Solid-state NMR for the analysis of high-affinity ligand/receptor Interactions

Concepts in Magnetic Resonance Part A: Bridging Education and Research

Volumn 34, Issue 3, 2009, Pages 144-172

  Williamson, P T F ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Dipolar recoupling; Ligands; Magic angle spinning; Membrane proteins; Oriented samples; Pharmacology; Rational drug design; Receptors; Small molecules

Indexed keywords

EID: 67649399085     PISSN: 15466086     EISSN: 15525023     Source Type: Journal    
DOI: 10.1002/cmr.a.20140     Document Type: Article

References (157)

1. Blundell TL, Jhoti H, Abell C. 2002. High-throughput crystallography for lead discovery in drug design. Nat Rev Drug Discov 1:45-53.
2. Pellecchia M, Sem DS, Wurthrich K. 2002. NMR in drug discovery. Nat Rev Drug Discov 1:211-219.
3. Roberts GCK. 2000. Application of NMR in drug discovery. Drug Discov Today 5:230-240.
4. Wallin E, von Heijne G. 1998. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7:1029-1038.
5. Terstappen GC, Reggiani A. 2001. In silico research in drug discovery. Trends Pharmacol Sci 22:23-26.
6. Drews J. 2000. Drug discovery: a historical perspective. Science 287:1960-1964.
7. Hadjuk PJ, Meadows RP, Fesik SW. 1999. NMR based screening in drug discovery. Q Rev Biophys 32:211-240.
8. Peng JW, Moore J, Abdul-Manan N. 2004. NMR experiments for lead generation in drug discovery. Prog Nuclear Magn Reson Spectrosc 44:225-256.
9. Post CB. 2003. Exchange-transferred NOE spectroscopy and bound ligand structure determination. Curr Opin Struct Biol 13:581-588.
10. Grisshammer R. 2006. Understanding recombinant expression of membrane proteins. Curr Opin Biotechnol 17:337-340.
11. Williamson PTF, Bains S, Chung C, Cooke R, Watts A. 2002. Probing the environment of neurotensin whilst bound to the neurotensin receptor by solid state NMR. FEBS Lett 518:111-115.
12. Luca S, White JF, Sohal AK, Filippov DV, van Boom JH, Grisshammer R, et al. 2003. The conformation of neurotensin bound to its G proteincoupled receptor. Proc Natl Acad Sci USA 100:10706-10711.
13. Grisshammer R, Tate CG. 1995. Overexpression of integral membrane-proteins for structural studies. Q Rev Biophys 28:315-422.
14. Sarramegna V, Talmont R, Demange P, Milon A. 2003. Heterologous expression of G-proteincoupled receptors: comparison of expression systems from the standpoint of large-scale production and purification. Cell Mol Life Sci 60:1529-1546.
15. Tate CG. 2001. Overexpression of mammalian integral membrane proteins for structural studies. FEBS Lett 504:94-98.
16. Long SB, Campbell EB, MacKinnon R. 2005. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309:897-903.
17. Tornroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, et al. 2006. Structural mechanism of plant aquaporin gating. Nature 439:688-694.
18. Jidenko M, Nielsen RC, Sorensen TLM, Moller JV, le Maire M, Nissen P, et al. 2005. Crystallization of a mammalian membrane protein overexpressed in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 102:11687-11691.
19. Creemers AFL, Klaassen CHW, Bovee-Geurts PHM, Kelle R, Kragl U, Raap J, et al. 1999. Solid state N-15 NMR evidence for a complex Schiff base counterion in the visual G-protein-coupled receptor rhodopsin. Biochemistry 38:7195-7199.
20. Ratnala VRP, Swarts HGP, VanOostrum J, Leurs R, DeGroot HJM, Bakker RA, et al. 2004. Largescale overproduction, functional purification and ligand affinities of the His-tagged human histamine H1 receptor. Eur J Biochem 271:2636-2646.
21. Ratnala VR, Kiihne SR, Buda F, Leurs R, de Groot HJ, DeGrip WJ. 2007. Solid-state NMR evidence for a protonation switch in the binding pocket of the H1 receptor upon binding of the agonist histamine. J Am Chem Soc 129:867-872.
