR Spectrosc. 29:123-67
14. 13. Cross TA. 1997. Solid-state nuclear magnetic resonance characterization of gramicidin channel structure. Meth. Enzymol. 289:672-98
15. 15N spin exchange in a protein. J. Am. Chem. Soc. 105:7471-3
16. 15. Cross TA, Opella SJ. 1983. Protein structure by solid-state NMR. J. Am. Chem. Soc. 105:306-8
17. 16. Cross TA, Opella SJ. 1985. Protein structure by solid-state nuclear magnetic resonance: residues 40 to 45 of bacteriophage fd coat protein. J. Mol. Biol. 182:367-81
18. 17. Cross TA, Opella SJ. 1994. Solid-state NMR structural studies of peptides and proteins in membranes. Curr. Op. Struct. Biol. 4:574-81
19. 18. Demura M, Minami M, Asakura T, Cross TA. 1998. Structure of Bombyx mori silk fibroin based on solid-state NMR orientational constraints and fiber diffraction unit cell parameters. J. Am. Chem. Soc. 120:1300-8
20. 19. Doyle DA, Cabral JM, Pfuetzner RA, Kuo A, Gulbis JM, et al. 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69-77
21. 13C MAS NMR dipolar correlation spectroscopy. Biochemistry 36:7513-19
22. 21. Feng X, Eden M, Brinkmann A, Luthman H, Eriksson L, et al. 1997. Direct determination of a peptide torsional angle ψ by double-quantum solid state NMR. J. Am. Chem. Soc. 119:12006-7
23. 22. Feng X, Lee YK, Sandstrom D, Eden M, Maisel H, et al. 1996. Direct determination of a molecular torsional angle by solid-state NMR. Chem. Phys. Lett. 257:314-20
24. 23. Feng X, Verdegem PJE, Eden M, Sandstrom D, Lee YK, et al. 1999. Determination of a molecular torsional angle in the meta-1 photo-intermediate of bovine Rhodopsin by double-quantum solid state NMR. In press
25. 24. Feng X, Verdegem PJE, Lee YK, Sandstrom D, Eden M, et al. 1997. Direct determination of a molecular torsional angle in the membrane protein Rhodopsin by solid state NMR. J. Am. Chem. Soc. 119:6853-57
26. 25. Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, et al. 1995. The minimum gene complement of Mycoplasma genitalium. Science 270:397-403
27. 26. Fu R, Smith SA, Bodenhausen G. 1997. Recoupling of heteronuclear dipolar interactions in solid state magic-angle spinning NMR by simultaneous frequency and amplitude modulation. Chem. Phys. Lett. 272:361-66
28. 15N-REDOR NMR spectroscopy. J. Am. Chem. Soc. 115:238-44
29. 28. Glaubitz C, Watts A. 1998. Magic angle-oriented sample spinning (MAOSS): a new approach toward biomembrane studies. J. Magn. Reson. 130:305-16
30. 29. Goetz JM, Schaefer J. 1997. Orientational information in solids from REDOR sidebands. J. Magn. Reson. 129:222-23
31. 30. Gregory DM, Mehta MA, Shiels JC, Drobny GP. 1997. Determination of local structure in solid nuclear acids using double quantum nuclear magnetic resonance spectroscopy. J. Chem. Phys. 107:28-42
32. 31. Gregory DW, Mitchell DJ, Stringer JA, Kiihne S, Shiels JC, et al. 1995. Windowless dipolar recoupling: the detection of weak dipolar couplings between spin 1/2 nuclei with large chemical shift anisotropies. Chem. Phys. Lett. 246:654-63
33. 32. Gregory DM, Wolfe G, Jarvie T, Shiels J, Drobny GP. 1996. Double-quantum filtering in magic-angle-spinning NMR spectroscopy applied to DNA oligomers. Mol. Phys. 89:1835-49
34. 27AI TRAPDOR NMR. J. Am. Chem. Soc. 117:8232-42
35. 34. Gröbner G, Choi G, Burnett IJ, Glaubitz C, Verdegem PJE, et al. 1998. Photoreceptor Rhodopsin: structural and conformational study of its chromophore 11-cis retinal in oriented membranes by deuterium solid-state NMR. FEBS Lett. 422:201-4
36. 35. Gullion T. 1995. Measurement of dipolar interactions between spin-1/2 and quadrupolar nuclei by rotational-echo, adiabatic-passage, double-resonance NMR. Chem. Phys. Lett. 246:325-30
37. 36. Gullion T, Baker D, Conradi MS. 1990. New, compensated Carr-Purcell sequences. J. Magn. Reson. 89:479-84
38. 37. Gullion T, Schaefer J. 1989. Rotationalecho double-resonance NMR. J. Magn. Reson. 81:196-200
39. 38. Hall DA, Douglas CM, Gerfen GJ, Inati SJ, Becerra LR, et al. 1997. Polarization-enhanced NMR spectroscopy of biomolecules in frozen solution. Science 276:930-32
40. 39. Harbison GS, Roberts JE, Herzfeld J, Griffin RG. 1988. Solid-state NMR detection of proton exchange between the Bacteriorhodopsin schiff base and bulk water. J. Am. Chem. Soc. 110:7221-23
41. 40. Heller J, Kolbert AC, Larsen R, Ernst M, Bekker T, et al. 1996. Solid-state NMR studies of the prion protein H1 fragment. Protein Sci. 5:1655-61
