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Membrane Protein Production for Structural Analysis

  • Isabelle Mus-Veteau
  • Pascal Demange
  • Francesca Zito
Chapter

Abstract

Membrane proteins (MPs) account for roughly 30 % of all open reading frames in fully sequenced genomes. However, to date, atomic structures have so far been obtained for only 474 integral MPs, with 150 new structures determined in the past 2 years. Only 10 % of the unique integral MP structures are derived from vertebrates. The majority of integral MPs is present in tissues at very low concentration, making production of recombinant proteins in heterologous systems suitable for large-scale production a prerequisite for structural studies. Since the first atomic structures of recombinant mammalian integral MPs published in 2005 (Jidenko et al., Proc Natl Acad Sci U S A 102:11687–11691, 2005; Long et al., Science 309:897–903, 2005), the structures of 37 recombinant mammalian integral MPs, of which 20 belong to the G protein-coupled receptors family, have been solved. This chapter reviews the advances in heterologous expression systems, stabilization tools, and structural methods that contributed to the growing number of recombinant mammalian integral MP structures solved this past years.

Keywords

Nuclear Magnetic Resonance Nuclear Magnetic Resonance Spectroscopy Nuclear Magnetic Resonance Structure Detergent Micelle Solution Nuclear Magnetic Resonance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Andréll J, Tate CG (2013) Overexpression of membrane proteins in mammalian cells for structural studies. Mol Membr Biol 30:52–63PubMedCentralPubMedGoogle Scholar
  2. Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, Harrell PM, Trinh YT, Zhang Q, Urbatsch IL, et al (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323:1718–1722Google Scholar
  3. Arechaga I, Miroux B, Karrasch S, Huijbregts R, de Kruijff B, Runswick MJ, and Walker, JE (2000) Characterisation of new intracellular membranes in Escherichia coli accompanying large scale over-production of the b subunit of F(1)F(o) ATP synthase. FEBS Lett 482:215–219Google Scholar
  4. Baconguis I, Gouaux E (2012) Structural plasticity and dynamic selectivity of acid-sensing ion channel-spider toxin complexes. Nature 489:400–405Google Scholar
  5. Baldus M (2006) Molecular interactions investigated by multi-dimensional solid-state NMR. Curr Opin Struct Biol 16:618–623PubMedGoogle Scholar
  6. Banères JL, Mouillac B (2012) Handling G-protein-coupled receptors: expression, purification and in vitro stabilization. Med Sci (Paris) 28:837–844Google Scholar
  7. Bayburt TH, Sligar SG (2010) Membrane protein assembly into Nanodiscs. FEBS Lett 584:1721–1727PubMedGoogle Scholar
  8. Bazzacco P, Billon-Denis E, Sharma KS, Catoire LJ, Mary S, Le Bon C, Point E, Banères JL, Durand G, Zito F, Pucci B, Popot JL (2012) Nonionic homopolymeric amphipols: application to membrane protein folding, cell-free synthesis, and solution nuclear magnetic resonance. Biochemistry 51:1416–1430PubMedGoogle Scholar
  9. Berardi MJ, Shih WM, Harrison SC, Chou JJ (2011) Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature 476:109–113PubMedCentralPubMedGoogle Scholar
  10. Bill RM, Henderson PJ, Iwata S, Kunji ER, Michel H, Neutze R et al (2011) Overcoming barriers to membrane protein structure determination. Nat Biotechnol 29:335–340PubMedGoogle Scholar
  11. Blesneac I, Ravaud S, Juillan-Binard C, Barret LA, Zoonens M, Polidori A, Miroux B, Pucci B, Pebay-Peyroula E (2012) Production of UCP1 a membrane protein from the inner mitochondrial membrane using the cell free expression system in the presence of a fluorinated surfactant. Biochim Biophys Acta 1818:798–805PubMedGoogle Scholar
  12. Blow N (2008) Structural genomics: inside a protein structure initiative center. Nat Meth 5:203–207Google Scholar
  13. Bocharov EV, Pustovalova YE, Pavlov KV, Volynsky PE, Goncharuk MV, Ermolyuk YS, Karpunin DV, Schulga AA, Kirpichnikov MP, Efremov RG et al (2007) Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger. J Biol Chem 282:16256–16266PubMedGoogle Scholar
  14. Bocharov EV, Mineev KS, Volynsky PE, Ermolyuk YS, Tkach EN, Sobol AG, Chupin VV, Kirpichnikov MP, Efremov RG, Arseniev AS (2008) Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state. J Biol Chem 283:6950–6956PubMedGoogle Scholar
  15. Bokoch MP, Zou YZ, Rasmussen SGF, Liu CW, Nygaard R, Rosenbaum DM, Fung JJ, Choi HJ, Thian FS, Kobilka TS et al (2010) Ligand-specific regulation of the extracellular surface of a G-protein-coupled receptor. Nature 463:108–121PubMedCentralPubMedGoogle Scholar
  16. Bonander N, Bill RM (2012) Optimising yeast as a host for recombinant protein production. Methods Mol Biol 866:1–9PubMedGoogle Scholar
  17. Bonander N, Hedfalk K, Larsson C, Mostad P, Chang C, Gustafsson L, Bill RM (2005) Design of improved membrane protein production experiments: quantitation of the host response. Protein Sci 14:1729–1740PubMedCentralPubMedGoogle Scholar
  18. Bowie JU (2001) Stabilizing membrane proteins. Curr Opin Struct Biol 11:397–402PubMedGoogle Scholar
  19. Bowler MW, Guijarro M, Petitdemange S, Baker I, Svensson O, Burghammer M, Mueller-Dieckmann C, Gordon EJ, Flot D, McSweeney SM et al (2010) Diffraction cartography: applying microbeams to macromolecular crystallography sample evaluation and data collection. Acta Crystallogr Sect D Biol Crystallogr 66:855–864Google Scholar
