Protein structure determination by solid-state NMR

Topics in Current Chemistry

Volumn 326, Issue , 2012, Pages 187-214

  Zhao, Xin ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

Author keywords

ligand conformation; MAS solid state NMR; Membrane proteins; structural changes and dynamics; Structure determination

Indexed keywords

LIGAND; MEMBRANE PROTEIN;

ARTICLE; CHEMISTRY; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION;

LIGANDS; MEMBRANE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION;

EID: 84859895646     PISSN: 03401022     EISSN: None     Source Type: Book Series    
DOI: 10.1007/128_2011_287     Document Type: Article

References (193)

1. Carpenter EP, Beis K, Cameron AD et al (2008) Overcoming the challenges of membrane protein crystallography. Curr Opin Struct Biol 18: 581-586
2. Lodish H, Berk A, Kaiser CA et al (2007) Molecular cell biology, 6th edn. W.H. Freeman, New York
3. White SH (2009) Biophysical dissection of membrane proteins. Nature 459: 344-346
4. Bill RM, Henderson PJF, Iwata S et al (2011) Overcoming barriers to membrane protein structure determination. Nat Biotechnol 29: 335-340
5. Okada T, Le Trong I, Fox BA et al (2000) X-ray diffraction analysis of three-dimensional crystals of bovine rhodopsin obtained from mixed micelles. J Struct Biol 130: 73-80 (Pubitemid 30470799)
6. Salom D, Lodowski DT, Stenkamp RE et al (2006) Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc Natl Acad Sci USA 103: 16123-16128 (Pubitemid 44715162)
7. Lange A, Giller K, Hornig S et al (2006) Toxin-induced conformational changes in apotassium channel revealed by solid-state NMR. Nature 440: 959-962
8. + channel. Nat Struct Mol Biol 15: 605-612 (Pubitemid 351799137)
9. Korukottu J, Schneider R, Vijayan V et al (2008) High-resolution 3D structure determination of kaliotoxin by solid-state NMR spectroscopy. PLoS One 3: e2359
10. Zachariae U, Schneider R, Velisetty P et al (2008) The molecular mechanism of toxininduced conformational changes in a potassium channel: relation to C-type inactivation. Structure 16: 747-754 (Pubitemid 351615012)
11. Ader C, Pongs O, Becker S et al (2010) Protein dynamics detected in a membrane-embedded potassium channel using two-dimensional solid-state NMR spectroscopy. Biochim Biophys Acta 1798: 286-290
12. Crocker E, Eilers M, Ahuja S et al (2006) Location of Trp265 in metarhodopsin II: implications for the activation mechanism of the visual receptor rhodopsin. J Mol Biol 357: 163-172 (Pubitemid 43339322)
13. Struts AV, Salgado GFJ, Tanaka K et al (2007) Structural analysis and dynamics of retinal chromophore in dark and metal states of rhodopsin from H-2 NMR of aligned membranes. J Mol Biol 372: 50-66 (Pubitemid 47223214)
14. Concistreè M, Gansmüller A, McLean N et al (2008) Double-quantum 13C nuclear magnetic resonance of bathorhodopsin, the first photointermediate in mammalian vision. J Am Chem Soc 130: 10490-10491
15. Mahalingam M, Martinez-Mayorga K, Brown MF et al (2008) Two protonation switches control rhodopsin activation in membranes. Proc Natl Acad Sci USA 105: 17795-17800
16. Ahuja S, Crocker E, EilersMet al (2009) Location of the retinal chromophore in the activated state of rhodopsin. J Biol Chem 284: 10190-10201
17. Ahuja S, Eilers M, Hirshfeld A et al (2009) 6-s-cis Conformation and polar binding pocket of the retinal chromophore in the photoactivated state of rhodopsin. J Am Chem Soc 131: 15160-15169
18. Ahuja S, Hornak V, Yan ECY et al (2009) Helix movement is coupled to displacement of the second extracellular loop in rhodopsin activation. Nat Struct Mol Biol 16: 168-175
19. Ahuja S, Smith SO (2009) Multiple switches in G protein-coupled receptor activation. Trends Pharmacol Sci 30: 494-502
20. Concistreè M, Gansmüller A, McLean N et al (2009) Light penetration and photoisomerization in rhodopsin studied by numerical simulations and double-quantum solid-state NMR spectroscopy. J Am Chem Soc 131: 6133-6140