22. Klammt C, Lohr F, Schafer B, Haase W, Dotsch V, Ruterjans H, et al. 2004. High level cell-free expression and specific labeling of integral membrane proteins. Eur J Biochem 271:568-580.
23. Seddon AM, Curnow P, Booth PJ. 2004. Membrane proteins, lipids and detergents: not just a soap opera. Biochim Biophys Acta 1666:105-117.
24. Lee AG. 2004. How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta 1666(1/2):62-87.
25. Pervushin K, Riek R, Wider G, Wuthrich K. 1997. 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 USA 94:12366-12371.
26. Herzfeld J, Berger AE. 1980. Sideband intensities in NMR spectra of samples spinning at the magic angle. J Chem Phys 73:6021-6030.
27. Ge MT, Budil DE, Freed JH. 1994. ESR studies of spin-labelled membranes aligned by isopotential spin-dry ultracentrifugation-lipid protein interactions. Biophys J 67:2326-2344.
28. Jarrell HC, Jovall PA, Giziewicz JB, Turner LA, Smith ICP. 1987. Determination of conformational properties of glycolipid headgroups by H-2 NMR of oriented multibilayers. Biochemistry 26:1805-1811.
29. Auge S, Mazarguil H, Tropis M, Milon A. 1997. Preparation of oriented lipid bilayers on ultrathin polymers for solid state NMR analyses of peptide-membrane interactions. J Magn Reson 124:455-458.
30. Grobner G, Taylor A, Williamson PTF, Choi G, Glaubitz C, Watts JA, et al. 1997 Macroscopic orientation of natural and model membranes for structural studies. Anal Biochem 254:132-138.
31. Sanders CR, Schwonek JP. 1992. Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid state NMR. Biochemistry 31:8898-8905.
32. Vold RR, Prosser RS. 1996. Magnetically oriented phospholipid bilayered micelles for structural studies of polypeptides. Does the ideal bicelle exist? J Magn Reson B 113:267-271.
33. Sanders CR, Hare BJ, Howard KP, Prestegard JH. 1994. Magnetically oriented phospholipid micelles as a tool for the study of membrane-associated molecules. Prog Nuclear Magn Reson Spectrosc 26:421-444.
34. Sanders CR, Prestegard JH. 1990. Magnetically orientable phospholipid bilayers containing small amount of a bile salt analogue, CHAPSO. Biophys J 58:447-460.
35. Ram P, Prestegard JH. 1988. Magnetic field induced ordering of bile salt/phospholipid micelles: new media for NMR structural investigations. Biochim Biophys Acta 940:289-294.
36. Prosser RS, Hunt SA, DiNatale JA, Vold RR. 1996. Magnetically aligned membrane model systems with positive order parameter: switching the sign of S-zz with paramagnetic ions. J Am Chem Soc 118:269-270.
37. Prosser RS, Volkov VB, Shiyanovskaya IV. 1998. Novel chelate-induced magnetic alignment of biological membranes. Biophys J 75:2163-2169.
38. Williamson PTF, Zandomeneghi G, Barrantes FJ, Watts A, Meier BH. 2005. Structure and dynamic analysis of the M4-TMD of the nicotinic acetylcholine receptor. Mol Membr Biol 22:485-496.
39. Zandomeneghi G, Meier BH. 2004. Adiabatic-passage cross polarization in N-15 NMR spectroscopy ofpeptides weakly associated to phospholipids: determination of large RDC. J Biomol NMR 30:303-309.
40. Zandomeneghi G, Williamson PTF, Hunkler A, Meier BH. 2003. Switched-angle spinning applied to bicelles containing phospholipid-associated peptides. J Biomol NMR 25:125-132.
41. Chandrasekhar I, van Gunsteren W, Zandomeneghi G, Williamson PTF, Meier BH. 2006. Orientation and conformational preference of leucine-enkephalin at the surface of a hydrated dimyristoylphosphatidylcholine bilayer: NMR and MD simulation. J Am Chem Soc 128:159-170.
42. Triba MN, Zoonens M, Popot JL, Devaux PF, Warschawski DE. 2006. Reconstitution and alignment by a magnetic field of a beta-barrel membrane protein in bicelles. Eur Biophys J 35:268-275.
