Solution NMR studies of polytopic α-helical membrane proteins

Current Opinion in Structural Biology

Volumn 21, Issue 4, 2011, Pages 497-508

  Nietlispach, Daniel ^a   Gautier, Antoine ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMANTADINE; BETA 2 ADRENERGIC RECEPTOR; CHEMOKINE RECEPTOR CCR5; G PROTEIN COUPLED RECEPTOR; INFLUENZA VIRUS A PROTON CHANNEL M2; KCSA PROTEIN; MEMBRANE LIPID; MEMBRANE PROTEIN; RIMANTADINE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALPHA HELIX; CONFORMATIONAL TRANSITION; DRUG BINDING SITE; ELECTRON SPIN RESONANCE; ISOTOPE LABELING; LIGAND BINDING; LIPID BILAYER; MICELLE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PH; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN REFOLDING; PROTEIN SOLUBILIZATION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; REVIEW; SOLUBILIZATION; TOTAL CORRELATION SPECTROSCOPY; TRANSVERSE RELAXATION OPTIMIZED SPECTROSCOPY;

ANIMALS; HUMANS; MEMBRANE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, G-PROTEIN-COUPLED; SOLUBILITY; SOLUTIONS;

EID: 80052090331     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2011.06.009     Document Type: Review

References (89)

1. Opella S.J., Marassi F.M. Structure determination of membrane proteins by NMR spectroscopy. Chemical Reviews 2004, 104:3587-3606.
2. McDermott A. Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR. Annu Rev Biophys 2009, 38:385-403.
3. Zhou Y.P., Cierpicki T., Jimenez R.H.F., Lukasik S.M., Ellena J.F., Cafiso D.S., Kadokura H., Beckwith J., Bushweller J.H. NMR solution structure of the integral membrane enzyme DsbB: functional insights into DsbB-catalyzed disulfide bond formation. Molecular Cell 2008, 31:896-908.
4. 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. Nature Structural & Molecular Biology 2010, 17:768-774.
5. Schnell J.R., Chou J.J. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 2008, 451:591-595.
6. Van Horn W.D., Kim H.J., Ellis C.D., Hadziselimovic A., Sulistijo E.S., Karra M.D., Tian C.L., Sonnichsen F.D., Sanders C.R. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 2009, 324:1726-1729.
7. Dahmane T., Damian M., Mary S., Popot J.L., Baneres J.L. Amphipol-assisted in vitro folding of G protein-coupled receptors. Biochemistry 2009, 48:6516-6521.
8. Popot J.L. Amphipols, nanodiscs, and fluorinated surfactants: three nonconventional approaches to studying membrane proteins in aqueous solutions. Annual Review of Biochemistry 2010, 79:737-775.
9. 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. Progress in Nuclear Magnetic Resonance Spectroscopy 2009, 55:335-360.
10. Fan Y., Shi L., Ladizhansky V., Brown L.S. Uniform isotope labeling of a eukaryotic seven-transmembrane helical protein in yeast enables high-resolution solid-state NMR studies in the lipid environment. Journal of Biomolecular NMR 2011, 49:151-161.
11. Pickford A.R., O'Leary J.M. Isotopic labeling of recombinant proteins from the methylotrophic yeast Pichia pastoris. Method Mol Biol 2004, 278:17-33.
12. Whittaker J.W. Selective isotopic labeling of recombinant proteins using amino acid auxotroph strains. Method Mol Biol 2007, 389:175-188.
13. Sobhanifar S., Reckel S., Junge F., Schwarz D., Kai L., Karbyshev M., Loehr F., Bernhard F., Doetsch V. Cell-free expression and stable isotope labelling strategies for membrane proteins. Journal of Biomolecular NMR 2010, 46:33-43.
14. Etezady-Esfarjani T., Hiller S., Villalba C., Wuthrich K. Cell-free protein synthesis of perdeuterated proteins for NMR studies. Journal of Biomolecular NMR 2007, 39:229-238.
15. Yokoyama J., Matsuda T., Koshiba S., Tochio N., Kigawa T. A practical method for cell-free protein synthesis to avoid stable isotope scrambling and dilution. Analytical Biochemistry 2011, 411:223-229.