21. Gansmuller A, Concistre M, McLean N et al (2009) Towards an interpretation of 13C chemical shifts in bathorhodopsin, a functional intermediate of a G-protein coupled receptor. Biochim Biophys Acta 1788: 1350-1357
22. Goncalves JA, South K, Ahuja S et al (2010) Highly conserved tyrosine stabilizes the active state of rhodopsin. Proc Natl Acad Sci USA 107: 19861-19866
23. Hornak V, Ahuja S, Eilers M et al (2010) Light activation of rhodopsin: insights from molecular dynamics simulations guided by solid-state NMR distance restraints. J Mol Biol 396: 510-527
24. Bedford L, Lowe J, Dick LR et al (2011) Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat Rev Drug Discov 10: 29-46
25. Struts AV, Salgado GFJ, Martínez-Mayorga K et al (2011) Retinal dynamics underlie its switch from inverse agonist to agonist during rhodopsin activation. Nat Struct Mol Biol 18: 392-394
26. Ratnala VRP, Kiihne SR, Buda F et al (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 (Pubitemid 46183937)
27. Cady SD, Schmidt-Rohr K, Wang J et al (2010) Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463: 689-692
28. Hu F, Luo W, Hong M (2010) Mechanisms of proton conduction and gating in influenza M2 proton channels from solid-state NMR. Science 330: 505-508
29. Helmus JJ, Surewicz K, Nadaud PS et al (2008) Molecular conformation and dynamics of the Y145Stop variant of human prion protein. Proc Natl Acad Sci USA 105: 6284-6289 (Pubitemid 351758338)
30. Ahmed M, Davis J, Aucoin D et al (2010) Structural conversion of neurotoxic amyloid-[beta] 1-42 oligomers to fibrils. Nat Struct Mol Biol 17: 561-567
31. Kawamura I, Ikeda Y, Sudo Y et al (2007) Participation of the surface structure of Pharaonis phoborhodopsin, ppR and its A149S and A149V mutants, consisting of the C-terminal alpha-helix and E-F loop, in the complex-formation with the cognate transducer pHtrII, as revealed by site-directed C-13 solid-state NMR. Photochem Photobiol 83: 339-345 (Pubitemid 46623055)
32. Saito H, Naito A (2007) NMR studies on fully hydrated membrane proteins, with emphasis on bacteriorhodopsin as a typical and prototype membrane protein. Biochim Biophys Acta 1768: 3145-3161 (Pubitemid 350236088)
33. Pfleger N, Lorch M, Woerner AC et al (2008) Characterisation of Schiff base and chromophore in green proteorhodopsin by solid-state NMR. J Biomol NMR 40: 15-21
34. Varga K, Aslimovska L, Watts A (2008) Advances towards resonance assignments for uniformly - C-13, N-15 enriched bacteriorhodopsin at 18.8 T in purple membranes. J Biomol NMR 41: 1-4
35. Bajaj VS, Mak-Jurkauskas ML, Belenky M et al (2009) Functional and shunt states of bacteriorhodopsin resolved by 250 GHz dynamic nuclear polarization-enhanced solid-state NMR. Proc Natl Acad Sci USA 106: 9244-9249
36. Hellmich UA, Pfleger N, Glaubitz C (2009) F-19-MAS NMR on proteorhodopsin: enhanced protocol for site-specific labeling for general application to membrane proteins. Photochem Photobiol 85: 535-539
37. Shi L, Lake EMR, Ahmed MAM et al (2009) Solid-state NMR study of proteorhodopsin in the lipid environment: secondary structure and dynamics. Biochim Biophys Acta 1788: 2563-2574
38. Shi LC, Ahmed MAM, Zhang WR et al (2009) Three-dimensional solid-state NMR study of a seven-helical integral membrane proton pump-structural insights. J Mol Biol 386: 1078-1093
39. Etzkorn M, Seidel K, Li L et al (2010) Complex formation and light activation in membraneembedded sensory rhodopsin II as seen by solid-state NMR spectroscopy. Structure 18: 293-300
40. Shi L, Kawamura I, Jung K-H et al (2011) Conformation of a seven-helical transmembrane photosensor in the lipid environment. Angew Chem Int Ed 50: 1302-1305
41. Yang J, Aslimovska L, Glaubitz C (2011) Molecular dynamics of proteorhodopsin in lipid bilayers by solid-state NMR. J Am Chem Soc 133: 4874-4881
42. Wasmer C, Lange A, Van Melckebeke H et al (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319: 1523-1526 (Pubitemid 351398180)
43. Wasmer C, Benkemoun L, Sabate R et al (2009) Solid-state NMR spectroscopy reveals that E. coli inclusion bodies of HET-s(218-289) are amyloids. Angew Chem Int Ed 48: 4858-4860
