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Nanotechnology Reviews

Editor-in-Chief: Kumar, Challa

Ed. by Hamblin, Michael R. / Bianco, Alberto / Jin, Rongchao / Köhler, J. Michael / Hudait, Mantu K. / Dai, Ning / Lytton-Jean, Abigail / Xie, Jianping / Bryan, Lynn A. / Thiessen, Rose / Alexiou, Christoph / Lee, Jae-Seung / Delville, Marie-Helene / Yan, Ning / Baretzky, Brigitte / Burg, Thomas P. / Fenniri, Hicham / Yang, Jun / Hosmane, Narayan S. / Dufrene, Yves / Podila, Ramakrishna / Eswaramoorthy, Muthusamy

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Volume 6, Issue 1

Issues

Membrane mimetics for solution NMR studies of membrane proteins

Konstantin S. MineevORCID iD: http://orcid.org/0000-0002-2418-9421 / Kirill D. Nadezhdin
  • Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Structural Biology, Mikluho-Maklaya Str, 16/10, Moscow 117997, Russian Federation
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2016-12-20 | DOI: https://doi.org/10.1515/ntrev-2016-0074

Abstract

Membrane proteins are one of the most challenging and attractive objects in modern structural biology, as they are targets for the majority of medicines. However, studies of membrane proteins are hindered by several obstacles, including their low ability to crystallize, highly dynamic behavior of some of their domains, and need for membrane-like environment. Although solution nuclear magnetic resonance (NMR) is a very powerful technique of structural biology in terms of the amount of provided data, it imposes several limitations on the object under investigation, with the main constraint being related to the size of the object. For this reason, the membrane mimetic has to form particles of small size and simultaneously to properly simulate the bilayer membrane to be applicable for solution NMR spectroscopy. Here we review the recent advances in the field of membrane mimetics for solution NMR studies, discuss the advantages and drawbacks of specific membrane-like environments, and formulate the criteria for the selection of proper environment for a particular membrane protein or domain.

Keywords: bicelles; membrane mimetics; micelles; nanodiscs; NMR

References

  • [1]

    Wallin E, von Heijne G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 1998, 7, 1029–1038.Google Scholar

  • [2]

    Arinaminpathy Y, Khurana E, Engelman DM, Gerstein MB. Computational analysis of membrane proteins: the largest class of drug targets. Drug Discov. Today 2009, 14, 1130–1135.Google Scholar

  • [3]

    Quast RB, Sonnabend A, Stech M, Wüstenhagen DA, Kubick S. High-yield cell-free synthesis of human EGFR by IRES-mediated protein translation in a continuous exchange cell-free reaction format. Sci. Rep. 2016, 6, 30399.Google Scholar

  • [4]

    Meissner A, Sorensen OW. Optimization of three-dimensional TROSY-type HCCH NMR correlation of aromatic (1)H-(13)C groups in proteins. J. Magn. Reson. 1999, 139, 447–450.Google Scholar

  • [5]

    Tugarinov V, Hwang PM, Kay LE. Nuclear magnetic resonance spectroscopy of high-molecular-weight proteins. Ann. Rev. Biochem. 2004, 73, 107–146.Google Scholar

  • [6]

    Pervushin K, Riek R, Wider G, Wüthrich K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. USA 1997, 94, 12366–12371.Google Scholar

  • [7]

    Tugarinov V, Hwang PM, Ollerenshaw JE, Kay LE. Cross-correlated relaxation enhanced 1H[bond]13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. J. Am. Chem. Soc. 2003, 125, 10420–10428.Google Scholar

  • [8]

    Kainosho M, Torizawa T, Iwashita Y, Terauchi T, Mei Ono A, Güntert P. Optimal isotope labelling for NMR protein structure determinations. Nature 2006, 440, 52–57.Google Scholar

  • [9]

    Miyanoiri Y, Ishida Y, Takeda M, Terauchi T, Inouye M, Kainosho M. Highly efficient residue-selective labeling with isotope-labeled Ile, Leu, and Val using a new auxotrophic E. coli strain. J. Biomol. NMR. 2016, 65, 109–119.Google Scholar

  • [10]

    Ruschak AM, Kay LE. Methyl groups as probes of supra-molecular structure, dynamics and function. J. Biomol. NMR. 2010, 46, 75–87.Google Scholar

  • [11]

    Velyvis A, Ruschak AM, Kay LE. An economical method for production of 2H,13CH3-threonine for solution NMR studies of large protein complexes: application to the 670 kDa proteasome. PLoS One 2012, 7, e43725.Google Scholar

  • [12]