43. Marcotte I, Auger M. 2005. Bicelles as model membranes for solid- and solution-state NMR studies of membrane peptides and proteins. Concepts Magn Reson A 24:17-37.
44. Bennett AE, Rienstra CM, Auger M, Lakshmi KV, Griffin RG. 1995. Heteronuclear decoupling in rotating solids. J Chem Phys 103:6951-6958.
45. Detken A, Hardy EH, Ernst M, Meier BH. 2002. Simple and efficient decoupling in magic-angle spinning solid state NMR; the XiX scheme. Chem Phys Lett 356:298-304.
46. Yu Y, Fung BM. 1998. An efficient broadband decoupling sequence for liquid crystals. J Magn Reson 130:317-320.
47. Fung BM, Khitrin AK, Ermolaev K. 2000. An improved broadband decoupling sequence for liquid crystals and solids. J Magn Reson 142:97-101.
48. Sinha N, Grant CV, Wu CH, de Angelis AA, Howell SC, Opella SJ. 2005. SPINAL modulated decoupling in high field double and triple resonance solid-state NMR experiments on stationary samples. J Magn Reson 177:197-202.
49. Verel R, van Beek JD, Meier BH. 1999. INADEQUATE-CR experiments in the solid state. J Magn Reson 140:300-303.
50. Baldus M, Meier BH. 1996. Total correlation spectroscopy in the solid state. The use of scalar couplings to determine the through-bond connectivity. J Magn Reson A 121:65-69.
51. Lesage A, Emsley L. 2001. Through-bond heteronuclear single-quantum correlation spectroscopy in solid-state NMR, and comparison to other throughbond and through-space experiments. J Magn Reson 148:449-454.
52. Hartmann SR, Hahn EL. 1962. Nuclear double resonance in the rotating frame. Phys Rev Lett 128:2042-2053.
53. Stejskal EO, Schaefer J, Waugh JS. 1977. Magicangle spinning and polarization trasnfer in proton enhanced NMR. J Magn Reson 28:105-112.
54. Krahn A, Priller U, Emsley L, Engelke F. 2008. Resonator with reduced sample heating and increased homogeneity for solid-state NMR. J Magn Reson 191:78-92.
55. Gorkov PL, Chekmenev EY, Li C, Cotten M, Buffy JJ, Traaseth NJ, et al. 2007. Using low-E resonators to reduce RF heating in biological samples for static solid-state NMR up to 900MHz. J Magn Reson 185:77-93.
56. Dillmann B, Elbayed K, Zeiger H, Weingertner MC, Piotto M, Engelke F. 2007. A novel low-E field coil to minimize heating of biological samples in solid-state multinuclear NMR experiments. J Magn Reson 187:10-18.
57. Stringer JA, Bronnimann CE, Mullen CG, Zhou DHH, Stellfox SA, Li Y, et al. 2005. Reduction of RF-induced sample heating with a scroll coil resonator structure for solid-state NMR probes. J Magn Reson 173:40-48.
58. Peersen OB, Wu XL, Kustanovich I, Smith SO. 1993. Variable-amplitude cross-polarization MAS NMR. J Magn Reson A 104:334-339.
59. Hediger S, Meier BH, Kurur ND, Bodenhausen G, Ernst RR. 1994. NMR Cross-polarization by adiabatic passage through the Hartmann-Hahn condition (APHH). Chem Phys Lett 223:283-288.
60. Warschawski DE, Devaux P. 2000. Polarization transfer in lipid membranes. J Magn Reson 145: 367-372.
61. Dvinskikh SV, Yamamoto K, Ulrich HN, Ramamoorthy A. 2007. Sensitivity and resolution enhancement in solid-state NMR spectroscopy of bicelles. J Magn Reson 183:228-235.
62. Bielecki A, Kolbert AC, Levitt MH. 1989. Frequency- switched pulse sequences-homonuclear decoupling and dilute spin NMR in solids. Chem Phys Lett 155(4/5):341-346.
63. vanRossum BJ, Forster H, deGroot HJM. 1997. High-field and high-speed CP-MAS C-13 NMR heteronuclear dipolar-correlation spectroscopy of solids with frequency-switched Lee-Goldburg homonuclear decoupling. J Magn Reson 124:516-519.