  20. Breyton C, Chabaud E, Chaudier Y, Pucci B, Popot JL (2004) Hemifluorinated surfactants: a non-dissociating environment for handling membrane proteins in aqueous solutions? FEBS Lett 564:312–318PubMedGoogle Scholar
  21. Breyton C, Pucci B, Popot JL (2010) Amphipols and fluorinated surfactants: two alternatives to detergents for studying membrane proteins in vitro. Methods Mol Biol 601:219–245PubMedGoogle Scholar
  22. Brohawn SG, del Marmol J, MacKinnon R (2012) Crystal Structure of the Human K2P TRAAK, a Lipid- and Mechano-Sensitive K+ Ion Channel. Science 335:436–441Google Scholar
  23. Brohawn SG, Campbell EB, MacKinnon R (2013) Domain-swapped chain connectivity and gated membrane access in a Fab-mediated crystal of the human TRAAK K+ channel. Proceedings of the National Academy of Sciences of the United States of America 110:2129–2134Google Scholar
  24. Cady SD, Mishanina TV, Hong M (2009) Structure of amantadine-bound M2 transmembrane peptide of influenza A in lipid bilayers from magic-angle-spinning solid-state NMR: the role of Ser31 in amantadine binding. J Mol Biol 385:1127–1141PubMedCentralPubMedGoogle Scholar
  25. Cady SD, Schmidt-Rohr K, Wang J, Soto CS, DeGrado WF, Hong M (2010) Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463:689–692PubMedCentralPubMedGoogle Scholar
  26. Caffrey M, Cherezov V (2009) Crystallizing membrane proteins using lipidic mesophases. Nat Protoc 4:706–731PubMedCentralPubMedGoogle Scholar
  27. Catoire LJ, Damian M, Giusti F, Martin A, van Heijenoort C, Popot JL, Guittet E, Baneres JL (2010) Structure of a GPCR ligand in its receptor-bound state: leukotriene B4 adopts a highly constrained conformation when associated to human BLT2. J Am Chem Soc 132:9049–9057PubMedGoogle Scholar
  28. Chabaud E, Barthelemy P, Mora N, Popot JL, Pucci B (1998) Stabilization of integral membrane proteins in aqueous solution using fluorinated surfactants. Biochimie 80:515–530PubMedGoogle Scholar
  29. Chae PS, Rasmussen SGF, Rana RR, Gotfryd K, Chandra R, Goren MA, Kruse AC, Nurva S, Loland CJ, Pierre Y et al (2010) Maltose-neopentyl glycol (MNG) amphiphiles for solubilization, stabilization and crystallization of membrane proteins. Nat Methods 7:1003–1090PubMedCentralPubMedGoogle Scholar
  30. Chapman HN, Fromme P, Barty A, White TA, Kirian RA, Aquila A, Hunter MS, Schulz J, DePonte DP, Weierstall U et al (2011) Femtosecond X-ray protein nanocrystallography. Nature 470:73–81PubMedCentralPubMedGoogle Scholar
  31. Chayen NE (2005) Methods for separating nucleation and growth in protein crystallisation. Prog Biophys Mol Biol 88:329–337PubMedGoogle Scholar
  32. Chen R (2012) Bacterial expression systems for recombinant protein production: E. coli and beyond. Biotechnol Adv 30:1102–1107PubMedGoogle Scholar
  33. Cherezov V, Peddi A, Muthusubramaniam L, Zheng YF, Caffrey M (2004) A robotic system for crystallizing membrane and soluble proteins in lipidic mesophases. Acta Crystallogr D Biol Crystallogr 60:1795–1807Google Scholar
  34. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SGF, Thian FS, Kobilka TS, Choi HJ, Kuhn P, Weis WI, Kobilka BK et al (2007) High-resolution crystal structure of an engineered human beta(2)-adrenergic G protein-coupled receptor. Science 318:1258–1265PubMedCentralPubMedGoogle Scholar
  35. Chien EY, Liu W, Zhao Q, Katritch V, Han GW, Hanson MA, Shi L, Newman AH, Javitch JA, Cherezov V, Stevens RC (2010) Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist. Science 330:1091–1095PubMedCentralPubMedGoogle Scholar
  36. Chun E, Thompson AA, Liu W, Roth CB, Griffith MT, Katritch V, Kunken J, Xu F, Cherezov V, Hanson MA, Stevens RC (2012) Fusion partner toolchest for the stabilization and crystallization of G protein-coupled receptors. Structure 20:967–976PubMedCentralPubMedGoogle Scholar
  37. Condreay JP, Kost TA (2007) Baculovirus expression vectors for insect and mammalian cells. Curr Drug Targets 8:1126–1131PubMedGoogle Scholar
  38. Dahmane T, Damian M, Mary S et al (2009) Amphipol-assisted in vitro folding of G protein-coupled receptors. Biochemistry 48:6516–6521PubMedGoogle Scholar
  39. Dahmane T, Giusti F, Catoire LJ, Popot JL (2011) Sulfonated amphipols: synthesis, properties, and applications. Biopolymers 95:811–823PubMedGoogle Scholar
  40. Dawson RJ, Benz J, Stohler P, Tetaz T, Joseph C, Huber S, Schmid G, Hugin D, Pflimlin P, Trube G et al (2012) Structure of the acid-sensing ion channel 1 in complex with the gating modifier Psalmotoxin 1. Nat Commun 3Google Scholar
  41. De Angelis AA, Opella SJ (2007) Bicelle samples for solid-state NMR of membrane proteins. Nat Protoc 2:2332–2338PubMedGoogle Scholar
  42. De Angelis AA, Howell SC, Opella SJ (2006) Assigning solid-state NMR spectra of aligned proteins using isotropic chemical shifts. J Magn Reson 183:329–332PubMedGoogle Scholar
  43. Deniaud A, Liguori L, Blesneac I, Lenormand JL, Pebay-Peyroula E (2010) Crystallization of the membrane protein hVDAC1 produced in cell-free system. Biochim Biophys Acta: Biomembr 1798:1540–1546Google Scholar
  44. Deniaud A, Bernaudat F, Frelet-Barrand A, Juillan-Binard C, Vernet T et al. (2011) Expression of a chloroplast ATP/ADP transporter in E. coli membranes: behind the Mistic strategy. Biochim Biophys Acta 1808: 2059–2066PubMedGoogle Scholar