    Clark L, Zahm JA, Ali R, Kukula M, Bian L, Patrie SM, Gardner KH, Rosen MK, Rosenbaum DM. Methyl labeling and TROSY NMR spectroscopy of proteins expressed in the eukaryote Pichia pastoris. J. Biomol. NMR. 2015, 62, 239–245.Google Scholar

  • [13]

    Rosen MK, Gardner KH, Willis RC, Parris WE, Pawson T, Kay LE. Selective methyl group protonation of perdeuterated proteins. J. Mol. Biol. 1996, 263, 627–636.Google Scholar

  • [14]

    Tugarinov V, Kay LE. Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods. J. Am. Chem. Soc. 2003, 125, 13868–13878.Google Scholar

  • [15]

    Religa TL, Sprangers R, Kay LE. Dynamic regulation of archaeal proteasome gate opening as studied by TROSY NMR. Science 2010, 328, 98–102.Google Scholar

  • [16]

    Fernández C, Wüthrich K. NMR solution structure determination of membrane proteins reconstituted in detergent micelles. FEBS Lett. 2003, 555, 144–150.Google Scholar

  • [17]

    Dürr UHN, Gildenberg M, Ramamoorthy A. The magic of bicelles lights up membrane protein structure. Chem. Rev. 2012, 112, 6054–6074.Google Scholar

  • [18]

    Dürr UHN, Soong R, Ramamoorthy A. When detergent meets bilayer: birth and coming of age of lipid bicelles. Prog. Nucl. Magn. Reson. Spectrosc. 2013, 69, 1–22.Google Scholar

  • [19]

    Poget SF, Girvin ME. Solution NMR of membrane proteins in bilayer mimics: small is beautiful, but sometimes bigger is better. Biochim. Biophys. Acta 2007, 1768, 3098–3106.Google Scholar

  • [20]

    Malhotra K, Alder NN. Advances in the use of nanoscale bilayers to study membrane protein structure and function. Biotechnol. Genet. Eng. Rev. 2014, 30, 79–93.Google Scholar

  • [21]

    Warschawski DE, Arnold AA, Beaugrand M, Gravel A, Chartrand É, Marcotte I. Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim. Biophys. Acta 2011, 1808, 1957–1974.Google Scholar

  • [22]

    Mäler L. Solution NMR studies of peptide-lipid interactions in model membranes. Mol. Membr. Biol. 2012, 29, 155–176.Google Scholar

  • [23]

    Raschle T, Hiller S, Etzkorn M, Wagner G. Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Curr. Opin. Struct. Biol. 2010, 20, 471–479.Google Scholar

  • [24]

    Sanders CR, Sönnichsen F. Solution NMR of membrane proteins: practice and challenges. Magn. Reson. Chem. 2006, 44, S24–S40.Google Scholar

  • [25]

    Gayen S, Li Q, Kang C. Solution NMR study of the transmembrane domain of single-span membrane proteins: opportunities and strategies. Curr. Protein Pept. Sci. 2012, 13, 585–600.Google Scholar

  • [26]

    Liang B, Tamm LK. NMR as a tool to investigate the structure, dynamics and function of membrane proteins. Nat. Struct. Mol. Biol. 2016, 23, 468–474.Google Scholar

  • [27]

    Barsukov IL, Nolde DE, Lomize AL, Arseniev AS. Three-dimensional structure of proteolytic fragment 163-231 of bacterioopsin determined from nuclear magnetic resonance data in solution. Eur. J. Biochem. 1992, 206, 665–672.Google Scholar

  • [28]

    Pervushin KV, Orekhov VYu null, Popov AI, Musina LYu null, Arseniev AS. Three-dimensional structure of (1-71)bacterioopsin solubilized in methanol/chloroform and SDS micelles determined by 15N-1H heteronuclear NMR spectroscopy. Eur. J. Biochem. 1994, 219, 571–583.Google Scholar

  • [29]

    Grabchuk IA, Orekhov VY, Musina LY, Arseniev AS. 1H-15N NMR signal assignment and the secondary structure of bacteriorhodopsin(1-231) in solution. Bioorg. Khim. 1997, 23, 616–629.Google Scholar

  • [30]

    Girvin ME, Rastogi VK, Abildgaard F, Markley JL, Fillingame RH. Solution structure of the transmembrane H+-transporting subunit c of the F1F0 ATP synthase. Biochemistry 1998, 37, 8817–8824.Google Scholar

  • [31]

    Mineev KS, Lyukmanova EN, Krabben L, Serebryakova MV, Shulepko MA, Arseniev AS, Kordyukova LV, Veit M. Structural investigation of influenza virus hemagglutinin membrane-anchoring peptide. Protein Eng. Des. Sel. 2013, 26, 547–552.Google Scholar

  • [32]