44. Zamoon J, Nitu F, Karim C et al (2005) Mapping the interaction surface of a membrane protein: unveiling the conformational switch of phospholamban in calcium pump regulation. Proc Natl Acad Sci USA 102: 4747-4752 (Pubitemid 40471525)
45. Li Y, Berthold DA, Frericks HL et al (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 (Pubitemid 47183662)
46. 2+ATPasebound phospholamban in lipid bilayers by solid-state nuclear magnetic resonance (NMR) spectroscopy. Biochemistry (Mosc) 47: 4369-4376 (Pubitemid 351522085)
47. Etzkorn M, Kneuper H, Dunnwald P et al (2008) Plasticity of the PAS domain and a potential role for signal transduction in the histidine kinase DcuS. Nat Struct Mol Biol 15: 1031-1039
48. Lange V, Becker-Baldus J, Kunert B et al (2010) A MAS NMR study of the bacterial ABC transporter ArtMP. ChemBioChem 11: 547-555
49. Hiller M, Higman VA, Jehle S et al (2008) [2,3-C-13]-Labeling of aromatic residues-getting a head start in the magic-angle-spinning NMR assignment of membrane proteins. J Am Chem Soc 130: 408-409 (Pubitemid 351455532)
50. Schneider R, Etzkorn M, Giller K et al (2010) The native conformation of the human VDAC1 N terminus. Angew Chem Int Ed 49: 1882-1885
51. Baldus M (2006) Molecular interactions investigated by multi-dimensional solid-state NMR. Curr Opin Struct Biol 16: 618-623 (Pubitemid 44466405)
52. Baldus M (2006) Solid-state NMR spectroscopy: molecular structure and organization at the atomic level. Angew Chem Int Ed Engl 45: 1186-1188 (Pubitemid 44097639)
53. Hong M (2006) Oligomeric structure, dynamics, and orientation of membrane proteins from solid-state NMR. Structure 14: 1731-1740 (Pubitemid 44855624)
54. Hong M (2006) Solid-state NMR studies of the structure, dynamics, and assembly of b-sheet membrane peptides and a-helical membrane proteins with antibiotic activities. Acc Chem Res 39: 176-183
55. Baldus M (2007) ICMRBS founder's medal 2006: biological solid-state NMR, methods and applications. J Biomol NMR 39: 73-86 (Pubitemid 47249696)
56. Hong M (2007) Structure, topology, and dynamics of membrane peptides and proteins from solid-state NMR spectroscopy. J Phys Chem B 111: 10340-10351 (Pubitemid 47441837)
57. McDermott A, Polenova T (2007) Solid state NMR: new tools for insight into enzyme function. Curr Opin Struct Biol 17: 617-622 (Pubitemid 350019021)
58. Naito A, Kawamura I (2007) Solid-state NMR as a method to reveal structure and membraneinteraction of amyloidogenic proteins and peptides. Biochim Biophys Acta 1768: 1900-1912 (Pubitemid 47125853)
59. Ramamoorthy A (2007) NMR structural studies on membrane proteins. Biochim Biophys Acta 1768: 2947-2948 (Pubitemid 350236106)
60. Watts A (2007) Solid state NMR for studying membrane proteins. In: Pifat-Mrzljak G (ed) Supramolecular structure and function 9. Springer, Netherlands
61. Bockmann A (2008) 3D protein structures by solid-state NMR spectroscopy: Ready for high resolution. Angew Chem Int Ed 47: 6110-6113
62. McDermott A (2009) Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR. Annu Rev Biophys 38: 385-403
63. Ramamoorthy A (2009) Beyond NMR spectra of antimicrobial peptides: dynamical images at atomic resolution and functional insights. Solid State Nucl Magn Reson 35: 201-207
64. Brown MF, Salgado GFJ, Struts AV (2010) Retinal dynamics during light activation of rhodopsin revealed by solid-state NMR spectroscopy. Biochim Biophys Acta 1798: 177-193
65. Goncalves JA, Ahuja S, Erfani S et al (2010) Structure and function of G protein-coupled receptors using NMR spectroscopy. Prog Nucl Magn Reson Spectrosc 57: 159-180
66. Renault M, Cukkemane A, Baldus M (2010) Solid-state NMR spectroscopy on complex biomolecules. Angew Chem Int Ed 49: 8346-8357
67. Smith SO (2010) Structure and activation of the visual pigment rhodopsin. Annu Rev Biophys 39: 309-328
68. Andrew ER, Bradbury A, Eades RG (1958) Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature 182: 1659
69. Andrew ER, Bradbury A, Eades RG (1959) Removal of dipolar broadening of nuclear magnetic resonance spectra of solids by specimen rotation. Nature 183: 1802-1803