  45. Deupi X, Edwards P, Singhal A, Nickle B, Oprian D, Schertler G et al (2012) Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II. Proc Natl Acad Sci U S A 109:119–124PubMedCentralPubMedGoogle Scholar
  46. Dore AS, Robertson N, Errey JC, Ng I, Hollenstein K, Tehan B, Hurrell E, Bennett K, Congreve M, Magnani F et al (2011) Structure of the adenosine A(2A) receptor in complex with ZM241385 and the xanthines XAC and caffeine. Structure 19:1283–1293Google Scholar
  47. Egorova-Zachernyuk TA, Bosman G, DeGrip WJ (2011) Uniform stable-isotope labeling in mammalian cells: formulation of a cost-effective culture medium. Appl Microbiol Biotechnol 89:397–406PubMedGoogle Scholar
  48. El Moustaine D, Granier S, Doumazane E, Scholler P, Rahmeh R, Bron P, Mouillac B, Baneres JL, Rondard P, Pin JP (2012) Distinct roles of metabotropic glutamate receptor dimerization in agonist activation and G-protein coupling. Proc Natl Acad Sci U S A 109: 16342–16347PubMedCentralPubMedGoogle Scholar
  49. Etezady-Esfarjani T, Hiller S, Villalba C, Wuthrich K (2007) Cell-free protein synthesis of perdeuterated proteins for NMR studies. J Biomol NMR 39:229–238PubMedGoogle Scholar
  50. Faham S, Bowie JU (2002) Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure. J Mol Biol 316:1–6PubMedGoogle Scholar
  51. Fan Y, Shi LC, Ladizhansky V, Brown LS (2011) Uniform isotope labeling of a eukaryotic seven-transmembrane helical protein in yeast enables high-resolution solid-state NMR studies in the lipid environment. J Biomol NMR 49:151–161PubMedGoogle Scholar
  52. Fredriksson R, Lagerström MC, Lundin LG, Schiöth HB (2003) The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 63:1256–1272PubMedGoogle Scholar
  53. Freigassner M, Pichler H, Glieder A (2009) Tuning microbial hosts for membrane protein production. Microb Cell Fact 8:69PubMedCentralPubMedGoogle Scholar
  54. Frelet-Barrand A, Boutigny S, Kunji ERS, Rolland N (2010a) Membrane protein expression in Lactococcus lactis. Methods Mol Biol 601:67–85Google Scholar
  55. Frelet-Barrand A, Boutigny S, Moyet L, Deniaud A, Seigneurin-Berny D et al (2010b) Lactococcus lactis, an alternative system for functional expression of peripheral and intrinsic Arabidopsis membrane proteins. PLoS ONE 7(3):e32325Google Scholar
  56. Gonzales EB, Kawate T, Gouaux E (2009) Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 460:599–604Google Scholar
  57. Goto NK, Gardner KH, Mueller GA, Willis RC, Kay LE (1999) A robust and cost-effective method for the production of Val, Leu, Ile (delta 1) methyl-protonated N-15-, C-13-, H-2-labeled proteins. J Biomol NMR 13:369–374PubMedGoogle Scholar
  58. Granier S, Manglik A, Kruse AC, Kobilka TS, Thian FS, Weis WI, Kobilka BK (2012) Structure of the δ-opioid receptor bound to naltrindole. Nature 485:400–404PubMedCentralPubMedGoogle Scholar
  59. Gruswitz F, Chaudhary S, Ho JD, Schlessinger A, Pezeshki B, Ho CM et al (2010) Function of human Rh based on structure of RhCG at 2.1 A. Proc Natl Acad Sci U S A 107:9638–9643PubMedCentralPubMedGoogle Scholar
  60. Haga K, Kruse AC, Asada H, Yurugi-Kobayashi T, Shiroishi M, Zhang C, Weis WI, Okada T, Kobilka BK, Haga T, Kobayashi T (2012) Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist. Nature 482:547–551PubMedCentralPubMedGoogle Scholar
  61. Hagn F, Etzkorn M, Raschle T, Wagner G (2013) Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J Am Chem Soc 135:1919–1925PubMedCentralPubMedGoogle Scholar
  62. Hamers-Casterman C, Atarhouch T, Muyldermans S, Robinson G, Hamers C, Songa EB, Bendahman N, Hamers R (1993) Naturally occurring antibodies devoid of light chains. Nature 3636428:446–448Google Scholar
  63. Hansen SB, Tao X, MacKinnon R (2011) Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature 477:495–498Google Scholar
  64. Hanson MA, Roth CB, Jo E, Griffith MT, Scott FL, Reinhart G, Desale H, Clemons B, Cahalan SM, Schuerer SC, Sanna MG, Han GW, Kuhn P, Rosen H, Stevens RC (2012) Crystal structure of a lipid G protein-coupled receptor. Science 335:851–855PubMedCentralPubMedGoogle Scholar
  65. Hefke F, Bagaria A, Reckel S, Ullrich S, Dötsch V, Glaubitz C, Güntert P (2011) Optimization of amino acid type-specific 13C and 15N labeling for the backbone assignment of membrane proteins by solution- and solid-state NMR with the UPLABEL algorithm. J Biomol NMR 49:75–84PubMedGoogle Scholar
  66. Hiller S, Garces RG, Malia TJ, Orekhov VY, Colombini M, Wagner G (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321:1206–1210PubMedCentralPubMedGoogle Scholar
  67. Hilty C, Fernandez C, Wider G, Wuthrich K (2002) Side chain NMR assignments in the membrane protein OmpX reconstituted in DHPC micelles. J Biomol NMR 23:289–301PubMedGoogle Scholar
  68. Hino T, Arakawa T, Iwanari H, Yurugi-Kobayashi T, Ikeda-Suno C, Nakada-Nakura Y, Kusano-Arai O, Weyand S, Shimamura T, Nomura N, Cameron AD, Kobayashi T, Hamakubo T, Iwata S, Murata T (2012) G-protein-coupled receptor inactivation by an allosteric inverse-agonist antibody. Nature 482:237–240PubMedCentralPubMedGoogle Scholar
  69. Hiroaki Y, Tani K, Kamegawa A, Gyobu N, Nishikawa K, Suzuki H, Walz T, Sasaki S, Mitsuoka K, Kimura K, et al (2006) Implications of the aquaporin-4 structure on array formation and cell adhesion. J Mol Biol 355:628–639Google Scholar
  70. Holton JM (2009) A beginner’s guide to radiation damage. J Synchrotron Radiat 16:133–142PubMedCentralPubMedGoogle Scholar