64. Rhim RK, Elleman DD, Vaughn RW. 1972. J Chem Phys 59:3740.
65. Mansfield P. 1971. J Chem Phys C 4:1444.
66. van Rossum BJ, Castellani F, Pauli J, Rehbein K, Hollander J, de Groot HJM, et al. 2003. Assignment of amide proton signals by combined evaluation of HN, NN and HNCA MAS-NMR correlation spectra. J Biomol Nmr 25:217-223.
67. Creemers AFL, Kiihne S, Bovee-Geurts PHM, DeGrip WJ, Lugtenburg J, de Groot HJM. 2002. H-1 and C-13 MAS NMR evidence for pronounced ligand-protein interactions involving the ionone ring of the retinylidene chromophore in rhodopsin. Proc Natl Acad Sci USA 99:9101-9106.
68. van Rossum BJ, Schulten EAM, Raap J, Oschkinat H, de Groot HJM. 2002. A 3-D structural model of solid self-assembled chlorophyll a/H2O from multispin labeling and MAS NMR 2-D dipolar correlation spectroscopy in high magnetic field. J Magn Reson 155:1-14.
69. Huster D, Schiller J, Arnold K. 2002. Comparison of collagen dynamics and isolated fibrils by solidstate in articular cartilage NMR Spectroscopy. Magn Reson Med 48:624-632.
70. Lorieau J, McDermott AE. 2006. 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 44:334-347.
71. Lorieau JL, McDermott AE. 2006. Conformational flexibility of a microcrystalline globular protein: order parameters by solid-state NMR spectroscopy. J Am Chem Soc 128:11505-11512.
72. Baldus M, Geurts DG, Hediger S, Meier BH. 1996. Efficient N-15-C-13 polarization transfer by adiabatic-passage Hartmann-Hahn cross polarization. J Magn Reson A 118:140-144.
73. Detken A, Hardy EH, Ernst M, Kainosho M, Kawakami T, Aimoto S, et al. 2001. Methods for sequential resonance assignment in solid uniformly 13C, 15N labelled peptides, quantification and application to antamanide. J Biomol NMR 20:203-221.
74. Pauli J, Baldus M, van Rossum B, de Groot HJM, Oschkinat H. 2001. Backbone and sidechain assignments of the alpha spectrin SH3 domain by magic angle spinning solid state NMR at 17.6T. Chembiochem 2:272-281.
75. Gullion T, Schaefer J. 1989. Rotational echo double resonance NMR. J Magn Reson 81:196-200.
76. Hing AW, Schaefer J. 1993. Two-dimensional rotational- echo double resonance of Val1-[1-13C]Gly2-[15N]Ala3-gramicidin A in multilamellar dimyristoylphosphatidylcholine dispersions. Biochemistry 32:7593-7604.
77. McDowell LM, Klug CA, Beusen DD, Schaefer J. 1996. Ligand geometry of the ternary complex of 5-enolpyruvylshikimate-3-phosphate synthase from rotational-echo double-resonance NMR. Biochemistry 35:5395-5340.
78. Studelska DR, McDowell LM, Adler M, O'Connor RD, Mehta AK, Guilford WJ, et al. 2003. Conformation of a bound inhibitor of blood coagulant factor Xa. Biochemistry 42:7942-7949.
79. Jaroniec CP, MacPhee CE, Astrof NS, Dobson CM, Griffin RG. 2004. Molecular conformation of a peptide fragment of transthyretin in an amyloid fibril. Proc Natl Acad Sci USA 99:16748-16753.
80. Watts JA, Watts A, Middleton DA. 2001. A model of reversible inhibitors in the gastric H+/K+-ATPase binding site determined by rotational echo double resonance NMR. J Biol Chem 276:43197-43204.
81. Murphy OJ, Kovacs FA, Sicard EL, Thompson LK. 2001. Site-directed solid-state NMR measurement of a ligand-induced conformational change in the serine bacterial chemoreceptor. Biochemistry 40:1358-1366.