70. Lowe IJ (1959) Free induction decays of rotating solids. Phys Rev Lett 2: 285-287
71. Sinning G, Mehring M, Pines A (1976) Dynamics of spin decoupling in carbon-13-proton NMR. Chem Phys Lett 43: 382-386
72. Mehring M (1983) Principles of high resolution NMR in solids. Springer, Berlin
73. Bennett AE, Rienstra CM, Auger M et al (1995) Heteronuclear decoupling in rotating solids. J Chem Phys 103: 6951-6958
74. Eden M, Levitt MH (1999) Pulse sequence symmetries in the nuclear magnetic resonance of spinning solids: application to heteronuclear decoupling. J Chem Phys 111: 1511-1519
75. Carravetta M, Eden M, Zhao X et al (2000) Symmetry principles for the design of radiofrequency pulse sequences in the nuclear magnetic resonance of rotating solids. Chem Phys Lett 321: 205-215
76. Fung BM, Khitrin AK, Ermolaev K (2000) An improved broadband decoupling sequence for liquid crystals and solids. J Magn Reson 142: 97-101
77. Detken A, Hardy EH, Ernst M et al (2002) Simple and efficient decoupling in magic-angle spinning solid-state NMR. The XiX scheme. Chem Phys Lett 356: 298-304
78. Pines A, Gibby MG, Waugh JS (1972) Proton-enhanced nuclear induction spectroscopy. A method for high resolution NMR of dilute spins in solids. J Chem Phys 56: 1776-1777
79. Pines A, Gibby MG, Waugh JS (1973) Proton-enhanced NMR of dilute spins in solids. J Chem Phys 59: 569-590
80. Hartmann SR, Hahn EL (1962) Nuclear double resonance in the rotating frame. Phys Rev 128: 2042-2053
81. Peersen OB, Wu X, Kustanovich I et al (1993) Variable amplitude cross polarization MAS NMR. J Magn Reson 104: 334-339
82. Hediger S, Meier BH, Kurur ND et al (1994) NMR cross polarization by adiabatic passage through the Hartmann-Hahn condition (APHH). Chem Phys Lett 223: 283-288
83. Metz G, Wu X, Smith SO (1994) Ramped-amplitude cross polarization in magic angle spinning NMR. J Magn Reson A 110: 219-227
84. 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
85. Griffin RG (1998) Dipolar recoupling in MAS spectra of biological solids. Nat Struct Biol 5: 508-512
86. Gullion T (1998) Introduction to rotational-echo, double-resonance NMR. Concepts Magn Reson 10: 277-289
87. Dusold S, Sebald A (2000) Dipolar recoupling under magic-angle spinning conditions. Annu Rep NMR Spectrosc 41: 185-264
88. Levitt M (2002) Symmetry-based pulse sequences in magic-angle spinning solid-state NMR. In: Encyclopedia of nuclear magnetic resonance, vol 9. Wiley, Chichester, UK, pp 165-196
89. Helmus JJ, Nadaud PS, Hofer N et al (2008) Determination of methyl [sup 13]C-[sup 15]N dipolar couplings in peptides and proteins by three-dimensional and four-dimensional magicangle spinning solid-state NMR spectroscopy. J Chem Phys 128: 052314
90. Loquet A, Bardiaux B, Gardiennet C et al (2008) 3D structure determination of the Crh protein from highly ambiguous solid-state NMR restraints. J Am Chem Soc 130: 3579-3589 (Pubitemid 351456062)
91. Loquet A, Laage S, Gardiennet C et al (2008) Methyl proton contacts obtained using heteronuclear through-bond transfers in solid-state NMR spectroscopy. J Am Chem Soc 130: 10625-10632
92. Manolikas T, Herrmann T, Meier BH (2008) Protein structure determination from 13C spindiffusion solid-state NMR spectroscopy. J Am Chem Soc 130: 3959-3966 (Pubitemid 351429863)
93. Petkova AT, Ishii Y, Balbach JJ et al (2002) A structural model for Alzheimer's b-amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci USA 99: 16742-16747 (Pubitemid 36034043)
94. Luca S, White JF, Sohal AK et al (2003) The conformation of neurotensin bound to its G protein-coupled receptor. Proc Natl Acad Sci USA 100: 10706-10711 (Pubitemid 37140092)
95. Carravetta M, Zhao X, Johannessen OG et al (2004) Protein-induced bonding perturbation of the rhodopsin chromophore detected by double-quantum solid-state NMR. J Am Chem Soc 126: 3948-3953 (Pubitemid 38391887)
96. Petkova AT, Leapman RD, Guo ZH et al (2005) Self-propagating,molecular- level polymorphism in Alzheimer's b-amyloid fibrils. Science 307: 262-265 (Pubitemid 40116242)
