Solution NMR study of the transmembrane domain of single-span membrane proteins: Opportunities and strategies

Current Protein and Peptide Science

Volumn 13, Issue 6, 2012, Pages 585-600

  Gayen, Shovanlal ^a   Li, Qingxin ^b   Kang, Congbao ^a  

^a Agency for Science   (Singapore)

^b INSTITUTE OF CHEMICAL AND ENGINEERING SCIENCES   (Singapore)

Author keywords

Membrane protein; NMR spectroscopy; Protein protein interaction; Single span membrane protein; Structure determination

Indexed keywords

ARGININE; BETA3 INTEGRIN; CD4 ANTIGEN; CELL ADHESION MOLECULE; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GLYCOPHORIN A; GLYCOPROTEIN GP 41; HETERODIMER; HOMODIMER; INTEGRIN; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; MEMBRANE PROTEIN; ORGANIC SOLVENT; PHOSPHOLAMBAN; POTASSIUM CHANNEL KCNE1; POTASSIUM CHANNEL KCNQ1; PROTEIN BNIP3; PROTEIN M2; PROTEIN TYROSINE KINASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA;

DRUG TARGETING; MICELLE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVERSE MICELLE; REVIEW; X RAY CRYSTALLOGRAPHY;

CELL MEMBRANE; HUMANS; MEMBRANE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, TERTIARY; SOLUTIONS;

EID: 84870175479     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/138920312803582979     Document Type: Review

References (168)

1. Fagerberg, L.; Jonasson, K.; von Heijne, G.; Uhlen, M.; Berglund, L.; Prediction of the human membrane proteome. Proteomics, 2010, 10 (6), 1141-1149.
2. Arinaminpathy, Y.; Khurana, E.; Engelman, D.M.; Gerstein, M.B.; Computational analysis of membrane proteins: the largest class of drug targets. Drug Discov Today, 2009, 14 (23-24), 1130-1135.
3. Overington, J.P.; Al-Lazikani, B.; Hopkins, A.L.; How many drug targets are there? Nat. Rev. Drug Discov., 2006, 5 (12), 993-996.
4. Kim, H.J.; Howell, S.C.; Van Horn, W.D.; Jeon, Y.H.; Sanders, C.R.; Recent Advances in the Application of Solution NMR Spectroscopy to Multi-Span Integral Membrane Proteins. Prog. Nucl. Magn. Reson. Spectrosc., 2009, 55 (4), 335-360.
5. Van Horn, W.D.; Kim, H.J.; Ellis, C.D.; Hadziselimovic, A.; Sulistijo, E.S.; Karra, M.D.; Tian, C.; Sonnichsen, F.D.; Sanders, C.R.; Solution nuclear magnetic resonance structure of membrane- integral diacylglycerol kinase. Science, 2009, 324 (5935), 1726-1729.
6. Gautier, A.; Mott, H.R.; Bostock, M.J.; Kirkpatrick, J.P.; Nietlispach, D.; Structure determination of the seven-helix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat. Struct. Mol. Biol., 2010, 17 (6), 768-774.
7. Hiller, S.; Garces, R.G.; Malia, T.J.; Orekhov, V.Y.; Colombini, M.; Wagner, G.; Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science, 2008, 321 (5893), 1206-1210.
8. Wang, G.; Determination of solution structure and lipid micelle location of an engineered membrane peptide by using one NMR experiment and one sample. Biochim. Biophys. Acta, 2007, 1768 (12), 3271-3281.
9. Wang, G.; NMR of membrane-associated peptides and proteins. Curr. Protein Pept. Sci., 2008, 9 (1), 50-69.
10. Fernandez, C.; Wuthrich, K.; NMR solution structure determination of membrane proteins reconstituted in detergent micelles. FEBS Lett., 2003, 555 (1), 144-150.
11. Patching, S.G.; NMR structures of polytopic integral membrane proteins. Mol. Membr. Biol., 2011, 28 (6), 370-397.
12. Liang, B.; Tamm, L.K.; Structure of outer membrane protein G by solution NMR spectroscopy. Proc. Natl. Acad. Sci. U. S. A., 2007, 104 (41), 16140-16145.
13. Park, S.H.; Berkamp, S.; Cook, G.A.; Chan, M.K.; Viadiu, H.; Opella, S.J.; Nanodiscs versus Macrodiscs for NMR of Membrane Proteins. Biochemistry, 2011, 50 (42), 8983-8985.
14. Opella, S.J.; Marassi, F.M.; Structure determination of membrane proteins by NMR spectroscopy. Chem. Rev., 2004, 104 (8), 3587-3606.
15. Liang, B.; Tamm, L.K.; NMR of membrane proteins in solution. Prog. Nucl. Magn. Reson., 2006, 48, 201-210.
16. Marassi, F.M.; Opella, S.J.; NMR structural studies of membrane proteins. Curr. Opin. Struct. Biol., 1998, 8 (5), 640-648.
17. Hubert, P.; Sawma, P.; Duneau, J.P.; Khao, J.; Henin, J.; Bagnard, D.; Sturgis, J.; Single-spanning transmembrane domains in cell growth and cell-cell interactions: More than meets the eye? Cell Adh. Migr., 2010, 4 (2), 313-324.
18. Almen, M.S.; Nordstrom, K.J.; Fredriksson, R.; Schioth, H.B.; Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin. BMC Biol., 2009, 7, 50.
19. Lemmon, M.A.; Schlessinger, J.; Cell signaling by receptor tyrosine kinases. Cell, 2010, 141 (7), 1117-1134.
20. Takeuchi, K.; Ito, F.; Receptor tyrosine kinases and targeted cancer therapeutics. Biol. Pharm. Bull., 2011, 34 (12), 1774-1780.