  71. Horsefield R, Norden K, Fellert M, Backmark A, Tornroth-Horsefield S, van Scheltinga ACT, Kvassman J, Kjellbom P, Johanson U, Neutze R (2008) High-resolution x-ray structure of human aquaporin 5. Proceedings of the National Academy of Sciences of the United States of America 105:13327–13332Google Scholar
  72. Hovers J, Potschies M, Polidori A, Pucci B, Raynal S, Bonneté F, Serrano-Vega MJ, Tate CG, Picot D, Pierre Y, Popot JL, Nehmé R, Bidet M, Mus-Veteau I, Busskamp H, Jung KH, Marx A, Timmins PA, Welte W (2011) A class of mild surfactants that keep integral membrane proteins water-soluble for functional studies and crystallization. Mol Membr Biol 28:171–181PubMedGoogle Scholar
  73. Imai S, Osawa M, Takeuchi K, Shimada I (2010) Structural basis underlying the dual gate properties of KcsA. Proc Natl Acad Sci U S A 107: 6216–6221PubMedCentralPubMedGoogle Scholar
  74. Jaakola VP, Griffith MT, Hanson MA, Cherezov V, Chien EY, Lane JR, Ijzerman AP, Stevens, RC (2008) The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322:1211–1217Google Scholar
  75. Jarvis DL, Finn EE (1995) Biochemical analysis of the N-glycosylation pathway in baculovirus-infected lepidopteran insect cells. Virology 212:500–511PubMedGoogle Scholar
  76. Jasti J, Furukawa H, Gonzales EB, Gouaux E (2007) Structure of acid-sensing ion channel 1 at 1.9A resolution and low pH. Nature 449:316-+Google Scholar
  77. Jidenko M, Nielsen RC, Sorensen TL et al (2005) Crystallization of a mammalian membrane protein overexpressed in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 102:11687–11691PubMedCentralPubMedGoogle Scholar
  78. Junge F, Schneider B, Reckel S, Schwarz D, Dötsch V et al (2008) Large-scale production of functional membrane proteins. Cell Mol Life Sci 65:1729–1755PubMedGoogle Scholar
  79. Junge F, Luh LM, Proverbio D, Schäfer B, Abele R, Beyermann M, Dötsch V, Bernhard F (2010) Modulation of G-protein coupled receptor sample quality by modified cell-free expression protocols: a case study of the human endothelin A receptor. J Struct Biol 172 :94–106PubMedGoogle Scholar
  80. Kainosho M, Torizawa T, Iwashita Y, Terauchi T, Mei Ono A, Güntert P (2006) Optimal isotope labelling for NMR protein structure determinations. Nature 440:52–57PubMedGoogle Scholar
  81. Kang HJ, Lee C, Drew D (2013) Breaking the barriers in membrane protein crystallography. Int J Biochem Cell Biol 45:636–644PubMedGoogle Scholar
  82. Kijac AZ, Li Y, Sligar SG, Rienstra CM (2007) Magic-angle spinning solid-state NMR spectroscopy of nanodisc-embedded human CYP3A4. Biochemistry 46:13696–13703PubMedCentralPubMedGoogle Scholar
  83. Kim HJ, Howell SC, Van Horn WD, Jeon YH, Sanders CR (2009) Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins. Prog Nucl Magn Reson Spectrosc 55:335–360PubMedCentralPubMedGoogle Scholar
  84. Kim TH, Chung KY, Manglik A, Hansen AL, Dror RO, Mildorf TJ, Shaw DE, Kobilka BK, Prosser RS (2013) The role of ligands on the equilibria between functional states of a G protein-coupled receptor. J Am Chem Soc 135:9465–9474PubMedCentralPubMedGoogle Scholar
  85. Konrat R, Yang DW, Kay LE (1999) A 4D TROSY-based pulse scheme for correlating (HNi)-H-1,Ni-15,C-13(i)alpha, C-13ʹ(i−1) chemical shifts in high molecular weight, N-15,C-13, H-2 labeled proteins. J Biomol NMR 15:309–313PubMedGoogle Scholar
  86. Kruse AC, Hu J, Pan AC, Arlow DH, Rosenbaum DM, Rosemond E, Green HF, Liu T, Chae PS, Dror RO, Shaw DE, Weis WI, Wess J, Kobilka BK (2012) Structure and dynamics of the M3 muscarinic acetylcholine receptor. Nature 482:552–556PubMedCentralPubMedGoogle Scholar
  87. Landau EM, Rosenbusch JP (1996) Lipidic cubic phases: a novel concept for the crystallization of membrane proteins. Proc Natl Acad Sci U S A 93: 14532–14535PubMedCentralPubMedGoogle Scholar
  88. Lau FW, Nauli S, Zhou Y, Bowie JU (1999) Changing single side-chains can greatly enhance the resistance of a membrane protein to irreversible inactivation. J Mol Biol 290:559–564PubMedGoogle Scholar
  89. Lebon G, Warne T, Edwards PC, Bennett K, Langmead CJ, Leslie AG, Tate CG (2011) Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature 474:521–525PubMedCentralPubMedGoogle Scholar
  90. Levin EJ, Cao Y, Enkavi G, Quick M, Pan Y, Tajkhorshid E, Zhou M (2012) Structure and permeation mechanism of a mammalian urea transporter. Proc Natl Acad Sci USA 109:11194–11199Google Scholar
  91. Liu J, Rost B (2001) Comparing function and structure between entire proteomes. Protein Sci 10:1970–1979PubMedCentralPubMedGoogle Scholar
  92. Liu W, Chun E, Thompson AA, Chubukov P, Xu F, Katritch V, Han GW, Roth CB, Heitman LH, IJzerman AP, Cherezov V, Stevens RC (2012a) Structural basis for allosteric regulation of GPCRs by sodium ions. Science 337:232–236Google Scholar
  93. Liu JJ, Horst R, Katritch V, Stevens RC, Wuthrich K (2012b) Biased signaling pathways in beta(2)-adrenergic receptor characterized by F-19-NMR. Science 335:1106–1110Google Scholar
  94. Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309:897–903PubMedGoogle Scholar
  95. Long SB, Tao X, Campbell EB, MacKinnon R (2007) Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450:376–382Google Scholar
  96. Lundstrom K (2006) Structural genomics for membrane proteins. Cell Mol Life Sci 63:2597–2607PubMedGoogle Scholar