82. Jaroniec CP, Tounge BA, Herzfeld J, Griffin RG. 2001. Frequency selective heteronuclear dipolar recoupling in rotating solids: accurate 13C-15N distance measurements in uniformly 13C-15N labeled peptides. J Am Chem Soc 123:3507-3519.
83. Rienstra CM, Tucker A, Jaroniec CP, Hohwy M, Reif B, McMahon B, et al. 2002. De novo determination of peptide structure with solid-state magicangle spinning NMR spectroscopy. Proc Natl Acad Sci USA 99:10260-10265.
84. Levitt MH, Raleigh DP, Creuzet F, Griffin RG. 1990. Theory and simulations of homonuclear spin pair systems in rotating solids. J Chem Phys 92:6347-6364.
85. Raleigh DP, Levitt MH, Griffin RG. 1988. Rotational resonance in solid-state NMR. Chem Phys Lett 146(1/2):71-76.
86. Colombo MG, Meier BH, Ernst RR. 1988. Rotordriven spin diffusion in natural-abundance C-13 spin systems. Chem Phys Lett 146:189-196.
87. Peersen OB, Groesbeek M, Aimoto S, Smith SO. 1995. Analysis of rotational resonance magnetization exchange curves from crystalline peptides. J Am Chem Soc 117:7228-7237.
88. Costa PR, Sun BQ, Griffin RG. 1997. Rotational resonance tickling: accurate internuclear distance measurement in solids. J Am Chem Soc 119: 10821-10830.
89. Detken A, Hardy EH, Ernst M, Kainosho M, Kawakami T, Aimoto S, et al. 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.
90. Williamson PTF, Verhoeven A, Miller KW, Meier BH, Watts A. 2007. Conformation of acetylcholine at its target site in the membrane embedded nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 104:18031-18036.
91. Williamson PTF, Verhoeven A, Ernst M, Meier BH. 2003. Determination of internuclear distances in uniformly labeled molecules by rotational-resonance solid-state NMR. J Am Chem Soc 125:2718-2722.
92. Verhoeven A, Williamson PTF, Zimmermann H, Ernst M, Meier BH. 2004. Rotational-resonance distance measurements in multi-spin systems. J Magn Reson 168:314-326.
93. Ladizhansky V, Griffin RG. 2004. Band-selective carbonyl to aliphatic side chain 13C-13C distance measurements in U-13C, 15N-labeled solid peptides by magic angle spinning NMR. J Am Chem Soc 126:948-958.
94. Petkova AT, Tycko R. 2004. Rotational resonance in uniformly C-13-labeled solids: effects on highresolution magic-angle spinning NMR spectra and applications in structural studies of biomolecular systems. J Magn Reson 168:137-146.
95. Grommek A, Meier BH, Ernst M. 2006. Distance information from proton-driven spin diffusion under MAS. Chem Phys Lett 427:404-409.
96. 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.
97. Takegoshi K, Nakamura S, Terao T. 2001. C-13-H-1 dipolar-assisted rotational resonance in magicangle spinning NMR. Chem Phys Lett 344(5/6):631-637.
98. Bennett AE, Ok JH, Griffin RG, Vega S. 1992. Chemical-shift correlation spectroscopy in rotating solids-radio frequency-driven dipolar recoupling and longitudinal exchange. J Chem Phys 96:8624-8627.
99. 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.
100. Hohwy M, Jakobsen HJ, Eden 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 108:2686-2694.
101. Nielsen NC, Bildsoe H, Jakobsen HJ, Levitt MH. 1994. Double-quantum homonuclear rotary resonance-efficient dipolar recovery in magic-anglespinning nuclear-magnetic-resonance. J Chem Phys 101:1805-1812.
102. Verel R, Ernst M, Meier BH. 2001. Adiabatic dipolar recoupling in solid-state NMR: the DREAM scheme. J Magn Reson 150:81-99.
103. 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.
104. Marin-Montesinos I, Brouwer DH, Antonioli G, Lai WC, Brinkmann A, Levitt MH. 2005. Heteronuclear decoupling interference during symmetrybased homonuclear recoupling in solid-state NMR J Magn Reson 177:307-317.