    Cohen LS, Arshava B, Neumoin A, Becker JM, Güntert P, Zerbe O, Naider F. Comparative NMR analysis of an 80-residue G protein-coupled receptor fragment in two membrane mimetic environments. Biochim. Biophys. Acta 2011, 1808, 2674–2684.Google Scholar

  • [33]

    Mortishire-Smith RJ, Pitzenberger SM, Burke CJ, Middaugh CR, Garsky VM, Johnson RG. Solution structure of the cytoplasmic domain of phopholamban: phosphorylation leads to a local perturbation in secondary structure. Biochemistry 1995, 34, 7603–7613.Google Scholar

  • [34]

    Jung H, Windhaber R, Palm D, Schnackerz KD. NMR and circular dichroism studies of synthetic peptides derived from the third intracellular loop of the beta-adrenoceptor. FEBS Lett. 1995, 358, 133–136.Google Scholar

  • [35]

    Shenkarev ZO, Finkina EI, Nurmukhamedova EK, Balandin SV, Mineev KS, Nadezhdin KD, Yakimenko ZA, Tagaev AA, Temirov YV, Arseniev AS, Ovchinnikova TV. Isolation, structure elucidation, and synergistic antibacterial activity of a novel two-component lantibiotic lichenicidin from Bacillus licheniformis VK21. Biochemistry 2010, 49, 6462–6472.Google Scholar

  • [36]

    Tulumello DV, Deber CM. Efficiency of detergents at maintaining membrane protein structures in their biologically relevant forms. Biochim. Biophys. Acta 2012, 1818, 1351–1358.Google Scholar

  • [37]

    Arseniev AS, Barsukov IL, Bystrov VF, Lomize AL, Ovchinnikov YA. 1H-NMR study of gramicidin A transmembrane ion channel: head-to-head right-handed, single-stranded helices. FEBS Lett. 1985, 186, 168–174.Google Scholar

  • [38]

    Lomize AL, Pervushin KV, Arseniev AS. Spatial structure of (34–65)bacterioopsin polypeptide in SDS micelles determined from nuclear magnetic resonance data. J. Biomol. NMR. 1992, 2, 361–372.Google Scholar

  • [39]

    Pervushin K, Sobol A, Musina L, Abdulaeva G, Arsenev A. Spatial structure of (1-36)bacterioopsin in methanol-chloroform and SDS micelles. Mol. Biol. 1992, 26, 920–933.Google Scholar

  • [40]

    Chill JH, Louis JM, Baber JL, Bax A. Measurement of 15N relaxation in the detergent-solubilized tetrameric KcsA potassium channel. J. Biomol. NMR. 2006, 36, 123–136.Google Scholar

  • [41]

    Chill JH, Louis JM, Miller C, Bax A. NMR study of the tetrameric KcsA potassium channel in detergent micelles. Protein Sci. 2006, 15, 684–698.Google Scholar

  • [42]

    Chill JH, Louis JM, Delaglio F, Bax A. Local and global structure of the monomeric subunit of the potassium channel KcsA probed by NMR. Biochim. Biophys. Acta 2007, 1768, 3260–3270.Google Scholar

  • [43]

    Krishnamani V, Hegde BG, Langen R, Lanyi JK. Secondary and Tertiary Structure of Bacteriorhodopsin in the SDS Denatured State. Biochemistry 2012, 51, 1051–1060.Google Scholar

  • [44]

    Gong X-M, Ding Y, Yu J, Yao Y, Marassi FM. Structure of the Na,K-ATPase regulatory protein FXYD2b in micelles: implications for membrane-water interfacial arginines. Biochim. Biophys. Acta 2015, 1848, 299–306.Google Scholar

  • [45]

    Li Y, Surya W, Claudine S, Torres J. Structure of a conserved Golgi complex-targeting signal in coronavirus envelope proteins. J. Biol. Chem. 2014, 289, 12535–12549.Google Scholar

  • [46]

    Miyamoto K, Togiya K. Solution structure of LC4 transmembrane segment of CCR5. PLoS One 2011, 6, e20452.Google Scholar

  • [47]

    Schubert M, Kolbe M, Kessler B, Oesterhelt D, Schmieder P. Heteronuclear multidimensional nmr spectroscopy of solubilized membrane proteins: resonance assignment of native bacteriorhodopsin. ChemBioChem 2002, 3, 1019–1023.Google Scholar

  • [48]

    Etzkorn M, Raschle T, Hagn F, Gelev V, Rice AJ, Walz T, Wagner G. Cell-free expressed bacteriorhodopsin in different soluble membrane mimetics: biophysical properties and NMR accessibility. Structure 2013, 21, 394–401.Google Scholar

  • [49]