  97. Ma Y, Muench D, Schneider T, Sahl HG, Bouhss A, Ghoshdastider U, Wang J, Doetsch V, Wang X, Bernhard F (2011) Preparative scale cell-free production and quality optimization of MraY homologues in different expression modes. J Biol Chem 286:38844–38853PubMedCentralPubMedGoogle Scholar
  98. Manglik A, Kruse AC, Kobilka TS, Thian FS, Mathiesen JM, Sunahara RK, Pardo L, Weis WI, Kobilka BK, Granier S (2012) Crystal structure of the µ-opioid receptor bound to a morphinan antagonist. Nature 485:321–326PubMedCentralPubMedGoogle Scholar
  99. Maslennikov I, Klammt C, Hwang E, Kefala G, Okamura M, Esquivies L, Mors K, Glaubitz C, Kwiatkowski W, Jeon YH et al. (2010) Membrane domain structures of three classes of histidine kinase receptors by cell-free expression and rapid NMR analysis. Proc Natl Acad Sci U S A 107: 10902–10907PubMedCentralPubMedGoogle Scholar
  100. Maslennikov I, Choe S (2013) Advances in NMR structures of integral membrane proteins. Current Opinion in Structural Biology 23:555–562Google Scholar
  101. Matthies D, Haberstock S, Joos F, Dötsch V, Vonck J, Bernhard F, Meier T (2011) Cell-free expression and assembly of ATP synthase. J Mol Biol 413 :593–603PubMedGoogle Scholar
  102. Miller AN, Long SB (2012) Crystal structure of the human two-pore domain potassium channel K2P1. Science 335:432–436Google Scholar
  103. Mineev KS, Bocharov EV, Pustovalova YE, Bocharova OV, Chupin VV, Arseniev AS (2010) Spatial structure of the transmembrane domain heterodimer of ErbB1 and ErbB2 receptor tyrosine kinases. J Mol Biol 400:231–243PubMedGoogle Scholar
  104. Miroux B, Walker JE (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260:289–298PubMedGoogle Scholar
  105. Moukhametzianov R, Burghammer M, Edwards PC, Petitdemange S, Popov D, Fransen M, McMullan G, Schertler GF, Riekel C (2008) Protein crystallography with a micrometre-sized synchrotron-radiation beam. Acta Crystallogr D Biol Crystallogr 64:158–166Google Scholar
  106. Moukhametzianov R, Warne T, Edwards PC, Serrano-Vega MJ, Leslie AG, Tate CG, Schertler GF (2011) Two distinct conformations of helix 6 observed in antagonist-bound structures of a beta1-adrenergic receptor. Proc Natl Acad Sci USA 108:8228–8232Google Scholar
  107. Mus-Veteau I (2010) Heterologous expression of membrane proteins for structural analysis. Methods Mol Biol 601: 1–16. (In Mus-Veteau (Ed.) Methods in molecular biology, heterologous expression of membrane proteins: methods and protocols, Humana Press)Google Scholar
  108. Muyldermans S (2001) Single domain camel antibodies: current status. J Biotechnol 74:277–302PubMedGoogle Scholar
  109. Nehme R, Joubert O, Bidet M, Lacombe B, Polidori A, Pucci B, Mus-Veteau I (2010) Stability study of the human G-protein coupled receptor, Smoothened. Biochim Biophys Acta 1798: 1100–1110PubMedGoogle Scholar
  110. Oxenoid K, Chou JJ (2005) The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proc Natl Acad Sci USA 102:10870–10875Google Scholar
  111. Nietlispach D, Gautier A (2011) Solution NMR studies of polytopic alpha-helical membrane proteins. Current Opinion in Structural Biology 21:497–508Google Scholar
  112. Palczewski K, Kumasaka T, Hori T et al (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739–745PubMedGoogle Scholar
  113. Park KH, Berrier C, Lebaupain F, Pucci B, Popot JL, Ghazi A, Zito F (2007) Fluorinated and hemifluorinated surfactants as alternatives to detergents for membrane protein cell-free synthesis. Biochem J 403:183–187PubMedCentralPubMedGoogle Scholar
  114. Park KH, Billon-Denis E, Dahmane T, Lebaupain F, Pucci B, Breyton C, Zito F (2011) In the cauldron of cell-free synthesis of membrane proteins: playing with new surfactants. Nat Biotechnol 28:255–261Google Scholar
  115. Park SH, Das BB, Casagrande F, Tian Y, Nothnagel HJ, Chu M, Kiefer H, Maier K, De Angelis AA, Marassi FM et al (2012) Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491:779–783PubMedCentralPubMedGoogle Scholar
  116. Parker JL, Newstead S (2012) Current trends in α-helical membrane protein crystallization: an update. Protein Sci 21:1358–1365PubMedCentralPubMedGoogle Scholar
  117. Pavia AA, Pucci B, Riess JG, Zarif L (1992) New perfluoro alkylated telomeric non ionic surfactants synthesis physicochemical and biological properties. Makromol Chem 193:2505–2517Google Scholar
  118. Periasamy A, Shadiac N, Amalraj A, Garajova S, Nagarajan Y, Waters S, Mertens HDT, Hrmova M (2012) Cell-free synthesis of membrane (1,3)-β-d-glucan (curdlan) synthase: co-translational insertion in liposomes and reconstitution in nanodiscs. Biochim Biophys Acta: Biomembr 1828:743–757Google Scholar
  119. Popot JL, Althoff T, Bagnard D, Baneres JL, Bazzacco P, Billon-Denis E, Catoire LJ, Champeil P, Charvolin D, Cocco MJ et al. (2011) Amphipols From A to Z. Annu Rev Biophys 40:379–408 (Rees DC, Dill KA, Williamson JR, eds.)Google Scholar
  120. Prive GG (2007) Detergents for the stabilization and crystallization of membrane proteins. Methods 41:388–397PubMedGoogle Scholar
  121. Quigley A, Dong YY, Pike AC, Dong L, Shrestha L, Berridge G, Stansfeld PJ, Sansom MS, Edwards AM, Bountra C et al (2013) The structural basis of ZMPSTE24-dependent laminopathies. Science 339:1604–1607Google Scholar
  122. Qureshi T, Goto NK (2012) Contemporary methods in structure determination of membrane proteins by solution NMR. In Zhu G (ed) NMR of proteins and small biomolecules. Springer, Heidelberg, pp 123–185Google Scholar