97. Mani R, Cady SD, Tang M et al (2006) Membrane-dependent oligomeric structure and pore formation of a b-hairpin antimicrobial peptide in lipid bilayers from solid-state NMR. Proc Natl Acad Sci USA 103: 16242-16247 (Pubitemid 44715181)
98. Tang M, Waring AJ, Lehrer RL et al (2008) Effects of guanidinium- phosphate hydrogen bonding on the membrane-bound structure and activity of an arginine-rich membrane peptide from solid-state NMR spectroscopy. Angew Chem Int Ed 47: 3202-3205
99. Song C, Tapaneeyakorn S, Murphy AC et al (2009) Enantioselective syntheses of a-Fmoc- Pbf-[2-13C]-l-arginine and Fmoc-[1,3-13C2]-l-proline and incorporation into the neurotensin receptor 1 lLigand, NT8-13. J Org Chem 74: 8980-8987
100. Castellani F, van Rossum B, Diehl A et al (2002) Structure of a protein determined by solidstate magic-angle-spinning NMR spectroscopy. Nature 420: 98-102 (Pubitemid 35291447)
101. Higman V, Flinders J, HillerMet al (2009) Assigning large proteins in the solid state: a MAS NMR resonance assignment strategy using selectively and extensively 13C-labelled proteins. J Biomol NMR 44: 245-260
102. Eilers M, Ying WW, Reeves PJ et al (2002) Magic angle spinning nuclear magnetic resonance of isotopically labeled rhodopsin. Methods Enzymol 343: 212-222 (Pubitemid 32954144)
103. Patel AB, Crocker E, Eilers M et al (2004) Coupling of retinal isomerization to the activation of rhodopsin. Proc Natl Acad Sci USA 101: 10048-10053 (Pubitemid 38891192)
104. Patel AB, Crocker E, Reeves PJ et al (2005) Changes in interhelical hydrogen bonding upon rhodopsin activation. J Mol Biol 347: 803-812 (Pubitemid 40357921)
105. Etzkorn M, Martell S, Andronesi OC et al (2007) Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angew Chem Int Ed Engl 46: 459-462 106.
106. Schneider R, Ader C, Lange A et al (2008) Solid-state NMR spectroscopy applied to a chimeric potassium channel in lipid bilayers. J Am Chem Soc 130: 7427-7435 (Pubitemid 351813236)
107. Hong M, Jakes K (1999) Selective and extensive C-13 labeling of a membrane protein for solid-state NMR investigations. J Biomol NMR 14: 71-74 (Pubitemid 29258287)
108. Igumenova TI, McDermott AE, Zilm KW et al (2004) Assignments of carbon NMR resonances for microcrystalline ubiquitin. J Am Chem Soc 126: 6720-6727 (Pubitemid 38697371)
109. 13C chemical shift assignments and conformational analysis. J Am Chem Soc 127: 12291-12305 (Pubitemid 41279253)
110. Heise H, Seidel K, Etzkorn M et al (2005) 3D NMR spectroscopy for resonance assignment and structure elucidation of proteins under MAS: novel pulse schemes and sensitivity considerations. J Magn Reson 173: 64-74 (Pubitemid 40206418)
111. Franks W, Kloepper K, Wylie B et al (2007) Four-dimensional heteronuclear correlation experiments for chemical shift assignment of solid proteins. J Biomol NMR 39: 107-131 (Pubitemid 47377484)
112. Huang L, McDermott AE (2008) Partial site-specific assignment of a uniformly C-13, N-15 enriched membrane protein, light-harvesting complex 1 (LH1), by solid state NMR. Biochim Biophys Acta 1777: 1098-1108
113. Li Y, Berthold DA, Gennis RB et al (2008) Chemical shift assignment of the transmembrane helices of DsbB, a 20-kDa integral membrane enzyme, by 3D magic-angle spinning NMR spectroscopy. Protein Sci 17: 199-204 (Pubitemid 351171832)
114. Shi L, Traaseth NJ, Verardi R et al (2009) 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: 195-205
115. Morcombe CR, Gaponenko V, Byrd RA et al (2005) 13C CPMAS spectroscopy of deuterated proteins: CP dynamics, line shapes, and T1 relaxation. J Am Chem Soc 127: 397-404 (Pubitemid 40094401)
116. Lesage A, Emsley L, Penin F et al (2006) Investigation of dipolar-mediated water-protein interactions in microcrystalline Crh by solid-state NMR spectroscopy. J Am Chem Soc 128: 8246-8255 (Pubitemid 43967769)
117. Akbey Ü, Lange S, Trent Franks W et al (2010) Optimum levels of exchangeable protons in perdeuterated proteins for proton detection in MAS solid-state NMR spectroscopy. J Biomol NMR 46: 67-73