    Isogai S, Deupi X, Opitz C, Heydenreich FM, Tsai C-J, Brueckner F, Schertler GFX, Veprintsev DB, Grzesiek S. Backbone NMR reveals allosteric signal transduction networks in the β1-adrenergic receptor. Nature 2016, 530, 237–241.Google Scholar

  • [50]

    Nygaard R, Zou Y, Dror RO, Mildorf TJ, Arlow DH, Manglik A, Pan AC, Liu CW, Fung JJ, Bokoch MP, Thian FS, Kobilka TS, Shaw DE, Mueller L, Prosser RS, Kobilka BK. The dynamic process of β2-adrenergic receptor activation. Cell 2013, 152, 532–542.Google Scholar

  • [51]

    Stehle J, Silvers R, Werner K, Chatterjee D, Gande S, Scholz F, Dutta A, Wachtveitl J, Klein-Seetharaman J, Schwalbe H. Characterization of the simultaneous decay kinetics of metarhodopsin states II and III in rhodopsin by solution-state NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 2014, 53, 2078–2084.Google Scholar

  • [52]

    Ozawa S, Kimura T, Nozaki T, Harada H, Shimada I, Osawa M. Structural basis for the inhibition of voltage-dependent K+ channel by gating modifier toxin. Sci. Rep. 2015, 5, 14226.Google Scholar

  • [53]

    Horst R, Liu JJ, Stevens RC, Wüthrich K. β2-Adrenergic receptor activation by agonists studied with 19F NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 2013, 52, 10762–10765.Google Scholar

  • [54]

    Thompson AA, Liu JJ, Chun E, Wacker D, Wu H, Cherezov V, Stevens RC. GPCR stabilization using the bicelle-like architecture of mixed sterol-detergent micelles. Methods 2011, 55, 310–317.Google Scholar

  • [55]

    Hagn F, Etzkorn M, Raschle T, Wagner G. Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J. Am. Chem. Soc. 2013, 135, 1919–1925.Google Scholar

  • [56]

    MacKenzie KR, Prestegard JH, Engelman DM. A transmembrane helix dimer: structure and implications. Science 1997, 276, 131–133.Google Scholar

  • [57]

    Hiller S, Garces RG, Malia TJ, Orekhov VY, Colombini M, Wagner G. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 2008, 321, 1206–1210.Google Scholar

  • [58]

    Sulistijo ES, Mackenzie KR. Structural basis for dimerization of the BNIP3 transmembrane domain. Biochemistry 2009, 48, 5106–5120.Google Scholar

  • [59]

    Bocharov EV, Lesovoy DM, Pavlov KV, Pustovalova YE, Bocharova OV, Arseniev AS. Alternative packing of EGFR transmembrane domain suggests that protein-lipid interactions underlie signal conduction across membrane. Biochim. Biophys. Acta 2016, 1858, 1254–1261.Google Scholar

  • [60]

    Shenkarev Z, Paramonov A, Lyukmanova E, Shingarova L, Yakimov S, Dubinnyi M, Chupin V, Kirpichnikov M, Blommers M, Arseniev A. NMR structural and dynamical investigation of the isolated voltage-sensing domain of the potassium channel KvAP: implications for voltage gating. J. Am. Chem. Soc. 2010, 132, 5630–5637.Google Scholar

  • [61]

    Mineev KS, Khabibullina NF, Lyukmanova EN, Dolgikh DA, Kirpichnikov MP, Arseniev AS. Spatial structure and dimer – monomer equilibrium of the ErbB3 transmembrane domain in DPC micelles. Biochim. Biophys. Acta 2011, 1808, 2081–2088.Google Scholar

  • [62]

    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. Proc. Natl. Acad. Sci. 2008, 105, 15370–15375.Google Scholar

  • [63]

    Van Horn WD, Kim H-J, Ellis CD, Hadziselimovic A, Sulistijo ES, Karra MD, Tian C, Sonnichsen FD, Sanders CR. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 2009, 324, 1726–1729.Google Scholar

  • [64]

    Arora A, Abildgaard F, Bushweller JH, Tamm LK. Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat. Struct. Biol. 2001, 8, 334–338.Google Scholar

  • [65]

    Bocharov EV, Lesovoy DM, Goncharuk SA, Goncharuk MV, Hristova K, Arseniev AS. Structure of FGFR3 transmembrane domain dimer: implications for signaling and human pathologies. Structure 2013, 21, 2087–2093.Google Scholar

  • [66]

    Nadezhdin KD, García-Carpio I, Goncharuk SA, Mineev KS, Arseniev AS, Vilar M. Structural basis of p75 transmembrane domain dimerization. J. Biol. Chem. 2016, 291, 12346–12357.Google Scholar

  • [67]