21. Kelleher, D.J.; Gilmore, R.; An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology, 2006, 16 (4), 47R-62R.
22. Vleugels, W.; Schollen, E.; Foulquier, F.; Matthijs, G.; Screening for OST deficiencies in unsolved CDG-I patients. Biochem. Biophys. Res. Commun., 2009, 390 (3), 769-774.
23. Pongs, O.; Schwarz, J.R.; Ancillary subunits associated with voltage-dependent K+ channels. Physiol. Rev., 2010, 90 (2), 755-796.
24. Takumi, T.; Ohkubo, H.; Nakanishi, S.; Cloning of a membrane protein that induces a slow voltage-gated potassium current. Science, 1988, 242 (4881), 1042-1045.
25. Barhanin, J.; Lesage, F.; Guillemare, E.; Fink, M.; Lazdunski, M.; Romey, G.; K(V)LQT1 and lsK (minK) proteins associate to form the I(Ks) cardiac potassium current. Nature, 1996, 384 (6604), 78-80.
26. Osteen, J.D.; Gonzalez, C.; Sampson, K.J.; Iyer, V.; Rebolledo, S.; Larsson, H.P.; Kass, R.S.; KCNE1 alters the voltage sensor movements necessary to open the KCNQ1 channel gate. Proc. Natl. Acad. Sci. U. S. A., 2010, 107 (52), 22710-22715.
27. Tyson, J.; Tranebjaerg, L.; Bellman, S.; Wren, C.; Taylor, J.F.; Bathen, J.; Aslaksen, B.; Sorland, S.J.; Lund, O.; Malcolm, S.; Pembrey, M.; Bhattacharya, S.; Bitner-Glindzicz, M.; IsK and KvLQT1: mutation in either of the two subunits of the slow component of the delayed rectifier potassium channel can cause Jervell and Lange-Nielsen syndrome. Hum. Mol. Genet., 1997, 6 (12), 2179-2185.
28. Hynes, R.O.; Integrins: a family of cell surface receptors. Cell, 1987, 48 (4), 549-554.
29. Hynes, R.O. Integrins: bidirectional, allosteric signaling machines. Cell, 2002, 110 (6), 673-687.
30. Kuijpers, T.W.; Van Lier, R.A.; Hamann, D.; de Boer, M.; Thung, L.Y.; Weening, R.S.; Verhoeven, A.J.; Roos, D.; Leukocyte adhesion deficiency type 1 (LAD-1)/variant. A novel immunodeficiency syndrome characterized by dysfunctional beta2 integrins. J. Clin. Invest., 1997, 100 (7), 1725-1733.
31. Tan S M, L.A.; INTEGRINS: THE DYNAMIC CELL ADHESION MOLECULES. Biomol. front., 2006.
32. Heckmann, D.; Kessler, H.; Design and chemical synthesis of integrin ligands. Methods Enzymol., 2007, 426, 463-503.
33. Hynes, R.O.; Cell-matrix adhesion in vascular development. J Thromb. Haemost., 2007, 5 Suppl 1, 32-40.
34. Xu, L.; Hynes, R.O.; GPR56 and TG2: possible roles in suppression of tumor growth by the microenvironment. Cell Cycle, 2007, 6 (2), 160-165.
35. Takada, Y.; Ye, X.; Simon, S.; The integrins. Genome Biol., 2007, 8 (5), 215.
36. Kang, C.; Tian, C.; Sonnichsen, F.D.; Smith, J.A.; Meiler, J.; George, A.L.; Jr.; Vanoye, C.G.; Kim, H.J.; Sanders, C.R.; Structure of KCNE1 and Implications for How It Modulates the KCNQ1 Potassium Channel. Biochemistry, 2008, 47(31), 7999-8006.
37. Lau, T.L.; Partridge, A.W.; Ginsberg, M.H.; Ulmer, T.S.; Structure of the integrin beta3 transmembrane segment in phospholipid bicelles and detergent micelles. Biochemistry, 2008, 47 (13), 4008-4016.
38. Kim, C.; Schmidt, T.; Cho, E.G.; Ye, F.; Ulmer, T.S.; Ginsberg, M.H.; Basic amino-acid side chains regulate transmembrane integrin signalling. Nature, 2012, 481 (7380), 209-213.
39. Barrett, P.J.; Song, Y.; Van Horn, W.D.; Hustedt, E.J.; Schafer, J.M.; Hadziselimovic, A.; Beel, A.J.; Sanders, C.R.; The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science, 2012, 336 (6085), 1168-1171.
40. MacKenzie, K.R.; Prestegard, J.H.; Engelman, D.M.; A transmembrane helix dimer: structure and implications. Science, 1997, 276 (5309), 131-133.
41. Bocharov, E.V.; Mineev, K.S.; Volynsky, P.E.; Ermolyuk, Y.S.; Tkach, E.N.; Sobol, A.G.; Chupin, V.V.; Kirpichnikov, M.P.; Efremov, R.G.; Arseniev, A.S.; Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state. J. Biol. Chem., 2008, 283 (11), 6950-6956.
42. Bocharov, E.V.; Mayzel, M.L.; Volynsky, P.E.; Mineev, K.S.; Tkach, E.N.; Ermolyuk, Y.S.; Schulga, A.A.; Efremov, R.G.; Arseniev, A.S.; Left-handed dimer of EphA2 transmembrane domain: Helix packing diversity among receptor tyrosine kinases. Biophys J., 2010, 98 (5), 881-889.