118. Zhou Donghua H, Shea John J, Nieuwkoop Andrew J et al (2007) Solid-state proteinstructure determination with proton-detected triple-resonance 3D magic-angle-spinning NMR spectroscopy. Angew Chem Int Ed 46: 8380-8383
119. Varga K, Ashmovska L, Parrot I et al (2007) NMR crystallography: the effect of deuteration on high resolution C-13 solid state NMR spectra of a 7-TM protein. Biochim Biophys Acta 1768: 3029-3035 (Pubitemid 350236099)
120. Tapaneeyakorn S, Goddard AD, Oates J et al (2011) Solution- and solid-state NMR studies of GPCRs and their ligands. Biochim Biophys Acta 1808: 1462-1475
121. Cross TA, Sharma M, YiMet al (2011) Influence of solubilizing environments on membrane protein structures. Trends Biochem Sci 36: 117-125
122. Pauli J, van Rossum B, Forster H et al (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
123. Igumenova TI, Wand AJ, McDermott AE (2004) Assignment of the backbone resonances for microcrystalline ubiquitin. J Am Chem Soc 126: 5323-5331 (Pubitemid 38509487)
124. Kijac AZ, Li Y, Sligar SG et al (2007) Magic-angle spinning solid-state NMR spectroscopy of nanodisc-embedded human CYP3A4. Biochemistry (Mosc) 46: 13696-13703 (Pubitemid 350223897)
125. Lange A, Luca S, Baldus M (2002) Structural constraints from proton-mediated rare-spin correlation spectroscopy in rotating solids. J Am Chem Soc 124: 9704-9705
126. Lange A, Becker S, Seidel K et al (2005) A concept for rapid protein-structure determination by solid-state NMR spectroscopy. Angew Chem Int Ed 44: 2089-2092
127. Suter D, Ernst RR (1985) Spin diffusion in resolved solid-state NMR spectra. Phys Rev B 32: 5608-5627
128. Lundstrom K (2007) Structural genomics and drug discovery. J Cell Mol Med 11: 224-238
129. Palczewski K, Kumasaka T, Hori T et al (2000) Crystal structure of rhodopsin: a G proteincoupled receptor. Science 289: 739-745 (Pubitemid 30650186)
130. Cherezov V, Rosenbaum DM, Hanson MA et al (2007) High-resolution crystal structure of an engineered human beta(2)-adrenergic G protein-coupled receptor. Science 318: 1258-1265 (Pubitemid 350172884)
131. Rosenbaum DM, Cherezov V, Hanson MA et al (2007) GPCR engineering yields highresolution structural insights into beta2-adrenergic receptor function. Science 318: 1266-1273 (Pubitemid 350172885)
132. Murakami M, Kouyama T (2008) Crystal structure of squid rhodopsin. Nature 453: 363-367 (Pubitemid 351693128)
133. Park JH, Scheerer P, Hofmann KP et al (2008) Crystal structure of the ligand-free G-proteincoupled receptor opsin. Nature 454: 183-187 (Pubitemid 351969893)
134. Scheerer P, Park JH, Hildebrand PW et al (2008) Crystal structure of opsin in its G-proteininteracting conformation. Nature 455: 497-502
135. Warne T, Serrano-Vega MJ, Baker JG et al (2008) Structure of a beta1-adrenergic G-proteincoupled receptor. Nature 454: 486-492
136. Chien EYT, Liu W, Zhao Q et al (2010) Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist. Science 330: 1091-1095
137. Wu B, Chien EYT, Mol CD et al (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330: 1066-1071
138. Rasmussen SGF, Choi H-J, Fung JJ et al (2011) Structure of a nanobody-stabilized active state of the b2 adrenoceptor. Nature 469: 175-180
139. Rosenbaum DM, Zhang C, Lyons JA et al (2011) Structure and function of an irreversible agonist-b2 adrenoceptor complex. Nature 469: 236-240
140. Warne T, Moukhametzianov R, Baker JG et al (2011) The structural basis for agonist and partial agonist action on a b1-adrenergic receptor. Nature 469: 241-244
141. Xu F, Wu H, Katritch V et al (2011) Structure of an agonist-bound human A2A adenosine receptor. Science 332: 322-327
142. Creemers AFL, Bovee-Geurts PHM, DeGrip WJ et al (2004) Solid-state NMR analysis of ligand-receptor interactions reveals an induced misfit in the binding site of isorhodopsin. Biochemistry (Mosc) 43: 16011-16018
143. van Gammeren AJ, Hulsbergen FB, Hollander JG et al (2004) Biosynthetic site-specific C-13 labeling of the light-harvesting 2 protein complex: a model for solid state NMR structure determination of transmembrane proteins. J Biomol NMR 30: 267-274 (Pubitemid 40069141)