    Bondarenko V, Mowrey D, Tillman T, Cui T, Liu LT, Xu Y, Tang P. NMR structures of the transmembrane domains of the α4β2 nAChR. Biochim. Biophys. Acta 2012, 1818, 1261–1268.Google Scholar

  • [68]

    Mowrey DD, Liu Q, Bondarenko V, Chen Q, Seyoum E, Xu Y, Wu J, Tang P. Insights into distinct modulation of α7 and α7β2 nicotinic acetylcholine receptors by the volatile anesthetic isoflurane. J. Biol. Chem. 2013, 288, 35793–35800.Google Scholar

  • [69]

    Yu L, Sun C, Song D, Shen J, Xu N, Gunasekera A, Hajduk PJ, Olejniczak ET. Nuclear magnetic resonance structural studies of a potassium channel-charybdotoxin complex. Biochemistry 2005, 44, 15834–15841.Google Scholar

  • [70]

    Zhou Y, Cierpicki T, Jimenez RHF, Lukasik SM, Ellena JF, Cafiso DS, Kadokura H, Beckwith J, Bushweller JH. NMR solution structure of the integral membrane enzyme DsbB: functional insights into DsbB-catalyzed disulfide bond formation. Mol. Cell 2008, 31, 896–908.Google Scholar

  • [71]

    Liang B, Tamm LK. Structure of outer membrane protein G by solution NMR spectroscopy. Proc. Natl. Acad. Sci. USA 2007, 104, 16140–16145.Google Scholar

  • [72]

    Zhang Q, Horst R, Geralt M, Ma X, Hong W-X, Finn MG, Stevens RC. Microscale NMR screening of new detergents for membrane protein structural biology. J. Am. Chem. Soc. 2008, 130, 7357–7363.Google Scholar

  • [73]

    Stanczak P, Zhang Q, Horst R, Serrano P, Wüthrich K. Micro-coil NMR to monitor optimization of the reconstitution conditions for the integral membrane protein OmpW in detergent micelles. J. Biomol. NMR. 2012, 54, 129–133.Google Scholar

  • [74]

    Horst R, Stanczak P, Wüthrich K. NMR polypeptide backbone conformation of the E. coli outer membrane protein W. Structure 2014, 22, 1204–1209.Google Scholar

  • [75]

    Marassi FM, Ding Y, Schwieters CD, Tian Y, Yao Y. Backbone structure of Yersinia pestis Ail determined in micelles by NMR-restrained simulated annealing with implicit membrane solvation. J. Biomol. NMR. 2015, 63, 59–65.Google Scholar

  • [76]

    Krueger-Koplin RD, Sorgen PL, Krueger-Koplin ST, Rivera-Torres IO, Cahill SM, Hicks DB, Grinius L, Krulwich TA, Girvin ME. An evaluation of detergents for NMR structural studies of membrane proteins. J. Biomol. NMR. 2004, 28, 43–57.Google Scholar

  • [77]

    Maslennikov I, Klammt C, Hwang E, Kefala G, Okamura M, Esquivies L, Mörs K, Glaubitz C, Kwiatkowski W, Jeon YH, Choe S. Membrane domain structures of three classes of histidine kinase receptors by cell-free expression and rapid NMR analysis. Proc. Natl. Acad. Sci. USA 2010, 107, 10902–10907.Google Scholar

  • [78]

    Zhuang T, Jap BK, Sanders CR. Solution NMR approaches for establishing specificity of weak heterodimerization of membrane proteins. J. Am. Chem. Soc. 2011, 133, 20571–20580.Google Scholar

  • [79]

    Barrett PJ, Song Y, Van Horn WD, Hustedt EJ, Schafer JM, Hadziselimovic A, Beel AJ, Sanders CR. The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 2012, 336, 1168–1171.Google Scholar

  • [80]

    Shenkarev ZO, Lyukmanova EN, Paramonov AS, Shingarova LN, Chupin VV, Kirpichnikov MP, Blommers MJJ, Arseniev AS. Lipid-protein nanodiscs as reference medium in detergent screening for high-resolution NMR studies of integral membrane proteins. J. Am. Chem. Soc 2010, 132, 5628–5629.Google Scholar

  • [81]

    Gautier A, Mott HR, Bostock MJ, Kirkpatrick JP, Nietlispach D. Structure determination of the seven-helix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat. Struct. Mol. Biol. 2010, 17, 768–774.Google Scholar

  • [82]

    Reckel S, Gottstein D, Stehle J, Löhr F, Verhoefen M-K, Takeda M, Silvers R, Kainosho M, Glaubitz C, Wachtveitl J, Bernhard F, Schwalbe H, Güntert P, Dötsch V. Solution NMR Structure of Proteorhodopsin. Angew. Chem. Int. Ed. 2011, 50, 11942–11946.Google Scholar