42. 41. Heller J, Laws DD, Tomaselli M, King DS, Wemmer DE, et al. 1997. Determination of dihedral angles in peptides through experimental and theoretical studies of α-carbon chemical shielding tensors. J. Am. Chem. Soc. 119:7827-31
43. 3-gramicidin A in multiamellar dimyristoylphosphatidylcholine dispersions. Biochemistry 32:7593-604
44. 43. Hing AW, Veda S, Schaefer J. 1992. Transferred-echo double-resonance NMR. J. Magn. Reson. 96:205-9
45. 15N]glycine benzyl ester. J. Am. Chem. Soc. 110:2378-83
46. 45. Hong M, Gross JD, Griffin RG. 1997. Site-resolved determination of peptide torsion angle phi from the relative orientation of backbone N-H and C-H bonds by solid state NMR. J. Phys. Chem. 101: 5869-74
47. 46. Hong M, Gross JD, Rienstra CM, Griffin RG. 1997. Coupling amplification in 2D MAS NMR and its application to torsion angle determination in peptides. J. Magn. Reson. 129:85-92
48. 47. Hu W, Cross TA. 1995. Tryptophan hydrogen bonding and electric dipole moments: functional roles in the gramicidin channel and implications for membrane proteins. Biochemistry 34:14147-55
49. 48. Hu W, Lazo ND, Cross TA. 1995. Tryptophan dynamics and structural refinement in a lipid bilayer environment: solid-state NMR of the gramicidin channel. Biochemistry 34:14138-46
50. 49. Ishii Y, Hirao K, Terao T, Terauchi T, Oba M, et al. 1998. Determination of peptide φ angles in solids by relayed anisotropy correlation NMR. Solid State Nucl. Magn. Reson. 11:169-75
51. 50. Ishii Y, Terao T. 1997. Theory and simulation of vibrational effects on structural measurements by solid-state nuclear magnetic resonance. J. Chem. Phys. 107:2760-74
52. 51. Ishii Y, Terao T. 1998. Manipulation of nuclear spin Hamiltonians by rf-field modulations and its applications to observation of powder patterns under magic-angle spinning. J. Chem. Phys. 109:1-9
53. 52. Ishii Y, Terao T, Kainosho M. 1996. Relayed anisotropy correlation NMR: determination of dihedral angles in solids. Chem. Phys. Lett. 256:133-40
54. 53. Jeener J, Meier BH, Bachmann P, Ernst RR. 1979. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 11:4546-53
55. 15N NMR study on crystalline Leu-and Met-enkephalins: distinction of polymorphs, backbone dynamics, and local conformational rearrangements induced by dehydration or freezing of motions of bound solvent molecules. J. Phys. Chem. 102:2826-34
56. 55. Ketchem R, Hu W, Cross TA. 1993. High-resolution conformation of gramicidin A in a lipid bilayer by solid state NMR. Science 261:1457-60
57. 56. Ketchem RR, Lee K-C, Huo S, Cross TA. 1996. Macromolecular structural elucidation with solid-state NMR-derived orientational constraints. J. Biomol. NMR 8:1-14
58. 57. Ketchem RR, Roux B, Cross TA. 1997. High-resolution polypeptide structure in a lameller phase lipid environment from solid state NMR derived orientational constraints. Structure 5:1655-69
59. 58. Kim Y, Valentine K, Opella SJ, Schendel SL, Cramer WA. 1998. Solid-state NMR studies of the membrane-bound closed state of the colicin E1 channel domain in lipid bilayers. Protein Sci. 7:342-8
60. 59. Koeppe REI, Killian JA, Greathouse DV. 1994. Orientations of the tryptophan9 and 11 side chains of the gramicidin channel based on deuterium nuclear magnetic resonance spectroscopy. Biophys. J. 66:14-24
61. 60. Kovacs F, Cross TA. 1997. Transmembrane four-helix bundle of influenza A M2 protein channel: structural implications from helix tilt and orientation. Biophys. J. 73:2511-17
62. 61. Kumashiro KK, Schmidt-Rohr K, Murphy OJ III, Ouellette KL, Cramer WA, et al. 1998. A novel tool for probing membrane protein structure: solid-state NMR with proton spin diffusion and X-nucleus detection. J. Am. Chem. Soc. 120-5043-51
63. 62. Lansbury PTJ, Costa PR, Griffiths JM, Simon EJ, Ahger M, et al. 1995. Structural model for the β-amyloid fibril based on interstrand alignment of an antiparallel-sheet comprising a C-terminal peptide. Nat. Struct. Biol. 2:990-98
64. 63. Lee D-K, Ramamoorthy A. 1998. A simple one-dimensional solid-state NMR method to characterize the nuclear spin interaction tensors associated with the peptide bond. J. Magn. Reson. 133:204-6
65. 64. Lee K-C 1994. Novel structural constraints and dynamics in the gramicidin cation channel. PhD dissertation. Florida State Univ., Tallahassee. 189 pp.