43. Bocharov, E.V.; Mayzel, M.L.; Volynsky, P.E.; Goncharuk, M.V.; Ermolyuk, Y.S.; Schulga, A.A.; Artemenko, E.O.; Efremov, R.G.; Arseniev, A.S.; Spatial structure and pH-dependent conformational diversity of dimeric transmembrane domain of the receptor tyrosine kinase EphA1. J. Biol. Chem., 2008, 283 (43), 29385-29395.
44. Bocharov, E.V.; Mineev, K.S.; Goncharuk, M.V.; Arseniev, A.S.; Structural and thermodynamic insight into the process of weak dimerization of the ErbB4 transmembrane domain by solution NMR. Biochim. Biophys. Acta, 2012, 1818(9), 2158-2170.
45. Call, M.E.; Schnell, J.R.; Xu, C.; Lutz, R.A.; Chou, J.J.; Wucherpfennig, K.W.; The structure of the zetazeta transmembrane dimer reveals features essential for its assembly with the T cell receptor. Cell, 2006, 127 (2), 355-368.
46. Bocharov, E.V.; Pustovalova, Y.E.; Pavlov, K.V.; Volynsky, P.E.; Goncharuk, M.V.; Ermolyuk, Y.S.; Karpunin, D.V.; Schulga, A.A.; Kirpichnikov, M.P.; Efremov, R.G.; Maslennikov, I.V.; Arseniev, A.S.; Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger. J. Biol. Chem., 2007, 282 (22), 16256-16266.
47. Sulistijo, E.S.; Mackenzie, K.R.; Structural basis for dimerization of the BNIP3 transmembrane domain. Biochemistry, 2009, 48 (23), 5106-5120.
48. Nadezhdin, K.D.; Bocharova, O.V.; Bocharov, E.V.; Arseniev, A.S.; Dimeric structure of transmembrane domain of amyloid precursor protein in micellar environment. FEBS Lett., 2012.
49. Lau, T.L.; Kim, C.; Ginsberg, M.H.; Ulmer, T.S.; The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling. Embo J, 2009, 28 (9), 1351-1361.
50. Yang, J.; Ma, Y.Q.; Page, R.C.; Misra, S.; Plow, E.F.; Qin, J.; Structure of an integrin alphaIIb beta3 transmembrane-cytoplasmic heterocomplex provides insight into integrin activation. Proc. Natl. Acad. Sci. U. S. A., 2009, 106 (42), 17729-17734.
51. Zhu, J.; Luo, B.H.; Barth, P.; Schonbrun, J.; Baker, D.; Springer, T.A.; The structure of a receptor with two associating transmembrane domains on the cell surface: integrin alphaIIbbeta3. Mol. Cell, 2009, 34 (2), 234-249.
52. Mineev, K.S.; Bocharov, E.V.; Pustovalova, Y.E.; Bocharova, O.V.; Chupin, V.V.; Arseniev, A.S.; Spatial structure of the transmembrane domain heterodimer of ErbB1 and ErbB2 receptor tyrosine kinases. J Mol. Biol., 2010, 400 (2), 231-243.
53. Call, M.E.; Wucherpfennig, K.W.; Chou, J.J.; The structural basis for intramembrane assembly of an activating immunoreceptor complex. Nat. Immunol., 2010, 11 (11), 1023-1029.
54. Oxenoid, K.; Chou, J.J.; The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proc. Natl. Acad. Sci. U. S. A., 2005, 102 (31), 10870-10875.
55. Schnell, J.R.; Chou, J.J.; Structure and mechanism of the M2 proton channel of influenza A virus. Nature, 2008, 451 (7178), 591-595.
56. Pielak, R.M.; Chou, J.J.; Kinetic analysis of the M2 proton conduction of the influenza virus. J. Am. Chem. Soc., 2010, 132 (50), 17695-17697.
57. Pielak, R.M.; Schnell, J.R.; Chou, J.J.; Mechanism of drug inhibition and drug resistance of influenza A M2 channel. Proc. Natl. Acad. Sci. U. S. A., 2009, 106 (18), 7379-7384.
58. Pielak, R.M.; Chou, J.J.; Influenza M2 proton channels. Biochim. Biophys. Acta, 2011, 1808 (2), 522-529.
59. Wang, J.; Pielak, R.M.; McClintock, M.A.; Chou, J.J.; Solution structure and functional analysis of the influenza B proton channel. Nat. Struct. Mol. Biol., 2009, 16 (12), 1267-1271.
60. Call, M.E.; Chou, J.J.; A view into the blind spot: solution NMR provides new insights into signal transduction across the lipid bilayer. Structure, 2010, 18 (12), 1559-1569.
61. Melnyk, R.A.; Partridge, A.W.; Yip, J.; Wu, Y.; Goto, N.K.; Deber, C.M.; Polar residue tagging of transmembrane peptides. Biopolymers, 2003, 71 (6), 675-685.
62. Itaya, M.; Brett, I.C.; Smith, S.O.; Synthesis, purification, and characterization of single helix membrane peptides and proteins for NMR spectroscopy. Methods Mol. Biol., 2012, 831, 333-357.
63. Isaksson, L.; Enberg, J.; Neutze, R.; Goran Karlsson, B.; Pedersen, A.; Expression screening of membrane proteins with cell-free protein synthesis. Protein Expr. Purif., 2012, 82 (1), 218-225.
64. Pedersen, A.; Hellberg, K.; Enberg, J.; Karlsson, B.G.; Rational improvement of cell-free protein synthesis. Nat. Biotechnol., 2011, 28 (3), 218-224.