  • [83]

    Butterwick JA, MacKinnon R. Solution structure and phospholipid interactions of the isolated voltage-sensor domain from KvAP. J. Mol. Biol. 2010, 403, 591–606.Google Scholar

  • [84]

    Renault M, Saurel O, Czaplicki J, Demange P, Gervais V, Löhr F, Réat V, Piotto M, Milon A. Solution state NMR structure and dynamics of KpOmpA, a 210 residue transmembrane domain possessing a high potential for immunological applications. J. Mol. Biol. 2009, 385, 117–130.Google Scholar

  • [85]

    Fernández C, Hilty C, Wider G, Güntert P, Wüthrich K. NMR structure of the integral membrane protein OmpX. J. Mol. Biol. 2004, 336, 1211–1221.Google Scholar

  • [86]

    Edrington TC, Kintz E, Goldberg JB, Tamm LK. Structural basis for the interaction of lipopolysaccharide with outer membrane protein H (OprH) from Pseudomonas aeruginosa. J. Biol. Chem. 2011, 286, 39211–39223.Google Scholar

  • [87]

    Kucharska I, Seelheim P, Edrington T, Liang B, Tamm LK. OprG harnesses the dynamics of its extracellular loops to transport small amino acids across the outer membrane of Pseudomonas aeruginosa. Structure 2015, 23, 2234–2245.Google Scholar

  • [88]

    Kucharska I, Liang B, Ursini N, Tamm LK. Molecular Interactions of lipopolysaccharide with an outer membrane protein from Pseudomonas aeruginosa probed by solution NMR. Biochemistry 2016, 55, 5061–5072.Google Scholar

  • [89]

    Columbus L, Lipfert J, Jambunathan K, Fox DA, Sim AYL, Doniach S, Lesley SA. Mixing and matching detergents for membrane protein NMR structure determination. J. Am. Chem. Soc. 2009, 131, 7320–7326.Google Scholar

  • [90]

    Eichmann C, Tzitzilonis C, Bordignon E, Maslennikov I, Choe S, Riek R. Solution NMR structure and functional analysis of the integral membrane protein YgaP from Escherichia coli. J. Biol. Chem. 2014, 289, 23482–23503.Google Scholar

  • [91]

    Eichmann C, Tzitzilonis C, Nakamura T, Kwiatkowski W, Maslennikov I, Choe S, Lipton SA, Riek R. S-nitrosylation induces structural and dynamical changes in a Rhodanese family protein. J. Mol. Biol. 2016, 428, 3737–3751.Google Scholar

  • [92]

    Call ME, Schnell JR, Xu C, Lutz RA, Chou JJ, Wucherpfennig KW. The structure of the ζζ transmembrane dimer reveals features essential for its assembly with the T cell receptor. Cell 2006, 127, 355–368.Google Scholar

  • [93]

    Call ME, Wucherpfennig KW, Chou JJ. The structural basis for intramembrane assembly of an activating immunoreceptor complex. Nature Immunol. 2010, 11, 1023–1029.Google Scholar

  • [94]

    Lyukmanova EN, Shenkarev ZO, Khabibullina NF, Kopeina GS, Shulepko MA, Paramonov AS, Mineev KS, Tikhonov RV, Shingarova LN, Petrovskaya LE, Dolgikh DA, Arseniev AS, Kirpichnikov MP. Lipid-protein nanodiscs for cell-free production of integral membrane proteins in a soluble and folded state: comparison with detergent micelles, bicelles and liposomes. Biochim. Biophys. Acta 2012, 1818, 349–358.Google Scholar

  • [95]

    Glover KJ, Whiles JA, Wu G, Yu N, Deems R, Struppe JO, Stark RE, Komives EA, Vold RR. Structural evaluation of phospholipid bicelles for solution-state studies of membrane-associated biomolecules. Biophys. J. 2001, 81, 2163–2171.Google Scholar

  • [96]

    Lee D, Walter KFA, Brückner A-K, Hilty C, Becker S, Griesinger C. Bilayer in small bicelles revealed by lipid-protein interactions using NMR spectroscopy. J. Am. Chem. Soc. 2008, 130, 13822–13823.Google Scholar

  • [97]

    Chou JJ, Baber JL, Bax A. Characterization of phospholipid mixed micelles by translational diffusion. J. Biomol. NMR. 2004, 29, 299–308.Google Scholar

  • [98]

    Lind J, Nordin J, Mäler L. Lipid dynamics in fast-tumbling bicelles with varying bilayer thickness: effect of model transmembrane peptides. Biochim. Biophys. Acta 2008, 1778, 2526–2534.Google Scholar

  • [99]