16. Maslennikov I., Klammt C., Hwang E., Kefala G., Okamura M., Esquivies L., Mors K., Glaubitz C., Kwiatkowski W., Jeon Y.H., et al. Membrane domain structures of three classes of histidine kinase receptors by cell-free expression and rapid NMR analysis. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:10902-10907.
17. Cook G.A., Zhang H., Park S.H., Wang Y., Opella S.J. Comparative NMR studies demonstrate profound differences between two viroporins: p7 of HCV and Vpu of HIV-1. Biochim Biophys Acta Biomembr 2011, 1808:554-560.
18. Poget S.F., Girvin M.E. Solution NMR of membrane proteins in bilayer mimics: small is beautiful, but sometimes bigger is better. Biochim Biophys Acta Biomembr 2007, 1768:3098-3106.
19. Gluck J.M., Wittlich M., Feuerstein S., Hoffmann S., Willbold D., Koenig B.W. Integral membrane proteins in nanodiscs can be studied by solution NMR spectroscopy. Journal of the American Chemical Society 2009, 131:12060-12061.
20. Raschle T., Hiller S., Etzkorn M., Wagner G. Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Current Opinion in Structural Biology 2010, 20:471-479.
21. Dowhan W., Bogdanov M. Lipid-dependent membrane protein topogenesis. Annual Review of Biochemistry 2009, 78:515-540.
22. Lee A.G. How lipids and proteins interact in a membrane: a molecular approach. Mol Biosyst 2005, 1:203-212.
23. Yu L.P., Sun C.H., Song D.Y., Shen J.W., Xu N., Gunasekera A., Hajduk P.J., Olejniczak E.T. Nuclear magnetic resonance structural studies of a potassium channel-charybdotoxin complex. Biochemistry 2005, 44:15834-15841.
24. Gautier A., Kirkpatrick J.P., Nietlispach D. Solution-state NMR spectroscopy of a seven-helix transmembrane protein receptor: backbone assignment, secondary structure, and dynamics. Angewandte Chemie International Edition 2008, 47:7297-7300.
25. Rovnyak D., Frueh D.P., Sastry M., Sun Z.Y.J., Stern A.S., Hoch J.C., Wagner G. Accelerated acquisition of high resolution triple-resonance spectra using non-uniform sampling and maximum entropy reconstruction. Journal of Magnetic Resonance 2004, 170:15-21.
26. Shen Y., Delaglio F., Cornilescu G., Bax A. TALOS plus: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. Journal of Biomolecular NMR 2009, 44:213-223.
27. Tugarinov V., Kay L.E. Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods. Journal of the American Chemical Society 2003, 125:13868-13878.
28. Hiller S., Ibraghimov I., Wagner G., Orekhov V.Y. Coupled decomposition of four-dimensional NOESY spectra. Journal of the American Chemical Society 2009, 131:12970-12978.
29. Isaacson R.L., Simpson P.J., Liu M., Cota E., Zhang X., Freemont P., Matthews S. A new labeling method for methyl transverse relaxation-optimized spectroscopy NMR spectra of alanine residues. Journal of the American Chemical Society 2007, 129:15428-15429.
30. Ayala I., Sounier R., Use N., Gans P., Boisbouvier J. An efficient protocol for the complete incorporation of methyl-protonated alanine in perdeuterated protein. Journal of Biomolecular NMR 2009, 43:111-119.
31. Royant A., Nollert P., Edman K., Neutze R., Landau E.M., Pebay-Peyroula E., Navarro J. X-ray structure of sensory rhodopsin II at 2.1-angstrom resolution. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:10131-10136.
32. Luecke H., Schobert B., Lanyi J.K., Spudich E.N., Spudich J.L. Crystal structure of sensory rhodopsin II at 2.4angstroms: insights into color tuning and transducer interaction. Science 2001, 293:1499-1503.
33. Kainosho M., Guntert P. SAIL-stereo-array isotope labeling. Quarterly Reviews of Biophysics 2009, 42:247-300.
34. Liang B.Y., Bushweller J.H., Tamm L.K. Site-directed parallel spin-labeling and paramagnetic relaxation enhancement in structure determination of membrane proteins by solution NMR spectroscopy. Journal of the American Chemical Society 2006, 128:4389-4397.