65. Li, Q.; Shuyi Chen, A.; Gayen, S.; Kang, C.; Expression and purification of the p75 neurotrophin receptor transmembrane domain using a ketosteroid isomerase tag. Microb. Cell Fact., 2012, 11 (1), 45.
66. Page, R.C.; Moore, J.D.; Nguyen, H.B.; Sharma, M.; Chase, R.; Gao, F.P.; Mobley, C.K.; Sanders, C.R.; Ma, L.; Sonnichsen, F.D.; Lee, S.; Howell, S.C.; Opella, S.J.; Cross, T.A.; Comprehensive evaluation of solution nuclear magnetic resonance spectroscopy sample preparation for helical integral membrane proteins. J. Struct. Funct. Genomics, 2006, 7 (1), 51-64.
67. Kang, C.; Li, Q.; Solution NMR study of integral membrane proteins. Curr. Opin. Chem. Biol., 2011, 15 (4), 560-569.
68. Cross, T.A.; Sharma, M.; Yi, M.; Zhou, H.X.; Influence of solubilizing environments on membrane protein structures. Trends Biochem. Sci., 2011, 36 (2), 117-125.
69. Arnold, T.; Linke, D.; Phase separation in the isolation and purification of membrane proteins. Biotechniques, 2007, 43 (4), 427-430.
70. Arnold, T.; Linke, D.; The use of detergents to purify membrane proteins. Curr. Protoc. Protein Sci., 2008, 8, 1-4.
71. Vinogradova, O.; Sonnichsen, F.; Sanders, C.R.; 2nd, On choosing a detergent for solution NMR studies of membrane proteins. J. Biomol. NMR., 1998, 11 (4), 381-386.
72. Sanders, C.R.; Sonnichsen, F.; Solution NMR of membrane proteins: practice and challenges. Magn. Reson. Chem., 2006, 44, S24-40.
73. Sanders, C.R.; Oxenoid, K.; Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins. Biochim. Biophys. Acta, 2000, 1508 (1-2), 129-145.
74. Tian, C.; Vanoye, C.G.; Kang, C.; Welch, R.C.; Kim, H.J.; George, A.L.; Jr.; Sanders, C.R.; Preparation, Functional Characterization, and NMR Studies of Human KCNE1, a Voltage-Gated Potassium Channel Accessory Subunit Associated with Deafness and Long QT Syndrome. Biochemistry, 2007, 46 (41), 11459-11472.
75. Columbus, L.; Lipfert, J.; Jambunathan, K.; Fox, D.A.; Sim, A.Y.; Doniach, S.; Lesley, S.A.; Mixing and matching detergents for membrane protein NMR structure determination. J. Am. Chem. Soc., 2009, 131 (21), 7320-7326.
76. Warschawski, D.E.; Arnold, A.A.; Beaugrand, M.; Gravel, A.; Chartrand, E.; Marcotte, I.; Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim. Biophys. Acta, 2011, 1808 (8), 1957-1974.
77. Dopico, A.M.; Bukiya, A.N.; Singh, A.K.; Large conductance, calcium- and voltage-gated potassium (BK) channels: Regulation by cholesterol. Pharmacol. Ther., 2012., 135(2), 133-150.
78. Oates, J.; Watts, A.; Uncovering the intimate relationship between lipids, cholesterol and GPCR activation. Curr. Opin. Struct. Biol., 2011, 21 (6), 802-807.
79. Oates, J.; Faust, B.; Attrill, H.; Harding, P.; Orwick, M.; Watts, A.; The role of cholesterol on the activity and stability of neurotensin receptor 1. Biochim. Biophys. Acta, 2012.
80. Tapaneeyakorn, S.; Goddard, A.D.; Oates, J.; Willis, C.L.; Watts, A.; Solution- and solid-state NMR studies of GPCRs and their ligands. Biochim. Biophys. Acta, 2011, 1808 (6), 1462-1475.
81. Katritch, V.; Cherezov, V.; Stevens, R.C.; Diversity and modularity of G protein-coupled receptor structures. Trends Pharmacol. Sci., 2012, 33 (1), 17-27.
82. Howell, S.C.; Mittal, R.; Huang, L.; Travis, B.; Breyer, R.M.; Sanders, C.R.; CHOBIMALT: a cholesterol-based detergent. Biochemistry, 2010, 49 (44), 9572-9583.
83. Beel, A.J.; Sakakura, M.; Barrett, P.J.; Sanders, C.R.; Direct binding of cholesterol to the amyloid precursor protein: An important interaction in lipid-Alzheimer's disease relationships? Biochim. Biophys. Acta, 2010, 1801 (8), 975-982.
84. Beel, A.J.; Mobley, C.K.; Kim, H.J.; Tian, F.; Hadziselimovic, A.; Jap, B.; Prestegard, J.H.; Sanders, C.R.; Structural studies of the transmembrane C-terminal domain of the amyloid precursor protein (APP): does APP function as a cholesterol sensor? Biochemistry, 2008, 47 (36), 9428-9446.
85. Li, Q.; Mittal, R.; Huang, L.; Travis, B.; Sanders, C.R.; Bolaamphiphile-class surfactants can stabilize and support the function of solubilized integral membrane proteins. Biochemistry, 2009, 48 (49), 11606-11608.
86. Diller, A.; Loudet, C.; Aussenac, F.; Raffard, G.; Fournier, S.; Laguerre, M.; Grelard, A.; Opella, S.J.; Marassi, F.M.; Dufourc, E.J.; Bicelles: A natural 'molecular goniometer' for structural, dynamical and topological studies of molecules in membranes. Biochimie, 2009, 91 (6), 744-751.