105. Concistre M, Gansmueller A, McLean N, Johannessen OG, Manrin Montesinos I, Bovee-Geurts PHM, et al. 2008. Double quantum 13C nuclear magnetic resonance of bathorhodopsin, the first photointermediate in mammalian vision. J Am Chem Soc 130:10490-10491.
106. Neue G, Dybowski C. 1997. Determining temperature in a magic angle spinning probe using the temperature dependence of the isotropic chemical shift of lead nitrate. Solid State Nucl Magn Reson 7:333-336.
107. Kelly AE, Ou HD, Withers R, Dotsch V. 2002. Low-conductivity buffers for high-sensitivity NMR measurements. J Am Chem Soc 124:12013-12019.
108. Gor'kov PL, Chekmenev EY, Fu RQ, Hu J, Cross TA, Cotten M, et al. 2006. A large volume flat coil probe for oriented membrane proteins. J Magn Reson 181:9-20.
109. Doty FD, Kulkarni J, Turner C, Entzminger G, Bielecki A. 2006. Using a cross-coil to reduce RF heating by an order of magnitude in triple-resonance multinuclear MAS at high fields. J Magn Reson 182:239-253.
110. Abragham A. 1961. Principles of Nuclear Magnetic Resonance. Oxford: Clarendon.
111. Jakeman DL, Mitchell DJ, Shuttleworth WA, Evans JN. 1998. Effects of sample preparation conditions on biomolecular solid-state NMR lineshapes. J Biomol NMR 12:417-421.
112. Middleton DA, Robins R, Feng XL, Levitt MH, Spiers ID, Schwalbe CH, et al. 1997. The conformation of an inhibitor bound to the gastric proton pump. FEBS Lett 410(2/3):269-274.
113. Williamson PTF, Grobner G, Spooner PJR, Miller KW, Watts A. 1998. Probing the agonist binding pocket in the nicotinic acetylcholine receptor: a high-resolution solid-state NMR approach. Biochemistry 37:10854-10859.
114. Glaubitz C, Groger A, Gottschalk K, Spooner P, Watts A, Schuldiner S, et al. 2000. P-31-CP-MAS NMR studies on TPP+ bound to the ion-coupled multidrug transport protein EmrE. FEBS Lett 480(2/3):127-131.
115. Spooner PJR, Rutherford NG, Watts A, Henderson PJF. 1994. NMR observation of substrate in the binding-site of an active sugar-H+ symport protein in native membranes. Proc Natl Acad Sci USA 91:3877-3881.
116. Spooner PJR, O'Reilly WJ, Homans SW, Rutherford NG, Henderson PJF, Watts A. 1998. Weak substrate binding to transport proteins studied by NMR. Biophys J 75:2794-2800.
117. Appleyard AN, Herbert RB, Henderson PJF, Watts A, Spooner PJR. 2000. Selective NMR observation of inhibitor and sugar binding to the galactose-H+ symport protein GalP, of Escherichia coli. Biochim Biophys Acta 1509(1/2):55-64.
118. Patching SG, Brough AR, Herbert RB, Rajakarier JA, Henderson PJF, Middleton DA. 2004. Substrate affinities for membrane transport proteins determined by C-13 cross-polarization magic-angle spinning nuclear magnetic resonance spectroscopy. J Am Chem Soc 126:3072-3080.
119. Patching SG, Herbert RB, O'Reilly J, Brough AR, Henderson PJF. 2004. Low C-13-background for NMR-based studies of ligand binding using C-13-depleted glucose as carbon source for microbial growth: C-13-labeled glucose and C-13-forskolin binding to the galactose-H+ symport protein GaIP in Escherichia coli. J Am Chem Soc 126:86-87.
120. Degroot HJM, Copie V, Smith SO, Allen PJ, Winkel C, Lugtenburg J, et al. 1988. Magic-angle-sample-spinning NMR difference spectroscopy. J Magn Reson 77:251-257.
121. Patching SG, Psakis G, Baldwin SA, Baldwin J, Henderson PJ, Middleton DA. 2008. Relative substrate affinities of wild-type and mutant forms of the Escherichia coli sugar transporter GalP determined by solid-state NMR. Mol Membr Biol 25(6/ 7):474-484.