  123. Rahmeh R, Damian M, Cottet M, Orcel H, Mendre C, Durroux T, Sharma KS, Durand G, Pucci B, Trinquet E, Zwier JM, Deupi X, Bron P, Banères JL, Mouillac B, Granier S (2012) Structural insights into biased G protein-coupled receptor signaling revealed by fluorescence spectroscopy. Proc Natl Acad Sci U S A 109:6733–6738PubMedCentralPubMedGoogle Scholar
  124. Raschle T, Hiller S, Yu T-Y, Rice AJ, Walz T, Wagner G (2009) Structural and functional characterization of the integral membrane protein VDAC-1 in lipid bilayer nanodiscs. J Am Chem Soc 131:17777–17779PubMedCentralPubMedGoogle Scholar
  125. Rasmussen SG, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC, Burghammer M, Ratnala VRP, Sanishvili R, Fischetti RF et al (2007) Crystal structure of the human beta(2) adrenergic G-protein-coupled receptor. Nature 450:383–384PubMedGoogle Scholar
  126. Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D, Mathiesen JM, Shah ST, Lyons JA, Caffrey M, Gellman SH, Steyaert J, Skiniotis G, Weis WI, Sunahara RK, Kobilka BK (2011) Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477:549–555PubMedCentralPubMedGoogle Scholar
  127. Religa TL, Sprangers R, Kay LE (2010) Dynamic regulation of archaeal proteasome gate opening as studied by TROSY NMR. Science 328:98–102PubMedGoogle Scholar
  128. Renault M, Saurel O, Czaplicki J, Demange P, Gervais V, Lohr F, Reat V, Piotto M, Milon A (2009) Solution state NMR structure and dynamics of KpOmpA, a 210 residue transmembrane domain possessing a high potential for immunological applications. J Mol Biol 385:117–130PubMedGoogle Scholar
  129. Renault M, Cukkemane A, Baldus M (2010) Solid-state NMR spectroscopy on complex biomolecules. Angew Chem Int Ed 49:8346–8357Google Scholar
  130. Ritchie TK, Grinkova YV, Bayburt TH, Denisov IG, Zolnerciks JK, Atkins WM, Sligar SG (2009) Chapter 11 Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. In: Nejat D (ed) Methods in Enzymology, vol 464. Academic, Waltham, pp 211–231Google Scholar
  131. Rodnin MV, Posokhov YO, Contino-Pepin C, Brettmann J, Kyrychenko A, Palchevskyy SS, Pucci B, Ladokhin AS (2008) Interactions of fluorinated surfactants with diphtheria toxin T-domain: testing new media for studies of membrane proteins. Biophys J 94:4348–4357PubMedCentralPubMedGoogle Scholar
  132. Roos C, Zocher M, Müller D, Münch D, Schneider T, Sahl HG, Scholz F, Wachtveitl J, Ma Y, Proverbio D et al. (2012) Characterization of co-translationally formed nanodisc complexes with small multidrug transporters, proteorhodopsin and with the E. coli MraY translocase. Biochim Biophys Acta: Biomembr 1818:3098–3106Google Scholar
  133. Roosild TP, Greenwald J, Vega M, Castronovo S, Riek R et al (2005) NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science 307:1317–1321PubMedGoogle Scholar
  134. Rosenbaum DM, Zhang C, Lyons JA, Holl R, Aragao D, Arlow DH, Rasmussen SG, Choi HJ, Devree BT, Sunahara RK, et al (2011) Structure and function of an irreversible agonist-beta(2) adrenoceptor complex. Nature 469:236–240Google Scholar
  135. Ruschak AM, Religa TL, Breuer S, Witt S, Kay LE (2010) The proteasome antechamber maintains substrates in an unfolded state. Nature 467:868–871PubMedGoogle Scholar
  136. Sahdev S, Khattar SK, Saini KS (2008) Production of active eukaryotic proteins through bacterial expression systems: a review of the existing biotechnology strategies. Mol Cell Biochem 307:249–264PubMedGoogle Scholar
  137. Salzmann M, Wider G, Pervushin K, Wuthrich K (1999) Improved sensitivity and coherence selection for [15N,1H]-TROSY elements in triple resonance experiments. J Biomol NMR 15:181–184PubMedGoogle Scholar
  138. Sanders CR, Sonnichsen F (2006) Solution NMR of membrane proteins: practice and challenges. Magn Reson Chem 44:S24–S40PubMedGoogle Scholar
  139. Sarramegna V, Talmont R, Demange P, Milon A (2003) Heterologous expression of G-protein-coupled receptors: comparison of expression systems from the standpoint of large-scale production and purification. Cell Mol Life Sci 60:1529–1546PubMedGoogle Scholar
  140. Schlegel S, Löfblom J, Lee C, Hjelm A, Klepsch M, Strous M, Drew D, Slotboom DJ, de Gier J-W (2012) Optimizing membrane protein overexpression in the Escherichia coli strain Lemo21(DE3). J Mol Biol 423:648–659PubMedGoogle Scholar
  141. Shahid SA, Bardiaux B, Franks WT, Krabben L, Habeck M, van Rossum B-J, Linke D (2012) Membrane-protein structure determination by solid-state NMR spectroscopy of microcrystals. Nat Methods 9:1212–1217PubMedGoogle Scholar
  142. Sharma M, Yi M, Dong H, Qin H, Peterson E, Busath DD, Zhou H-X, Cross TA (2010) Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer. Science 330:509–512PubMedCentralPubMedGoogle Scholar
  143. Shenkarev ZO, Paramonov AS, Lyukmanova EN, Shingarova LN, Yakimov SA, Dubinnyi MA, Chupin VV, Kirpichnikov MP, Blommers MJJ, Arseniev AS (2010) NMR structural and dynamical investigation of the isolated voltage-sensing domain of the potassium channel KvAP: implications for voltage gating. J Am Chem Soc 132:5630–5637PubMedGoogle Scholar
  144. Shenkarev ZO, Paramonov AS, Lyukmanova EN, Gizatullina AK, Zhuravleva AV, Tagaev AA, Yakimenko ZA, Telezhinskaya IN, Kirpichnikov MP, Ovchinnikova TV et al (2013) Peptaibol antiamoebin I: spatial structure, backbone dynamics, interaction with bicelles and lipid-protein nanodiscs, and pore formation in context of barrel-stave model. Chem Biodivers 10:838–863PubMedGoogle Scholar