87. Sanders, C.R.; Prosser, R.S.; Bicelles: a model membrane system for all seasons? Structure, 1998, 6 (10), 1227-1234.
88. van Meer, G.; Voelker, D.R.; Feigenson, G.W.; Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol., 2008, 9 (2), 112-124.
89. Kang, C.; Vanoye, C.G.; Welch, R.C.; Van Horn, W.D.; Sanders, C.R.; Functional delivery of a membrane protein into oocyte membranes using bicelles. Biochemistry, 2010, 49 (4), 653-655.
90. Van Horn, W.D.; Ogilvie, M.E.; Flynn, P.F.; Use of reverse micelles in membrane protein structural biology. J. Biomol. NMR., 2008, 40 (3), 203-211.
91. Kielec, J.M.; Valentine, K.G.; Babu, C.R.; Wand, A.J.; Reverse micelles in integral membrane protein structural biology by solution NMR spectroscopy. Structure, 2009, 17 (3), 345-351.
92. Baker, K.A.; Tzitzilonis, C.; Kwiatkowski, W.; Choe, S.; Riek, R.; Conformational dynamics of the KcsA potassium channel governs gating properties. Nat. Struct. Mol. Biol., 2007, 14 (11), 1089-1095.
93. Chill, J.H.; Louis, J.M.; Miller, C.; Bax, A.; NMR study of the tetrameric KcsA potassium channel in detergent micelles. Protein Sci., 2006, 15 (4), 684-698.
94. Breyton, C.; Pucci, B.; Popot, J.L.; Amphipols and fluorinated surfactants: Two alternatives to detergents for studying membrane proteins in vitro. Methods Mol. Biol., 2010, 601, 219-245.
95. Popot, J.L.; Althoff, T.; Bagnard, D.; Baneres, J.L.; Bazzacco, P.; Billon-Denis, E.; Catoire, L.J.; Champeil, P.; Charvolin, D.; Cocco, M.J.; Cremel, G.; Dahmane, T.; de la Maza, L.M.; Ebel, C.; Gabel, F.; Giusti, F.; Gohon, Y.; Goormaghtigh, E.; Guittet, E.; Kleinschmidt, J.H.; Kuhlbrandt, W.; Le Bon, C.; Martinez, K.L.; Picard, M.; Pucci, B.; Sachs, J.N.; Tribet, C.; van Heijenoort, C.; Wien, F.; Zito, F.; Zoonens, M.; Amphipols from A to Z. Annu. Rev. Biophys., 2011, 40, 379-408.
96. Catoire, L.J.; Zoonens, M.; van Heijenoort, C.; Giusti, F.; Guittet, E.; Popot, J.L.; Solution NMR mapping of water-accessible residues in the transmembrane beta-barrel of OmpX. Eur. Biophys. J., 2010, 39 (4), 623-630.
97. Wang, X.; Corin, K.; Baaske, P.; Wienken, C.J.; Jerabek-Willemsen, M.; Duhr, S.; Braun, D.; Zhang, S.; Peptide surfactants for cell-free production of functional G protein-coupled receptors. Proc. Natl. Acad. Sci. U. S. A., 2011, 108 (22), 9049-9054.
98. Zhang, Q.; Tao, H.; Hong, W.X.; New amphiphiles for membrane protein structural biology. Methods, 2011, 55 (4), 318-323.
99. Coey, A.T.; Sahu, I.D.; Gunasekera, T.S.; Troxel, K.R.; Hawn, J.M.; Swartz, M.S.; Wickenheiser, M.R.; Reid, R.J.; Welch, R.C.; Vanoye, C.G.; Kang, C.; Sanders, C.R.; Lorigan, G.A.; Reconstitution of KCNE1 into Lipid Bilayers: Comparing the Structural, Dynamic, and Activity Differences in Micelle and Vesicle Environments. Biochemistry, 2011, 50 (50), 10851-10859.
100. Yu, T.Y.; Raschle, T.; Hiller, S.; Wagner, G.; Solution NMR spectroscopic characterization of human VDAC-2 in detergent micelles and lipid bilayer nanodiscs. Biochim. Biophys. Acta, 2012, 1818 (6), 1562-1569.
101. Raschle, T.; Hiller, S.; Yu, T.Y.; Rice, A.J.; Walz, T.; Wagner, G.; Structural and functional characterization of the integral membrane protein VDAC-1 in lipid bilayer nanodiscs. J. Am. Chem. Soc., 2009, 131 (49), 17777-17779.
102. Lyukmanova, E.N.; Shenkarev, Z.O.; Paramonov, A.S.; Sobol, A.G.; Ovchinnikova, T.V.; Chupin, V.V.; Kirpichnikov, M.P.; Blommers, M.J.; Arseniev, A.S.; Lipid-protein nanoscale bilayers: a versatile medium for NMR investigations of membrane proteins and membrane-active peptides. J. Am. Chem. Soc., 2008, 130 (7), 2140-2141.
103. Raschle, T.; Hiller, S.; Etzkorn, M.; Wagner, G.; Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Curr. Opin. Struct. Biol., 2010, 20 (4), 471-479.
104. Potluri, S.; Yan, A.K.; Chou, J.J.; Donald, B.R.; Bailey-Kellogg, C.; Structure determination of symmetric homo-oligomers by a complete search of symmetry configuration space, using NMR restraints and van der Waals packing. Proteins, 2006, 65 (1), 203-219.
105. Otting, G.; Protein NMR using paramagnetic ions. Annu. Rev. Biophys., 2010, 39, 387-405.
106. Montaville, P.; Jamin, N.; Determination of membrane protein structures using solution and solid-state NMR. Methods Mol. Biol., 2010, 654, 261-282.