    Mineev KS, Nadezhdin KD, Goncharuk SA, Arseniev AS. Characterization of small isotropic bicelles with various compositions. Langmuir 2016, 32, 6624–6637.Google Scholar

  • [100]

    Struppe J, Whiles JA, Vold RR. Acidic phospholipid bicelles: a versatile model membrane system. Biophys. J. 2000, 78, 281–289.Google Scholar

  • [101]

    Marcotte I, Dufourc EJ, Ouellet M, Auger M. Interaction of the neuropeptide met-enkephalin with zwitterionic and negatively charged bicelles as viewed by 31P and 2H solid-state NMR. Biophys. J. 2003, 85, 328–339.Google Scholar

  • [102]

    Barbosa-Barros L, de la Maza A, López-Iglesias C, López O. Ceramide effects in the bicelle structure. Colloids Surf. A Physicochem. Eng. Asp. 2008, 317, 576–584.Google Scholar

  • [103]

    Ye W, Liebau J, Mäler L. New membrane mimetics with galactolipids: lipid properties in fast-tumbling bicelles. J. Phys. Chem. B. 2013, 117, 1044–1050.Google Scholar

  • [104]

    Liebau J, Pettersson P, Zuber P, Ariöz C, Mäler L. Fast-tumbling bicelles constructed from native Escherichia coli lipids. Biochim. Biophys. Acta 2016, 1858, 2097–2105.Google Scholar

  • [105]

    Sasaki H, Fukuzawa S, Kikuchi J, Yokoyama S, Hirota H, Tachibana K. Cholesterol doping induced enhanced stability of bicelles. Langmuir 2003, 19, 9841–9844.Google Scholar

  • [106]

    Gayen A, Mukhopadhyay C. Evidence for effect of GM1 on opioid peptide conformation: NMR study on leucine enkephalin in ganglioside-containing isotropic phospholipid bicelles. Langmuir 2008, 24, 5422–5432.Google Scholar

  • [107]

    Gayen A, Goswami SK, Mukhopadhyay C. NMR evidence of GM1-induced conformational change of Substance P using isotropic bicelles. Biochim. Biophys. Acta 2011, 1808, 127–139.Google Scholar

  • [108]

    Yamaguchi T, Uno T, Uekusa Y, Yagi-Utsumi M, Kato K. Ganglioside-embedding small bicelles for probing membrane-landing processes of intrinsically disordered proteins. Chem. Commun. (Camb.) 2013, 49, 1235–1237.Google Scholar

  • [109]

    Cavagnero S, Dyson HJ, Wright PE. Improved low pH bicelle system for orienting macromolecules over a wide temperature range. J. Biomol. NMR. 1999, 13, 387–391.Google Scholar

  • [110]

    Sanders CR, Schwonek JP. Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry 1992, 31, 8898–8905.Google Scholar

  • [111]

    Gabriel NE, Roberts MF. Interaction of short-chain lecithin with long-chain phospholipids: characterization of vesicles that form spontaneously. Biochemistry 1986, 25, 2812–2821.Google Scholar

  • [112]

    Gabriel NE, Roberts MF. Spontaneous formation of stable unilamellar vesicles. Biochemistry 1984, 23, 4011–4015.Google Scholar

  • [113]

    Sanders CR, Prestegard JH. Magnetically orientable phospholipid bilayers containing small amounts of a bile salt analogue, CHAPSO. Biophys. J. 1990, 58, 447–460.Google Scholar

  • [114]

    Lee SC, Bennett BC, Hong W-X, Fu Y, Baker KA, Marcoux J, Robinson CV, Ward AB, Halpert JR, Stevens RC, Stout CD, Yeager MJ, Zhang Q. Steroid-based facial amphiphiles for stabilization and crystallization of membrane proteins. Proc. Natl. Acad. Sci. USA 2013, 110, e1203–1211.Google Scholar

  • [115]

    Morgado L, Zeth K, Burmann BM, Maier T, Hiller S. Characterization of the insertase BamA in three different membrane mimetics by solution NMR spectroscopy. J. Biomol. NMR. 2015, 61, 333–345.Google Scholar

  • [116]

    Matsui R, Ohtani M, Yamada K, Hikima T, Takata M, Nakamura T, Koshino H, Ishida Y, Aida T. Chemically locked bicelles with high thermal and kinetic stability. Angew. Chem. Int. Ed. 2015, 54, 13284–13288.Google Scholar

  • [117]

    Triba MN, Warschawski DE, Devaux PF. Reinvestigation by phosphorus NMR of lipid distribution in bicelles. Biophys. J. 2005, 88, 1887–1901.Google Scholar

  • [118]