66. 65. Lee YK, Kurur ND, Helme M, Johnnessen OG, Nielsen NC, et al. 1995. Efficient dipolar recoupling in the NMR of rotating solids. A sevenfold symmetric radiofrequency pulse sequence. Chem. Phys. Lett. 242:304-9
67. 66. Levitt MH, Raleigh DP, Creuzet F, Griffin RG. 1990. Theory and simulations of homonuclear spin pair systems in rotating solids. J. Chem. Phys. 92:6347-64
68. 67. Li Y, Evans JNS. 1995. The importance of XY-8 phase cycling in the rotational-echo double-resonance experiment with total sideband suppresion. J. Magn. Reson. Ser. A 116:150-55
69. 68. Linder M, Hohener A, Ernst RR. 1980. Orientation of tensorial interactions determined from two-dimensional NMR powder spectra. J. Chem. Phys. 73:4959-70
70. 69. Lizak MJ, Gullion T, Conradi MS. 1991. Measurement of like-spin dipole couplings. J. Magn. Reson. 91:254-60
71. 70. Mai W, Hu W, Wang C, Cross TA. 1993. Orientational constraints as three-dimensional structural constraints from chemical shift anisotropy: the polypeptide backbone of gramicidin A in a lipid bilayer. Protein Sci. 2:532-42
72. 15N-labeled membrane protein in phospholipid bilayers. Proc. Natl. Acad. Sci. USA 94:8551-56
73. 72. Marsh RE, Corey RB, Pauling L. 1955. An investigation of the structure of silk fibroin. Biochim. Biophys. Acta 16:1-34
74. 13C REDOR, X-ray diffraction, and molecular dynamics calculation. J. Phys. Chem. 100:14995-5004
75. 15N-REDOR NMR spectroscopy. Chem. Phys. Lett. 229:506-11
76. 75. Neuhaus D, Williamson M. 1989. The Nuclear Overhauser Effect in Structural and Conformational Analysis. Weinheim, Germany: VCH
77. 13C chemical shifts. J. Phys. Chem. B 102: 7476-83
78. 77. Normile D. 1998. Race for stronger magnets turns into marathon. Science 281: 164-65
79. 78. North CL, Cross TA. 1995. Correlations between function and dynamics: time scale coincidence for ion translocation and molecular dynamics in the gramicidin channel backbone. Biochemistry 34: 5883-95
80. 79. Oas TG, Griffin RG, Levitt MH. 1988. Rotary resonance recoupling of dipolar interactions in solid-state nuclear magnetic resonance spectroscopy. J. Chem. Phys. 89:692-95
81. 13C dipole-coupled chemical shift powder patterns. J. Am. Chem. Soc. 109:5962-66
82. 81. Ok JH, Spencer RGS, Bennett AE, Griffin RG. 1992. Homonuclear correlation spectroscopy in rotating solids. Chem. Phys. Lett. 197:389-95
83. 82. Oldfield E, Rothgeb TM. 1980. NMR of individual sites in protein crystals. Magnetic ordering effects. J. Am. Chem. Soc. 102:3635-37
84. 83. Opella SJ. 1997. NMR and membrane proteins. Nat. Struct. Biol. 4(Suppl.):845-48
85. 84. Pascal SM, Cross TA. 1993. High-resolution structure and dynamic implications for a double-helical gramicidin A conformer. J. Biomol. NMR 3:495-513
86. 85. Pebay-Peyroula E, Rummel G, Rosenbush JP, Landau EM. 1997. X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science 277:1676-81
87. 2H nuclear nagnetic resonance of the gramicidin A backbone in a phospholipid bilayer. Biochemistry 30:4687-96
88. 87. Prosser RS, Hunt SA, DiNatale JA, Vold RR. 1996. Magnetically aligned membrane model systems with positive order parameter: switching the sign of Szz with paramagnetic ions. J. Am. Chem. Soc. 118:269-70
89. 88. Ramamoorthy A, Gierasch LM, Opella SJ. 1995. Four-dimensional solid-state NMR experiment that correlates the chemical-shift and dipolar-coupling frequencies of two heteronuclei with the exchange of dilute-spin magnetization. J. Magn. Reson. 109:112-16
90. 89. Ramamoorthy A, Gierasch LM, Opella SJ. 1996. Three-dimensioal solid-state NMR correlation experiment with 1H homonuclcar spin exchange. J. Magn. Reson. 111:81-84