35. Bayrhuber M., Meins T., Habeck M., Becker S., Giller K., Villinger S., Vonrhein C., Griesinger C., Zweckstetter M., Zeth K. Structure of the human voltage-dependent anion channel. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:15370-15375.
36. Otting G. Protein NMR using paramagnetic ions. Annu Rev Biophys 2010, 39:387-405.
37. Su X.C., Man B., Beeren S., Liang H., Simonsen S., Schmitz C., Huber T., Messerle B.A., Otting G. A dipicolinic acid tag for rigid lanthanide tagging of proteins and paramagnetic NMR spectroscopy. Journal of the American Chemical Society 2008, 130:10486-10487.
38. Haussinger D., Huang J.R., Grzesiek S. DOTA-M8: an extremely rigid, high-affinity lanthanide chelating tag for PCS NMR spectroscopy. Journal of the American Chemical Society 2009, 131:14761-14767.
39. Keizers P.H.J., Saragliadis A., Hiruma Y., Overhand M., Ubbink M. Design, synthesis, and evaluation of a lanthanide chelating protein probe: CLaNP-5 yields predictable paramagnetic effects independent of environment. Journal of the American Chemical Society 2008, 130:14802-14812.
40. Ma J.H., Goldberg G.I., Tjandra N. Weak alignment of biomacromolecules in collagen gels: an alternative way to yield residual dipolar couplings for NMR measurements. Journal of the American Chemical Society 2008, 130:16148-16149.
41. Cavalli A., Salvatella X., Dobson C.M., Vendruscolo M. Protein structure determination from NMR chemical shifts. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:9615-9620.
42. Shen Y., Lange O., Delaglio F., Rossi P., Aramini J.M., Liu G.H., Eletsky A., Wu Y.B., Singarapu K.K., Lemak A., et al. Consistent blind protein structure generation from NMR chemical shift data. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:4685-4690.
43. Raman S., Lange O.F., Rossi P., Tyka M., Wang X., Aramini J., Liu G.H., Ramelot T.A., Eletsky A., Szyperski T., et al. NMR structure determination for larger proteins using backbone-only data. Science 2010, 327:1014-1018.
44. Raman S., Huang Y.J.P., Mao B.C., Rossi P., Aramini J.M., Liu G.H., Montelione G.T., Baker D. Accurate automated protein NMR structure determination using unassigned NOESY data. Journal of the American Chemical Society 2010, 132:202-207.
45. Goncalves J.A., Ahuja S., Erfani S., Eilers M., Smith S.O. Structure and function of G protein-coupled receptors using NMR spectroscopy. Progress in Nuclear Magnetic Resonance Spectroscopy 2010, 57:159-180.
46. Topiol S., Sabio M. X-ray structure breakthroughs in the GPCR transmembrane region. Biochemical Pharmacology 2009, 78:11-20.
47. Tate C.G., Schertler G.F.X. Engineering G protein-coupled receptors to facilitate their structure determination. Current Opinion in Structural Biology 2009, 19:386-395.
48. Rosenbaum D.M., Rasmussen S.G.F., Kobilka B.K. The structure and function of G-protein-coupled receptors. Nature 2009, 459:356-363.
49. Rasmussen S.G.F., Choi H.J., Fung J.J., Pardon E., Casarosa P., Chae P.S., DeVree B.T., Rosenbaum D.M., Thian F.S., Kobilka T.S., et al. Structure of a nanobody-stabilized active state of the beta(2) adrenoceptor. Nature 2011, 469:175-180.
50. Standfuss J., Edwards P.C., D'Antona A., Fransen M., Xie G., Oprian D.D., Schertler G.F. The structural basis of agonist induced activation in constitutively active rhodopsin. Nature 2011, 10.1038/nature09795.
51. Choe H.W., Kim Y.J., Park J.H., Morizumi T., Pai E.F., Krauss N., Hofmann K.P., Scheerer P., Ernst O.P. Crystal structure of metarhodopsin II. Nature 2011, 10.1038/nature09789.