144. Higman V, Rösner H, Ugolini R et al (2009) Probing the urea dependence of residual structure in denatured human a-lactalbumin. J Biomol NMR 45: 121-131
145. Smith SO, Courtin J, de Groot H et al (1991) 13C magic-angle spinning NMR studies of bathorhodopsin, the primary photoproduct of rhodopsin. Biochemistry (Mosc) 30: 7409-7415
146. Verdegem PJE, Bovee-Geurts PHM, De Grip WJ et al (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 (Mosc) 38: 11316-11324
147. Verhoeven MA, Creemers AFL, Bovee-Geurts PHM et al (2001) Ultra-high-field MAS NMR assay of a multispin labeled ligand bound to its G-protein receptor target in the natural membrane environment: electronic structure of the retinylidene chromophore in rhodopsin. Biochemistry (Mosc) 40: 3282-3288 (Pubitemid 32221629)
148. 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 (Pubitemid 34764573)
149. Spooner PJR, Sharples JM, Verhoeven MA et al (2002) Relative orientation between the b-ionone ring and the polyene chain for the chromophore of rhodopsin in native membranes. Biochemistry (Mosc) 41: 7549-7555 (Pubitemid 34627781)
150. Spooner PJR, Sharples JM, Goodall SC et al (2003) Conformational similarities in the b-ionone ring region of the rhodopsin chromophore in its ground state and after photoactivation to the metarhodopsin-I intermediate. Biochemistry (Mosc) 42: 13371-13378 (Pubitemid 37444885)
151. Spooner PJR, Sharples JM, Goodall SC et al (2004) The ring of the rhodopsin chromophore in a hydrophobic activation switch within the binding pocket. J Mol Biol 343: 719-730 (Pubitemid 39311617)
152. Lopez JJ, Shukla AK, Reinhart C et al (2008) The structure of the neuropeptide bradykinin bound to the human G-protein coupled receptor bradykinin B2 as determined by solid-state NMR spectroscopy. Angew Chem Int Ed 47: 1668-1671
153. Tikhonova IG, Costanzi S (2009) Unraveling the structure and function of G protein-coupled receptors through NMR spectroscopy. Curr Pharm Des 15: 4003-4016
154. Takegoshi K, Nakamura S, Terao T (2001) 13C-1H dipolar-assisted rotational resonance in magic-angle spinning NMR. Chem Phys Lett 344: 631-637 (Pubitemid 33628408)
155. Ambrosio M, Zürn A, Lohse MJ (2011) Sensing G protein-coupled receptor activation. Neuropharmacology 60: 45-51
156. Smock RG, Gierasch LM (2009) Sending signals dynamically. Science 324: 198-203
157. Saito H, Kawase Y, Kira A et al (2007) Surface and dynamic structures of bacteriorhodopsin in a 2D crystal, a distorted or disrupted lattice, as revealed by site-directed solid-state 13C NMR. Photochem Photobiol 83: 253-262 (Pubitemid 46623063)
158. Brown MF, Martinez-Mayorga K, Nakanishi K et al (2009) Retinal conformation and dynamics in activation of rhodopsin illuminated by solid-state H-2 NMR spectroscopy. Photochem Photobiol 85: 442-453
159. Hurley JH, Misra S (2000) Signaling and subcellular targeting by membrane-binding domains. Annu Rev Biophys Biomol Struct 29: 49-79 (Pubitemid 30599588)
160. Tossi A, Sandri L, Giangaspero A (2000) Amphipathic, alpha-helical antimicrobial peptides. Biopolymers 55: 4-30
161. Tamm LK, Han X, Li YL et al (2002) Structure and function of membrane fusion peptides. Biopolymers 66: 249-260 (Pubitemid 36098317)
162. Richard JP, Melikov K, Vives E et al (2003) Cell-penetrating peptides - a reevaluation of the mechanism of cellular uptake. J Biol Chem 278: 585-590 (Pubitemid 36043612)
163. Zimmerberg J, McLaughlin S (2004) Membrane curvature: how BAR domains bend bilayers. Curr Biol 14: R250-R252 (Pubitemid 38431278)
164. Cho WH, Stahelin RV (2005) Membrane-protein interactions in cell signaling and membrane trafficking. Annu Rev Biophys Biomol Struct 34: 119-151 (Pubitemid 40847721)
165. Hong H, Park S, FloresJimenez RH et al (2007) Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins. J Am Chem Soc 129: 8320-8327 (Pubitemid 47035142)
166. Oldfield E, Bowers JL, Forbes J (1987) High-resolution proton and carbon-13 NMR of membranes: why sonicate? Biochemistry 26: 6919-6923