91. 90. Sanders CR, Landis GC. 1995. Reconstitution of membrane proteins into lipidrich bilayered mixed micelles for NMR studies. Biochemistry 34:4030-40
92. 91. Schmidt-Rohr K. 1996. A double-quantum solid-state NMR for determining torsion angles in polymers. Macromolecules 29:3975-81
93. 13C-labeled amino acids and peptides by separated-local-field double-quantum NMR. J. Am. Chem. Soc. 118:7601-3
94. 1H combined rotation and multiple pulse spectroscopy NMR. J. Am. Chem. Soc. 118:7604-7
95. 94. Shon K-J, Kim Y, Colnage LA, Opella SJ. 1991. NMR studies of the structure and dynamics of membrane-bound bacteriophage Pf1 coat protein. Science 252:1303-8
96. 95. Simmons AH, Michal CA, Jelinski LW. 1996. Molecular orientation and two-component nature of the crystalline fraction of spider dragline silk. Science 271: 84-87
97. 96. Smith R, Separovic F, Milne TJ, Whittaker A, Bennett FM, et al. 1994. Structure and orientation of the pore-forming peptide, melittin, in lipid bilayers. J. Mol. Biol. 241:456-66
98. 13C-NMR studies of the effects of sodium ions on the gramicidin A ion channel. Biochim. Biophys. Acta 1026:161-66
99. 98. Spencer RGS, Halverson KJ, Auger M, McDermott AE, Griffin RG, et al. 1991. An unusual peptide conformation may precipitate amyloid formation in Alzheimer's disease: application of solid-state NMR to the determination of protein secondary structure. Biochemistry 30:10382-87
100. 99. Takegoshi K, Nomura K, Terao T. 1995. Rotational resonance in the tilted rotating frame. Chem. Phys. Lett. 232:424-28
101. 14N electric field gradient tensor orientations with respect to the molecular frame in a polypeptide. J. Am. Chem. Soc. 114:5312-21
102. 101. Terao T. 1998. Structural measurements by solid-state NMR. J. Mol. Struct. 441: 283-394
103. 102. Terwilliger TC, Weissman L, Eisenberg D. 1982. The structure of melittin in the form I crystals and its implications for melittin's lytic and surface activities. Biophys. J. 37:353-61
104. 103. Tycko R, Dabbagh G. 1990. Measurement of nuclear magnetic dipole-dipole couplings in magic angle spinning NMR. Chem. Phys. Lett. 173:461-65
105. 104. Tycko R, Dabbagh G, Mirau PA. 1989. Determination of chemical-shift-anosotropy lineshapes in a two-dimensional magic-angle-spinning NMR experiment. J. Magn. Reson. 85:265-74
106. 105. Tycko R, Weliky DP, Berger AE. 1996. Investigation of molecular structure in solids by two-dimensional NMR exchange spectroscopy with magic angle spinning. J. Chem. Phys. 105:7915-30
107. 106. Ulrich AS, Wallat I, Heyn MP, Watts A. 1995. Re-orientation of retinal in the M-photointermediate of Bacteriorhodopsin. Struct. Biol. 2:190-92
108. 2H-NMR. Biochemistry 33: 5370-75
109. 13C MAS NMR spectroscopy. J. Am. Chem. Soc. 119:169-74
110. 109. Weliky DP, Tycko R. 1996. Determination of peptide conformations by two-dimensional magic angle spinning NMR exchange spectroscopy with rotor synchronization. J. Am. Chem. Soc. 118: 8487-88
111. 110. Wu CH, Ramamoorthy A, Opella SJ. 1994. High-resolution heteronuclear dipolar solid-state NMR spectroscopy. J. Magn. Reson. 109:270-72
112. 13C NMR. J. Biochem. 123:78-86
113. 112. Yamazaki T, Otomo T, Oda N, Kyogoku Y, Uegaki, et al. 1998. Segmental isotope labeling for protein NMR using peptide splicing. J. Am. Chem. Soc. 120:5591-92
114. 113. Zwahlen C, Vincent SJF, Di Bari L, Levitt MH, Bodenhausen G. 1994. Quenching spin diffusion in selective measurements of transient overhauser effects in nuclear magnetic resonance. Applications to oligonucleotides. J. Am. Chem. Soc. 116: 362-68