  145. Shi P, Wang H, Xi Z, Shi C, Xiong Y, Tian C (2011) Site-specific 19F NMR chemical shift and side chain relaxation analysis of a membrane protein labeled with an unnatural amino acid. Protein Sci 20:224–228PubMedCentralPubMedGoogle Scholar
  146. Shi P, Li D, Chen H, Xiong Y, Wang Y, Tian C (2012) In situ 19F NMR studies of an E. coli membrane protein. Protein Sci 21:596–600PubMedCentralPubMedGoogle Scholar
  147. Shibata Y, Gvozdenovic-Jeremic J, Love J, Kloss B, White JF, Grisshammer R, Tate CG (2013) Optimising the combination of thermostabilising mutations in the neurotensin receptor for structure determination. Biochim Biophys Acta 1828:1293–1301PubMedCentralPubMedGoogle Scholar
  148. Shimamura T, Shiroishi M, Weyand S, Tsujimoto H, Winter G, Katritch V, Abagyan R, Cherezov V, Liu W, Han GW, Kobayashi T, Stevens RC, Iwata S (2011) Structure of the human histamine H1 receptor complex with doxepin. Nature 475:65–70PubMedCentralPubMedGoogle Scholar
  149. Shintre CA, Pike ACW, Li Q, Kim JI, Barr AJ, Goubin S, Shrestha L, Yang J, Berridge G, Ross J et al (2013) Structures of ABCB10, a human ATP-binding cassette transporter in apo- and nucleotide-bound states. Proceedings of the National Academy of Sciences of the USA 110:9710–9715Google Scholar
  150. Sobhanifar S, Reckel S, Junge F, Schwarz D, Kai L, Karbyshev M, Lohr F, Bernhard F, Dotsch V (2010a) Cell-free expression and stable isotope labelling strategies for membrane proteins. J Biomol NMR 46:33–43Google Scholar
  151. Sobhanifar S, Schneider B, Löhr F, Gottstein D, Ikeya T, Mlynarcyk K, Pulawski W, Ghoshdastider U, Kolinski M et al. (2010b) Structural investigation of the C-terminal catalytic fragment of presenilin 1. Proc Natl Acad Sci U S A 107:9644–9649Google Scholar
  152. Sobolevsky AI, Rosconi MP, Gouaux E (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462:745–756Google Scholar
  153. Standfuss J, Xie G, Edwards PC, Burghammer M, Oprian DD, Schertler GF (2007) Crystal structure of a thermally stable rhodopsin mutant. J Mol Biol 372:1179–1188PubMedCentralPubMedGoogle Scholar
  154. Standfuss J, Edwards PC, D’Antona A, Fransen M, Xie G, Oprian DD et al (2011) The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471:656–660PubMedCentralPubMedGoogle Scholar
  155. Steyaert J, Kobilka BK (2011) Nanobody stabilization of G protein-coupled receptor conformational states. Curr Opin Struct Biol 21:567–572PubMedCentralPubMedGoogle Scholar
  156. Stock D, Leslie AG, Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286:1700–1705PubMedGoogle Scholar
  157. Tani K, Mitsuma T, Hiroaki Y, Kamegawa A, Nishikawa K, Tanimura Y, Fujiyoshi Y (2009) Mechanism of aquaporin-4’s fast and highly selective water conduction and proton exclusion. J Mol Biol 389:694–706Google Scholar
  158. Talbot JC, Dautant A, Polidori A, Pucci B, Cohen-Bouhacina T, Maali A, Salin B, Brèthes D, Velours J, Giraud MF (2009) Hydrogenated and fluorinated surfactants derived from Tris (hydroxymethyl)-acrylamidomethane allow the purification of a highly active yeast F1-F0 ATP-synthase with an enhanced stability. J Bioenerg Biomembr 41:349–360PubMedGoogle Scholar
  159. Tate CG (2010) Practical considerations of membrane protein instability during purification and crystallisation. Methods Mol Biol 601:187–203PubMedGoogle Scholar
  160. Tate CG, Whiteley E, Betenbaugh MJ (1999) Molecular chaperones stimulate the functional expression of the cocaine-sensitive serotonin transporter. J Biol Chem 274:17551–17558PubMedGoogle Scholar
  161. Tate CG, Haase J, Baker C, Boorsma M, Magnani F et al (2003) Comparison of seven different heterologous protein expression systems for the production of the serotonin transporter. Biochim Biophys Acta 1610:141–153PubMedGoogle Scholar
  162. Tate CG (2012) A crystal clear solution for determining G-protein-coupled receptor structures. Trends Biochem Sci 37:343–352Google Scholar
  163. Tao X, Avalos JL, Chen J, MacKinnon R (2009) Crystal structure of the eukaryotic strong inward-rectifier K+ channel Kir2.2 at 3.1 A resolution. Science 326:1668–1674Google Scholar
  164. Tao X, Le A, Limapichat W, Dougherty DA, MacKinnon R (2010) A gating charge transfer center in voltage sensors. Science 328:67–73Google Scholar
  165. Thompson AA, Liu JJ, Chun E, Wacker D, Wu H, Cherezov V, Stevens RC (2011) GPCR stabilization using the bicelle-like architecture of mixed sterol-detergent micelles. Methods 55:310–317PubMedCentralPubMedGoogle Scholar
  166. Thompson AA, Liu W, Chun E, Katritch V, Wu H, Vardy E, Huang XP, Trapella C, Guerrini R, Calo G, Roth BL, Cherezov V, Stevens RC (2012) Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic. Nature 485:395–399PubMedCentralPubMedGoogle Scholar
  167. Toyoshima C, Nakasako M, Nomura H, Ogawa H (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405:647–655PubMedGoogle Scholar
  168. Traaseth NJ, Shi L, Verardi R, Mullen DG, Barany G, Veglia G (2009) Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach. Proc Natl Acad Sci 106:10165–10170PubMedCentralPubMedGoogle Scholar
  169. Tribet C, Audebert R, Popot J-L (1996) Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc Natl Acad Sci U S A 93:15047–15050PubMedCentralPubMedGoogle Scholar
  170. Ujwal R, Bowie JU (2011) Crystallizing membrane proteins using lipidic bicelles. Methods 55:337–341PubMedCentralPubMedGoogle Scholar