107. Hohlweg, W.; Kosol, S.; Zangger, K.; Determining the orientation and localization of membrane-bound peptides. Curr. Protein Pept. Sci., 2011.
108. Prosser, R.S.; Evanics, F.; Kitevski, J.L.; Patel, S.; The measurement of immersion depth and topology of membrane proteins by solution state NMR. Biochim. Biophys. Acta, 2007, 1768 (12), 3044-3051.
109. Berardi, M.J.; Shih, W.M.; Harrison, S.C.; Chou, J.J.; Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature, 2011.
110. Suk, J.E.; Situ, A.J.; Ulmer, T.S.; Construction of Covalent Membrane Protein Complexes and High-Throughput Selection of Membrane Mimics. J. Am. Chem. Soc., 2012, 134(22), 9030-9033.
111. Klammt, C.; Maslennikov, I.; Bayrhuber, M.; Eichmann, C.; Vajpai, N.; Chiu, E.J.; Blain, K.Y.; Esquivies, L.; Kwon, J.H.; Balana, B.; Pieper, U.; Sali, A.; Slesinger, P.A.; Kwiatkowski, W.; Riek, R.; Choe, S.; Facile backbone structure determination of human membrane proteins by NMR spectroscopy. Nat. Methods, 2012, 9(8), 834-839.
112. Tulumello, D.V.; Deber, C.M.; Efficiency of detergents at maintaining membrane protein structures in their biologically relevant forms. Biochim. Biophys. Acta, 2012, 1818 (5), 1351-1358.
113. Fontaine, F.; Fuchs, R.T.; Storz, G.; Membrane localization of small proteins in Escherichia coli. J. Biol. Chem., 2011, 286 (37), 32464-32474.
114. Liang, B.; Arora, A.; Tamm, L.K.; Fast-time scale dynamics of outer membrane protein A by extended model-free analysis of NMR relaxation data. Biochim. Biophys. Acta, 2010, 1798 (2), 68-76.
115. Hwang, P.M.; Kay, L.E.; Solution structure and dynamics of integral membrane proteins by NMR: a case study involving the enzyme PagP. Methods Enzymol., 2005, 394, 335-350.
116. Ma, D.; Tillman, T.S.; Tang, P.; Meirovitch, E.; Eckenhoff, R.; Carnini, A.; Xu, Y.; NMR studies of a channel protein without membranes: Structure and dynamics of water-solubilized KcsA. Proc. Natl. Acad. Sci. U. S. A., 2008, 105 (43), 16537-16542.
117. Traaseth, N.J.; Veglia, G.; Probing excited states and activation energy for the integral membrane protein phospholamban by NMR CPMG relaxation dispersion experiments. Biochim. Biophys. Acta, 2010, 1798 (2), 77-81.
118. Zhuang, T.; Jap, B.K.; Sanders, C.R.; Solution NMR approaches for establishing specificity of weak heterodimerization of membrane proteins. J. Am. Chem. Soc., 2011, 133 (50), 20571-20580.
119. Gao, J.; Chang, Y.S.; Jallal, B.; Viner, J.; Targeting the insulin-like growth factor axis for the development of novel therapeutics in oncology. Cancer Res., 2012, 72 (1), 3-12.
120. Campos-Olivas, R.; NMR Screening and Hit Validation in Fragment Based Drug Discovery. Curr. Top. Med. Chem., 2010.
121. Shuker, S.B.; Hajduk, P.J.; Meadows, R.P.; Fesik, S.W.; Discovering high-affinity ligands for proteins: SAR by NMR. Science, 1996, 274 (5292), 1531-1534.
122. Fesik, S.W.; NMR structure-based drug design. J. Biomol. NMR., 1993, 3 (3), 261-269.
123. Wirmer-Bartoschek, J.; Bartoschek, S.; NMR in drug discovery on membrane proteins. Future Med. Chem., 2012, 4 (7), 869-875.
124. Constantinescu, S.N.; Keren, T.; Socolovsky, M.; Nam, H.; Henis, Y.I.; Lodish, H.F.; Ligand-independent oligomerization of cell- surface erythropoietin receptor is mediated by the transmembrane domain. Proc. Natl. Acad. Sci. U. S. A., 2001, 98 (8), 4379-4384.
125. Matthews, E.E.; Thevenin, D.; Rogers, J.M.; Gotow, L.; Lira, P.D.; Reiter, L.A.; Brissette, W.H.; Engelman, D.M.; Thrombopoietin receptor activation: transmembrane helix dimerization, rotation, and allosteric modulation. FASEB J., 2011, 25 (7), 2234-2244.
126. Erickson-Miller, C.L.; DeLorme, E.; Tian, S.S.; Hopson, C.B.; Stark, K.; Giampa, L.; Valoret, E.I.; Duffy, K.J.; Luengo, J.L.; Rosen, J.; Miller, S.G.; Dillon, S.B.; Lamb, P.; Discovery and characterization of a selective, nonpeptidyl thrombopoietin receptor agonist. Exp. Hematol., 2005, 33 (1), 85-93.
127. Kim, M.J.; Park, S.H.; Opella, S.J.; Marsilje, T.H.; Michellys, P.Y.; Seidel, H.M.; Tian, S.S.; NMR structural studies of interactions of a small, nonpeptidyl Tpo mimic with the thrombopoietin receptor extracellular juxtamembrane and transmembrane domains. J. Biol. Chem., 2007, 282 (19), 14253-14261.