122. Krabben L, van Rossum BJ, Weise C, Hucho F, Bocharov E, Shulga AA, et al. 2005. Neurotoxin II bound to the nicotinic acetylcholine receptor shows little structural changes: a solid-state NMR approach. FEBS J 272:376-376.
123. Lange A, Giller K, Hornig S, Martin-Eauclaire MF, Pongs O, Becker S, et al. 2006 Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440:959-962.
124. Verel R, Baldus M, Ernst M, Meier BH. 1998. A homonuclear spin-pair filter for solid-state NMR based on adiabatic-passage techniques. Chem Phys Lett 287(3/4):421-428.
125. Wishart DS, Sykes BD, Richards FM. 1991. Relationship between nuclear-magnetic-resonance chemical-shift and protein secondary structure. J Mol Biol 222:311-333.
126. Luca S, Filippov DV, van Bloom JH, Oschkinat H, de Groot HJM, Baldus M. 2001. Secondary chemical shifts in immobilized peptides and proteins: a qualitative basis for structure refinement under magic angle spinning. J Biomol NMR 20:325-331.
127. 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.
128. Middleton DA, Rankin S, Esmann M, Watts A. 2000. Structural insights into the binding of cardiac glycosides to the digitalis receptor revealed by solid-state NMR. Proc Natl Acad Sci USA 97:13602-13607.
129. Degroot HJM, Harbison GS, Herzfeld J, Griffin RG. 1989. Nuclear magnetic-resonance study of the Schiff-base in bacteriorhodopsin-counterion effects on the N-15 shift anisotropy. Biochemistry 28:3346-3353.
130. Smith SO, Palings I, Miley ME, Courtin J, Degroot H, Lugtenburg J, et al. 1990. Solid-state NMRstudies of the mechanism of the opsin shift in the visual pigment rhodopsin. Biochemistry 29:8158-8164.
131. Smith SO, Courtin J, Degroot H, Gebhard R, Lugtenburg J. 1991. C-13 magic-angle spinning NMRstudies of bathorhodopsin, the primary photoproduct of rhodopsin. Biochemistry 30:7409-7415.
132. Creemers AFL, Bovee-Geurts PHM, DeGrip WJ, Lugtenburg J, de Groot HJM. 2004. Solid-state NMR analysis of ligand-receptor interactions reveals an induced misfit in the binding site of isorhodopsin. Biochemistry 43:16011-16018.
133. La Penna G, Buda F, Bifone A, de Groot HJM. 1998. The transition state in the isomerization of rhodopsin. Chem Phys Lett 294:447-453.
134. Buda F, De Groot HJM, Bifone A. 1996. Charge localization and dynamics in rhodopsin. Phys Rev Lett 77:4474-4477.
135. Han M, Dedecker BS, Smith SO. 1993. Localization of the retinal protonated schiff-base counterion in rhodopsin. Biophys J 65:899-906.
136. EgorovaZachernyuk TA, vanRossum B, Boender GJ, Franken E, Ashurst J, Raap J, et al. 1997. Characterization of pheophytin ground states in Rhodobacter sphaeroides R26 photosynthetic reaction centers from multispin pheophytin enrichment and 2-D C-13 MAS NMR dipolar correlation spectroscopy. Biochemistry 36:7513-7519.
137. Kiihne S, Creemers AFL, de Grip WJ, Bovee-Geurts PHM, Lugtenburg J, de Groot HJM. 2005. Selective interface detection: mapping binding site contacts in membrane proteins by NMR spectroscopy. J Am Chem Soc 127:5734-5735.
138. Crocker E, Patel AB, Eilers M, Jayaraman S, Getmanova E, Reeves PJ, et al. 2004. Dipolar assisted rotational resonance NMR of tryptophan and tyrosine in rhodopsin. J Biomol NMR 29: 11-20.
139. Etzkorn M, Bockmann A, Lange A, Baldus M. 2004. Probing molecular interfaces using 2D magic-angle-spinning NMR on protein mixtures with different uniform labeling. J Am Chem Soc 126:14746-14751.
140. Helmle M, Lee YK, Verdegem PJE, Feng X, Karlsson T, Lugtenburg J, et al. 1999. Anomalous rotational resonance spectra in magic-angle spinning NMR. J Magn Reson 140:379-403.