167. Jeener J, Meier BH, Bachmann P et al (1979) Investigation of exchange processes by twodimensional NMR spectroscopy. J Chem Phys 71: 4546-4553
168. 1H nuclear magnetic resonance of a transmembrane peptide. Biophys J 69: 1917-1932
169. Huster D, Kuhn K, Kadereit D et al (2001) H-1 high-resolution magic angle spinning NMR spectroscopy for the investigation of a Ras lipopeptide in a lipid membrane. Angew Chem Int Ed Engl 40: 1056-1058
170. Zhang W, Crocker E, McLaughlin S et al (2003) Binding of peptides with
171. Sprang SR (2011) Cell signalling: binding the receptor at both ends. Nature 469: 172-173
172. Abragam A, Goldman M (1978) Principles of dynamic nuclear polarisation. Rep Prog Phys 41: 395
173. Bajaj VS, Farrar CT, Hornstein MK et al (2003) Dynamic nuclear polarization at 9 T using a novel 250 GHz gyrotron microwave source. J Magn Reson 160: 85-90
174. Zysmilich MG, McDermott A (1994) Photochemically induced dynamic nuclear polarization in the solid-state 15N spectra of reaction centers from photosynthetic bacteria Rhodobacter sphaeroides R-26. J Am Chem Soc 116: 8362-8363
175. Bargon J (2006) The inter-relationship between triplet energies and spin chemistry. Photochem Photobiol Sci 5: 970-978 (Pubitemid 44526276)
176. Daviso E, Diller A, Alia A et al (2008) Photo-CIDNP MAS NMR beyond the T-1 limit by fast cycles of polarization extinction and polarization generation. J Magn Reson 190: 43-51 (Pubitemid 350235249)
177. Raftery D (2006) Xenon NMR spectroscopy. In: Webb GA (ed) Annual reports on NMR spectroscopy. Vol 57, Acadamic Press, Salt Lake City, USA, pp. 205-270 (Pubitemid 43588429)
178. Ruset IC, Ketel S, Hersman FW (2006) Optical pumping system design for large production of hyperpolarized. Phys Rev Lett 96: 053002
179. Bajaj VS, Hornstein MK, Kreischer KE et al (2007) 250 GHz CW gyrotron oscillator for dynamic nuclear polarization in biological solid state NMR. J Magn Reson 189: 251-279 (Pubitemid 350051986)
180. Mak-Jurkauskas ML, Bajaj VS, Hornstein MK et al (2008) Energy transformations early in the bacteriorhodopsin photocycle revealed by DNP-enhanced solid-state NMR. Proc Natl Acad Sci USA 105: 883-888 (Pubitemid 351282050)
181. 1H T1 relaxation. J Magn Reson 184: 350-356 (Pubitemid 46177670)
182. Wickramasinghe NP, Parthasarathy S, Jones CR et al (2009) Nanomole-scale protein solidstate NMR by breaking intrinsic 1HT1 boundaries. Nat Methods 6: 215-218
183. Cavalli A, Salvatella X, Dobson CM et al (2007) Protein structure determination from NMR chemical shifts. Proc Natl Acad Sci USA 104: 9615-9620 (Pubitemid 47175315)
184. Shen Y, Bax A (2010) Prediction of Xaa-Pro peptide bond conformation from sequence and chemical shifts. J Biomol NMR 46: 199-204
185. Wishart DS, Arndt D, Berjanskii M et al (2008) CS23D: a web server for rapid protein structure generation using NMR chemical shifts and sequence data. Nucleic Acids Res 36: W496-W502
186. Robustelli P, Cavalli A, Vendruscolo M (2008) Determination of protein structures in the solid state from NMR chemical shifts. Structure 16: 1764-1769
187. Shen Y, Vernon R, Baker D et al (2009) De novo protein structure generation from incomplete chemical shift assignments. J Biomol NMR 43: 63-78
188. Li J, Edwards PC, Burghammer M et al (2004) Structure of bovine rhodopsin in a trigonal crystal form. J Mol Biol 343: 1409-1438 (Pubitemid 39387834)
189. Levitt MH, Oas TG, Griffin RG (1988) Rotary resonance recoupling in heteronuclear spin pair systems. Isr J Chem 28: 271-282
190. Oas TG, Griffin RG, Levitt MH (1988) Rotary resonance recoupling of dipolar interactions in solid-state nuclear magnetic resonance spectroscopy. J Chem Phys 89: 692-695
191. Szeverenyi NM, Sullivan MJ, Maciel GE (1982) Observation of spin exchange by twodimensional fourier transform 13C cross polarization-magic-angle spinning. J Magn Reson 47: 462-475
192. Suter D, Ernst RR (1982) Spectral spin diffusion in the presence of an extraneous dipolar reservoir. Phys Rev B 25: 6038-6041
193. Cornilescu G, Delaglio F, and Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289-302 (Pubitemid 29143535)