128. Yanamala, N.; Dutta, A.; Beck, B.; van Fleet, B.; Hay, K.; Yazbak, A.; Ishima, R.; Doemling, A.; Klein-Seetharaman, J.; NMR-based screening of membrane protein ligands. Chem. Biol. Drug Des., 2010, 75 (3), 237-256.
129. Du, Q.S.; Huang, R.B.; Wang, S.Q.; Chou, K.C.; Designing inhibitors of M2 proton channel against H1N1 swine influenza virus. PLoS One, 2010, 5 (2), e9388.
130. Page, R.C.; Lee, S.; Moore, J.D.; Opella, S.J.; Cross, T.A.; Backbone structure of a small helical integral membrane protein: A unique structural characterization. Protein Sci., 2009, 18 (1), 134-146.
131. Hu, Y.; Zhao, E.; Li, H.; Xia, B.; Jin, C.; Solution NMR structure of the TatA component of the twin-arginine protein transport system from gram-positive bacterium Bacillus subtilis. J. Am. Chem. Soc., 2010, 132 (45), 15942-15944.
132. Wittlich, M.; Thiagarajan, P.; Koenig, B.W.; Hartmann, R.; Willbold, D.; NMR structure of the transmembrane and cytoplasmic domains of human CD4 in micelles. Biochim. Biophys. Acta, 2010, 1798 (2), 122-127.
133. Buck-Koehntop, B.A.; Mascioni, A.; Buffy, J.J.; Veglia, G.; Structure, dynamics, and membrane topology of stannin: a mediator of neuronal cell apoptosis induced by trimethyltin chloride. J. Mol. Biol., 2005, 354 (3), 652-665.
134. Jaroniec, C.P.; Kaufman, J.D.; Stahl, S.J.; Viard, M.; Blumenthal, R.; Wingfield, P.T.; Bax, A.; Structure and dynamics of micelle- associated human immunodeficiency virus gp41 fusion domain. Biochemistry, 2005, 44 (49), 16167-16180.
135. Papavoine, C.H.; Christiaans, B.E.; Folmer, R.H.; Konings, R.N.; Hilbers, C.W.; Solution structure of the M13 major coat protein in detergent micelles: a basis for a model of phage assembly involving specific residues. J. Mol. Biol., 1998, 282 (2), 401-419.
136. Mascioni, A.; Porcelli, F.; Ilangovan, U.; Ramamoorthy, A.; Veglia, G.; Conformational preferences of the amylin nucleation site in SDS micelles: an NMR study. Biopolymers, 2003, 69 (1), 29-41.
137. Franzin, C.M.; Teriete, P.; Marassi, F.M.; Structural similarity of a membrane protein in micelles and membranes. J. Am. Chem. Soc., 2007, 129 (26), 8078-8079.
138. Teriete, P.; Franzin, C.M.; Choi, J.; Marassi, F.M.; Structure of the Na,K-ATPase regulatory protein FXYD1 in micelles. Biochemistry, 2007, 46 (23), 6774-6783.
139. Park, S.H.; Son, W.S.; Mukhopadhyay, R.; Valafar, H.; Opella, S.J.; Phage-induced alignment of membrane proteins enables the measurement and structural analysis of residual dipolar couplings with dipolar waves and lambda-maps. J. Am. Chem. Soc., 2009, 131 (40), 14140-14141.
140. Pielak, R.M.; Chou, J.J.; Solution NMR structure of the V27A drug resistant mutant of influenza A M2 channel. Biochemical and Biophysical Research Communications, 2010, 401 (1), 58-63.
141. Lau, T.L.; Dua, V.; Ulmer, T.S.; Structure of the integrin alphaIIb transmembrane segment. J. Biol. Chem., 2008, 283 (23), 16162-16168.
142. Wang, Z.Y.; Suzuki, H.; Kobayashi, M.; Nozawa, T.; Solution structure of the Rhodobacter sphaeroides PufX membrane protein: implications for the quinone exchange and protein-protein interactions. Biochemistry, 2007, 46 (12), 3635-3642.
143. Tunnicliffe, R.B.; Ratcliffe, E.C.; Hunter, C.N.; Williamson, M.P.; The solution structure of the PufX polypeptide from Rhodobacter sphaeroides. FEBS Lett., 2006, 580 (30), 6967-6971.
144. Tunnicliffe, R.B.; Ratcliffe, E.C.; Hunter, C.N.; Williamson, M.P.; The solution structure of the PufX polypeptide from Rhodobacter sphaeroides. FEBS Lett., 2006, 580 (30), 6967-6971.
145. Wang, Z.Y.; Gokan, K.; Kobayashi, M.; Nozawa, T.; Solution structures of the core light-harvesting alpha and beta polypeptides from Rhodospirillum rubrum: implications for the pigment-protein and protein-protein interactions. J. Mol. Biol., 2005, 347 (2), 465-477.
146. Zubkov, S.; Lennarz, W.J.; Mohanty, S.; Structural basis for the function of a minimembrane protein subunit of yeast oligosaccharyltransferase. Proc. Natl. Acad. Sci. U. S. A., 2004, 101 (11), 3821-3826.
147. Gayen, S.; Kang, C.; Solution structure of a human minimembrane protein Ost4, a subunit of the oligosaccharyltransferase complex. Biochem. Biophys. Res. Commun., 2011, 409 (3), 572-576.
148. Dmitriev, O.; Jones, P.C.; Jiang, W.; Fillingame, R.H.; Structure of the Membrane Domain of Subunit b of the Escherichia coli F0F1 ATP Synthase. J. Biol. Chem., 1999, 274 (22), 15598-15604.