52. Bokoch M.P., Zou Y.Z., Rasmussen S.G.F., Liu C.W., Nygaard R., Rosenbaum D.M., Fung J.J., Choi H.J., Thian F.S., Kobilka T.S., et al. Ligand-specific regulation of the extracellular surface of a G-protein-coupled receptor. Nature 2010, 463:108-112.
53. Klein-Seetharaman J., Yanamala N.V.K., Javeed F., Reeves P.J., Getmanova E.V., Loewen M.C., Schwalbe H., Khorana H.G. Differential dynamics in the G protein-coupled receptor rhodopsin revealed by solution NMR. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:3409-3413.
54. Werner K., Lehner I., Dhiman H.K., Richter C., Glaubitz C., Schwalbe H., Klein-Seetharaman J., Khorana H.G. Combined solid state and solution NMR studies of alpha,epsilon-N-15 labeled bovine rhodopsin. Journal of Biomolecular NMR 2007, 37:303-312.
55. Werner K., Richter C., Klein-Seetharaman J., Schwalbe H. Isotope labeling of mammalian GPCRs in HEK293 cells and characterization of the C-terminus of bovine rhodopsin by high resolution liquid NMR spectroscopy. Journal of Biomolecular NMR 2008, 40:49-53.
56. Cady S.D., Schmidt-Rohr K., Wang J., Soto C.S., DeGrado W.F., Hong M. Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 2010, 463:689-692.
57. Hu F.H., Luo W.B., Cady S.D., Hong M. Conformational plasticity of the influenza A M2 transmembrane helix in lipid bilayers under varying pH, drug binding, and membrane thickness. Biochim Biophys Acta Biomembr 2011, 1808:415-423.
58. 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 Mol Cell Biol Lipids 2010, 1801:975-982.
59. Chill J.H., Louis J.M., Miller C., Bax A. NMR study of the tetrameric KcsA potassiumchannel in detergent micelles. Protein Science 2006, 15:684-698.
60. Baker K.A., Tzitzilonis C., Kwiatkowski W., Choe S., Riek R. Conformational dynamics of the KcsA potassium channel governs gating properties. Nature Structural & Molecular Biology 2007, 14:1089-1095.
61. Soubias O., Gawrisch K. Probing specific lipid-protein interaction by saturation transfer difference NMR spectroscopy. Journal of the American Chemical Society 2005, 127:13110-13111.
62. Hilty C., Wider G., Fernandez C., Wuthrich K. Membrane protein-lipid interactions in mixed micelles studied by NMR spectroscopy with the use of paramagnetic reagents. Chembiochem 2004, 5:467-473.
63. Respondek M., Madl T., Gobl C., Golser R., Zangger K. Mapping the orientation of helices in micelle-bound peptides by paramagnetic relaxation waves. Journal of the American Chemical Society 2007, 129:5228-5234.
64. Prosser R.S., Luchette P.A., Westerman P.W. Using O-2 to probe membrane immersion depth by F-19 NMR. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:9967-9971.
65. 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 Biomembr 2007, 1768:3044-3051.
66. Page R.C., Li C., Hu J., Gao F.P., Cross T.A. Lipid bilayers: an essential environment for the understanding of membrane proteins. Magnetic Resonance in Chemistry 2007, 45:S2-S11.
67. Franzin C.M., Gong X.M., Thai K., Yu J.H., Marassi F.M. NMR of membrane proteins in micelles and bilayers: the FXYD family proteins. Methods 2007, 41:398-408.
68. Traaseth N.J., Shi L., Verardi R., Mullen D.G., Barany G., Veglia G. Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:10165-10170.
69. Shi L., Traaseth N.J., Verardi R., Cembran A., Gao J.L., Veglia G. A refinement protocol to determine structure, topology, and depth of insertion of membrane proteins using hybrid solution and solid-state NMR restraints. Journal of Biomolecular NMR 2009, 44:195-205.
70. Kang C.B., 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, 49:653-655.
71. Poget S.F., Cahill S.M., Girvin M.E. Isotropic bicelles stabilize the functional form of a small multidrug-resistance pump for NMR structural studies. Journal of the American Chemical Society 2007, 129:2432-2433.