  171. Unnerståle S, Mäler L, Draheim RR (2011) Structural characterization of AS1-membrane interactions from a subset of HAMP domains. Biochim Biophys Acta: Biomembr 1808:2403–2412Google Scholar
  172. Unwin N (2005) Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution. J Mol Biol 346:967–989PubMedGoogle Scholar
  173. Vaiphei ST, Tang Y, Montelione G, Inouye M (2011) The use of the condensed single protein production system for isotope-labeled outer membrane proteins, OmpA and OmpX in E. coli. Mol Biotechnol 47:205–210PubMedCentralPubMedGoogle Scholar
  174. Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF, Babu MM (2013) Molecular signatures of G-protein-coupled receptors. Nature 494:185–194PubMedGoogle Scholar
  175. Verardi R, Shi L, Traaseth NJ, Walsh N, Veglia G (2011) Structural topology of phospholamban pentamer in lipid bilayers by a hybrid solution and solid-state NMR method. Proc Natl Acad Sci U S A 108:9101–9106PubMedCentralPubMedGoogle Scholar
  176. Wacker D, Wang C, Katritch V, Han GW, Huang XP, Vardy E, McCorvy JD, Jiang Y, Chu M, Siu FY, Liu W, Xu HE, Cherezov V, Roth BL, Stevens RC (2013) Structural features for functional selectivity at serotonin receptors. Science 340:615–619PubMedCentralPubMedGoogle Scholar
  177. Wada T, Shimono K, Kikukawa T, Hato M, Shinya N, Kim SY, Kimura-Someya T, Shirouzu M, Tamogami J, Miyauchi S et al (2011) Crystal structure of the eukaryotic light-driven proton-pumping rhodopsin, Acetabularia rhodopsin II, from marine alga. J Mol Biol 411:986–998PubMedGoogle Scholar
  178. Wang C, Wu H, Katritch V, Han GW, Huang XP, Liu W, Siu FY, Roth BL, Cherezov V, Stevens RC (2013) Structure of the human smoothened receptor bound to an antitumour agent. Nature 497:338–343PubMedCentralPubMedGoogle Scholar
  179. Warne T, Serrano-Vega MJ, Baker JG, Moukhametzianov R, Edwards PC, Henderson R, Leslie AG, Tate CG, Schertler GF (2008) Structure of a beta1-adrenergic G-protein-coupled receptor. Nature 454:486–491PubMedCentralPubMedGoogle Scholar
  180. Warne T, Moukhametzianov R, Baker JG, Nehmé R, Edwards PC, Leslie AG, Schertler GF, Tate CG (2011) The structural basis for agonist and partial agonist action on a β(1)-adrenergic receptor. Nature 469:241–244PubMedCentralPubMedGoogle Scholar
  181. Warne T, Edwards PC, Leslie AG, Tate CG (2012) Crystal structures of a stabilized β1-adrenoceptor bound to the biased agonists bucindolol and carvedilol. Structure 20:841–849PubMedGoogle Scholar
  182. Warschawski DE, Arnold AA, Beaugrand M, Gravel A, Chartrand E, Marcotte I (2011) Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim Biophys Acta: Biomembr 1808:1957–1974Google Scholar
  183. White JF, Noinaj N, Shibata Y, Love J, Kloss B, Xu F, Gvozdenovic-Jeremic J, Shah P, Shiloach J, Tate CG, Grisshammer R (2012) Structure of the agonist-bound neurotensin receptor. Nature 490:508–513PubMedCentralPubMedGoogle Scholar
  184. Whorton MR, MacKinnon R (2011) Crystal Structure of the Mammalian GIRK2 K+ Channel and Gating Regulation by G Proteins, PIP2, and Sodium. Cell 147:199–208Google Scholar
  185. Whorton MR, MacKinnon R (2013) X-ray structure of the mammalian GIRK2-betagamma G-protein complex. Nature 498:190–197Google Scholar
  186. Wu B, Chien EY, Mol CD, Fenalti G, Liu W, Katritch V, Abagyan R, Brooun A, Wells P, Bi FC, Hamel DJ, Kuhn P, Handel TM, Cherezov V, Stevens RC (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330:1066–1071PubMedCentralPubMedGoogle Scholar
  187. Wu H, Wacker D, Mileni M, Katritch V, Han GW, Vardy E, Liu W, Thompson AA, Huang XP, Carroll FI, Mascarella SW, Westkaemper RB, Mosier PD, Roth BL, Cherezov V, Stevens RC (2012) Structure of the human κ-opioid receptor in complex with JDTic. Nature 485:327–332PubMedCentralPubMedGoogle Scholar
  188. Xie G, Timasheff SN (1997) The thermodynamic mechanism of protein stabilization by trehalose. Biophys Chem 64:25–43PubMedGoogle Scholar
  189. Xu F, Stevens RC (2011) Trapping small caffeine in a large GPCR pocket. Structure 19:1204–1207Google Scholar
  190. Xu Y, Kong J, Kong W (2013) Improved membrane protein expression in Lactococcus lactis by fusion to Mistic. Microbiology 159:1002–1009PubMedGoogle Scholar
  191. Yang DW, Kay LE (1999) Improved lineshape and sensitivity in the HNCO-family of triple resonance experiments. J Biomol NMR 14:273–276Google Scholar
  192. Zhang C, Srinivasan Y, Arlow DH, Fung JJ, Palmer D, Zheng Y, Green HF, Pandey A, Dror RO, Shaw DE et al (2012) High-resolution crystal structure of human protease-activated receptor 1. Nature 492:387–392Google Scholar
  193. Zhang QH, Ma XQ, Ward A, Hong WX, Jaakola VP, Stevens RC, Finn MG, Chang G (2007) Designing facial amphiphiles for the stabilization of integral membrane proteins. Angew Chem Int Ed 46:7023–7025Google Scholar
  194. Zhou Y, Bowie JU (2000) Building a thermostable membrane protein. J Biol Chem 275:6975–6979PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Isabelle Mus-Veteau
    • 1
  • Pascal Demange
    • 2
  • Francesca Zito
    • 3
  1. 1.Institute for Molecular and Cellular PharmacologyUMR-CNRS 7275, University of Nice-Sophia AntipolisValbonneFrance
  2. 2.Institute of Pharmacology and Structural BiologyUMR-CNRS 5089, Université de ToulouseToulouseFrance
  3. 3.Laboratory of Physico-Chemical Biology of Membrane Proteins, UMR-CNRS 7099Institute of Physico-Chemical Biology, and Université Paris DiderotParisFrance

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