149. Goetz, M.; Carlotti, C.; Bontems, F.; Dufourc, E.J.; Evidence for an alpha-helix --> pi-bulge helicity modulation for the neu/erbB-2 membrane-spanning segment. A 1H NMR and circular dichroism study. Biochemistry, 2001, 40 (21), 6534-6540.
150. Sorgen, P.L.; Cahill, S.M.; Krueger-Koplin, R.D.; Krueger-Koplin, S.T.; Schenck, C.C.; Girvin, M.E.; Structure of the Rhodobacter sphaeroides light-harvesting 1 beta subunit in detergent micelles. Biochemistry, 2002, 41 (1), 31-41.
151. Pellecchia, M.; Sem, D.S.; Wuthrich, K.; NMR in drug discovery. Nat. Rev. Drug Discov., 2002, 1 (3), 211-219.
152. Martini, S.; Bonechi, C.; Casolaro, M.; Corbini, G.; Rossi, C.; Drug-protein recognition processes investigated by NMR relaxation data. A study on corticosteroid-albumin interactions. Biochem. Pharmacol., 2006, 71 (6), 858-864.
153. Jahnke, W.; Spin labels as a tool to identify and characterize protein-ligand interactions by NMR spectroscopy. Chembiochem, 2002, 3 (2-3), 167-173.
154. Cutting, B.; Strauss, A.; Fendrich, G.; Manley, P.W.; Jahnke, W.; NMR resonance assignment of selectively labeled proteins by the use of paramagnetic ligands. J. Biomol. NMR., 2004, 30 (2), 205-210.
155. Jahnke, W.; Rudisser, S.; Zurini, M.; Spin label enhanced NMR screening. J. Am. Chem. Soc., 2001, 123 (13), 3149-3150.
156. Price, W.S.; Recent Advances in NMR Diffusion Techniques for Studying Drug Binding. Austral. J. Chem., 2003, 56 (9), 855-860.
157. Wang, Y.S.; Liu, D.; Wyss, D.F.; Competition STD NMR for the detection of high-affinity ligands and NMR-based screening. Magn. Reson. Chem., 2004, 42 (6), 485-489.
158. Meyer, B.; Klein, J.; Mayer, M.; Meinecke, R.; Moller, H.; Neffe, A.; Schuster, O.; Wulfken, J.; Ding, Y.; Knaie, O.; Labbe, J.; Palcic, M.M.; Hindsgaul, O.; Wagner, B.; Ernst, B.; Saturation transfer difference NMR spectroscopy for identifying ligand epitopes and binding specificities. Ernst. Schering Res. Found. Workshop, 2004, (44), 149-167.
159. Takeuchi, K.; Yokogawa, M.; Matsuda, T.; Sugai, M.; Kawano, S.; Kohno, T.; Nakamura, H.; Takahashi, H.; Shimada, I.; Structural basis of the KcsA K(+) channel and agitoxin2 pore-blocking toxin interaction by using the transferred cross-saturation method. Structure, 2003, 11 (11), 1381-1392.
160. Claasen, B.; Axmann, M.; Meinecke, R.; Meyer, B.; Direct observation of ligand binding to membrane proteins in living cells by a saturation transfer double difference (STDD) NMR spectroscopy method shows a significantly higher affinity of integrin alpha(IIb)beta3 in native platelets than in liposomes. J. Am. Chem. Soc., 2005, 127 (3), 916-919.
161. Meinecke, R.; Meyer, B.; Determination of the binding specificity of an integral membrane protein by saturation transfer difference NMR: RGD peptide ligands binding to integrin alphaIIbbeta3. J. Med. Chem., 2001, 44 (19), 3059-3065.
162. Dalvit, C.; Fogliatto, G.; Stewart, A.; Veronesi, M.; Stockman, B.; WaterLOGSY as a method for primary NMR screening: practical aspects and range of applicability. J. Biomol. NMR., 2001, 21 (4), 349-359.
163. Dalvit, C.; Flocco, M.; Knapp, S.; Mostardini, M.; Perego, R.; Stockman, B.J.; Veronesi, M.; Varasi, M.; High-throughput NMR- based screening with competition binding experiments. J. Am. Chem. Soc., 2002, 124 (26), 7702-7709.
164. Dalvit, C.; Fasolini, M.; Flocco, M.; Knapp, S.; Pevarello, P.; Veronesi, M.; NMR-Based screening with competition water- ligand observed via gradient spectroscopy experiments: detection of high-affinity ligands. J. Med. Chem., 2002, 45 (12), 2610-2614.
165. Yanamala, N.; Dutta, A.; Beck, B.; Van Fleet, B.; Hay, K.; Yazbak, A.; Ishima, R.; Doemling, A.; Klein-Seetharaman, J.; NMR-Based Screening of Membrane Protein Ligands. Chem. Biol. Drug Des., 2010, 75 (3), 237-256.
166. Seidel, R.D.; Zhuang, T.; Prestegard, J.H.; Bound-State Residual Dipolar Couplings for Rapidly Exchanging Ligands of His-Tagged Proteins. J. Am. Chem. Soc., 2007, 129 (15), 4834-4839.
167. Entress, R.M.; Dancer, R.J.; O'Brien, D.P.; Try, A.C.; Cooper, M.A.; Williams, D.H.; 19F NMR in the measurement of binding affinities of chloroeremomycin to model bacterial cell-wall surfaces that mimic VanA and VanB resistance. Chem. Biol., 1998, 5 (6), 329-337.
168. Yu, L.; Hajduk, P.J.; Mack, J.; Olejniczak, E.T.; Structural studies of Bcl-xL/ligand complexes using 19F NMR. J. Biomol. NMR., 2006, 34 (4), 221-227.