72. Lau T.L., Kim C., Ginsberg M.H., Ulmer T.S. The structure of the integrin alpha IIb beta 3 transmembrane complex explains integrin transmembrane signalling. EMBO Journal 2009, 28:1351-1361.
73. Koehler J., Sulistijo E.S., Sakakura M., Kim F.J., Ellis C.D., Sanders C.R. Lysophospholipid micelles sustain the stability and catalytic activity of diacylglycerol kinase in the absence of lipids. Biochemistry 2010, 49:7089-7099.
74. Shenkarev Z.O., Lyukmanova E.N., Paramonov A.S., Shingarova L.N., Chupin V.V., Kirpichnikov M.P., Blommers M.J.J., Arseniev A.S. Lipid-protein nanodiscs as reference medium in detergent screening for high-resolution NMR studies of integral membrane proteins. Journal of the American Chemical Society 2010, 132:5628-5629.
75. Inaba K., Murakami S., Suzuki M., Nakagawa A., Yamashita E., Okada K., Ito K. Crystal structure of the DsbB-DsbA complex reveals a mechanism of disulfide bond generation. Cell 2006, 127:789-801.
76. Takeuchi K., Takahashi H., Kawano S., Shimada I. Identification and characterization of the slowly exchanging pH-dependent conformational rearrangement in KcsA. Journal of Biological Chemistry 2007, 282:15179-15186.
77. Imai S., Osawa M., Takeuchi K., Shimada I. Structural basis underlying the dual gate properties of KcsA. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:6216-6221.
78. 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, 75:237-256.
79. Assadi-Porter F.M., Tonelli M., Maillet E., Hallenga K., Benard O., Max M., Markley J.L. Direct NMR detection of the binding of functional ligands to the human sweet receptor, a heterodimeric family 3 GPCR. Journal of the American Chemical Society 2008, 130:7212-7213.
80. Kofuku Y., Yoshiura C., Ueda T., Terasawa H., Hirai T., Tominaga S., Hirose M., Maeda Y., Takahashi H., Terashima Y., et al. Structural basis of the interaction between chemokine stromal cell-derived factor-1/CXCL12 and its G-protein-coupled receptor CXCR4. Journal of Biological Chemistry 2009, 284:35240-35250.
81. Yoshiura C., Kofuku Y., Ueda T., Mase Y., Yokogawa M., Osawa M., Terashima Y., Matsushima K., Shimada I. NMR analyses of the interaction between CCR5 and its ligand using functional reconstitution of CCR5 in lipid bilayers. Journal of the American Chemical Society 2010, 132:6768-6777.
82. Weis W.I., Kobilka B.K. Structural insights into G-protein-coupled receptor activation. Current Opinion in Structural Biology 2008, 18:734-740.
83. Bokoch M.P., Zou Y.Z., Rasmussen S.G.F., Liu C.W., Nygaard R., Rosenbaum D.M., Fung J.J., Choi H.J., Thian F.S., Kobilka T.S., et al. Ligand-specific regulation of the extracellular surface of a G-protein-coupled receptor. Nature 2010, 463:108-121.
84. Ruan K.H., Cervantes V., Wu J.X. Ligand-specific conformation determines agonist activation and antagonist blockade in purified human thromboxane A2 receptor. Biochemistry 2009, 48:3157-3165.
85. Ma D.J., 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. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:16537-16542.
86. Oxenoid K., Chou J.J. The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:10870-10875.
87. Trbovic N., Klammt C., Koglin A., Lohr F., Bernhard F., Dotsch V. Efficient strategy for the rapid backbone assignment of membrane proteins. Journal of the American Chemical Society 2005, 127:13504-13505.
88. Poget S.F., Krueger-Koplin S.T., Krueger-Koplin R.D., Cahill S.M., Shekar S.C., Girvin M.E. NMR assignment of the dimeric S. aureus small multidrug-resistance pump in LPPG micelles. Journal of Biomolecular NMR 2006, 36:10.
89. Huang C.D., Mohanty S. Challenging the limit: NMR assignment of a 31kDa helical membrane protein. Journal of the American Chemical Society 2010, 132:3662-3663.