141. Verdegem PJE, Helmle M, Lugtenburg J, De Groot HJM. 1997. Internuclear distance measurements up to 0.44 nm for retinals in the solid-statewith 1-D rotational resonance NMR spectroscopy. J Am Chem Soc 119:169-174.
142. Verdegem PJE, Bovee-Geurts PHM, de Grip WJ, Lugtenburg J, de Groot HJM. 1999. Retinylidene ligand structure in bovine rhodopsin, metarhodopsin-I, and 10-methylrhodopsin from internuclear distance measurements using C-13-labeling and 1-D rotational resonance MAS NMR. Biochemistry 38:11316-11324.
143. Verhoeven A, Williamson PTF, Zimmermann H, Ernst M, Meier BH. 2004. Rotational-resonance distance measurements in multi-spin systems. J Magn Reson 168:314-326.
144. Heller J, Larsen R, Ernst M, Kolbert AC, Baldwin M, Prusiner SB, et al. 1996. Application of rota-SS-NMR FOR ANALYSIS OF LIGAND/RECEPTOR INTERACTIONS 171 tional resonance to inhomogeneously broadened systems. Chem Phys Lett 251:223-229.
145. Lansing JC, Hohwy M, Jaroniec CP, Creemers AFL, Lugtenburg J, Herzfeld J, et al. 2002. Chromophore distortions in the bacteriorhodopsin photocycle: evolution of H-C14-C15-H dihedral angle measured by solid-state NMR. Biochemistry 41:431-438.
146. Feng X, Verdegem PJE, Eden M, Sandstrom D, Lee YK, Bovee-Geurts PHM, et al. 2000. Determination of a molecular torsional angle in the metarhodopsin-I photointermediate of rhodopsin by double-quantum solid-state NMR. J Biomol NMR 16:1-8.
147. Hong M, Gross JD, Griffin RG. 1997. Site-resolved determination of peptide torsion angle phi from the relative orientations of backbone N-H and C-H bonds by solid-state NMR. J Phys Chem B 101:5869-5874.
148. Costa PR, Gross JD, Hong M, Griffin RG. 1997. Solid-state NMR measurement of Psi in peptides: a NCCN 2Q-heteronuclear local field experiment. Chem Phys Lett 280(1/2):95-103.
149. Ulrich AS, Watts A, Wallat I, Heyn MP. 1994. Distorted structure of the retinal chromophore in bacteriorhodopsin resolved by 2H-NMR. Biochemistry 33:5370-5375.
150. Ulrich AS, Wallat I, Heyn MP, Watts A. 1995. Reorientation of retinal in the M-photointermediate of bacteriorhodopsin. Nat Struct Biol 2:190-192.
151. Grobner G, Choi G, Burnett IJ, Glaubitz C, Verdegem PJE, Lugtenburg J, 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 422:201-204.
152. Williamson PTF, Watts JA, Addona GH, Miller KW, Watts A. 2001. Dynamics and orientation of N+(CD3)(3)-bromoacetylcholine bound to its binding site on the nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 98:2346-2351.
153. Taylor AM, Grobner G, Williamson PTF, Watts A. 1999. Binding properties of the stilbene disulfonate sites on human erythrocyte AE1: kinetic, thermodynamic, and solid state deuterium NMR analyses. Biochemistry 38:11172-11179.
154. Glaubitz C. 2000. An introduction to MAS NMR spectroscopy on oriented membrane proteins. Concepts Magn Reson 12:137-151.
155. Grobner G, Burnett IJ, Glaubitz C, Choi G, Mason AJ, Watts A. 2000. Observations of light-induced structural changes of retinal within rhodopsin. Nature 405:810-813.
156. Creemers AFL, Kiihne S, Bovee-Geurts PHM, de Grip WJ, Lugtenburg J, de Groot HJM. 2002. 1H and 13C MAS NMR evidence for pronounced ligand-protein interactions involving the ionone ring of the retinylidene chromophore in rhodopsin. Proc Natl Acad Sci USA 99:9101-9106.
157. Williamson PTF, Verhoeven A, Miller KW, Meier BH, Watts A. 2007. Conformation of acetylcholine at its target site in the membrane embedded nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 104:18031-18036.