    Beaugrand M, Arnold AA, Hénin J, Warschawski DE, Williamson PTF, Marcotte I. Lipid concentration and molar ratio boundaries for the use of isotropic bicelles. Langmuir 2014, 30, 6162–6170.Google Scholar

  • [119]

    Ye W, Lind J, Eriksson J, Mäler L. Characterization of the morphology of fast-tumbling bicelles with varying composition. Langmuir 2014, 30, 5488–5496.Google Scholar

  • [120]

    Li M, Morales HH, Katsaras J, Kučerka N, Yang Y, Macdonald PM, Nieh M-P. Morphological characterization of DMPC/CHAPSO bicellar mixtures: a combined SANS and NMR study. Langmuir 2013, 29, 15943–15957.Google Scholar

  • [121]

    Park SH, Prytulla S, De Angelis AA, Brown JM, Kiefer H, Opella SJ. High-resolution NMR spectroscopy of a GPCR in aligned bicelles. J. Am. Chem. Soc. 2006, 128, 7402–7403.Google Scholar

  • [122]

    Prosser RS, Evanics F, Kitevski JL, Al-Abdul-Wahid MS. Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins. Biochemistry 2006, 45, 8453–8465.Google Scholar

  • [123]

    Poget SF, Cahill SM, Girvin ME. Isotropic bicelles stabilize the functional form of a small multidrug-resistance pump for NMR structural studies. J. Am. Chem. Soc. 2007, 129, 2432–2433.Google Scholar

  • [124]

    Bocharov EV, Pustovalova YE, Pavlov KV, Volynsky PE, Goncharuk MV, Ermolyuk YS, Karpunin DV, Schulga AA, Kirpichnikov MP, Efremov RG, Maslennikov IV, Arseniev AS. Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger. J. Biol. Chem. 2007, 282, 16256–16266.Google Scholar

  • [125]

    Mineev KS, Bocharov EV, Pustovalova YE, Bocharova OV, Chupin VV, Arseniev AS. Spatial structure of the transmembrane domain heterodimer of ErbB1 and ErbB2 receptor tyrosine kinases. J. Mol. Biol. 2010, 400, 231–243.Google Scholar

  • [126]

    Bocharov EV, Mineev KS, Volynsky PE, Ermolyuk YS, Tkach EN, Sobol AG, Chupin VV, Kirpichnikov MP, Efremov RG, Arseniev AS. 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, 6950–6956.Google Scholar

  • [127]

    Bocharov EV, Mineev KS, Goncharuk MV, Arseniev AS. Structural and thermodynamic insight into the process of “weak” dimerization of the ErbB4 transmembrane domain by solution NMR. Biochim. Biophys. Acta 2012, 1818, 2158–2170.Google Scholar

  • [128]

    Bocharov EV, Mayzel ML, Volynsky PE, Mineev KS, Tkach EN, Ermolyuk YS, Schulga AA, Efremov RG, Arseniev AS. Left-handed dimer of EphA2 transmembrane domain: helix packing diversity among receptor tyrosine kinases. Biophys. J 2010, 98, 881–889.Google Scholar

  • [129]

    Bocharov EV, Mayzel ML, Volynsky PE, Goncharuk MV, Ermolyuk YS, Schulga AA, Artemenko EO, Efremov RG, Arseniev AS. Spatial structure and pH-dependent conformational diversity of dimeric transmembrane domain of the receptor tyrosine kinase EphA1. J. Biol. Chem. 2008, 283, 29385–29395.Google Scholar

  • [130]

    Lau T-L, Kim C, Ginsberg MH, Ulmer TS. The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling. EMBO J. 2009, 28, 1351–1361.Google Scholar

  • [131]

    Endres NF, Das R, Smith AW, Arkhipov A, Kovacs E, Huang Y, Pelton JG, Shan Y, Shaw DE, Wemmer DE, Groves JT, Kuriyan J. Conformational coupling across the plasma membrane in activation of the EGF receptor. Cell 2013, 152, 543–556.Google Scholar

  • [132]

    Schmidt T, Ye F, Situ AJ, An W, Ginsberg MH, Ulmer TS. A Conserved ectodomain-transmembrane domain linker motif tunes the allosteric regulation of cell surface receptors. J. Biol. Chem. 2016, 291, 17536–17546.Google Scholar

  • [133]

    Liu Y, Kahn RA, Prestegard JH. Dynamic structure of membrane-anchored Arf*GTP. Nat. Struct. Mol. Biol. 2010, 17, 876–881.Google Scholar

  • [134]

    Zhang M, Huang R, Im S-C, Waskell L, Ramamoorthy A. Effects of membrane mimetics on cytochrome P450-cytochrome b5 interactions characterized by NMR spectroscopy. J. Biol. Chem. 2015, 290, 12705–12718.Google Scholar

  • [135]

    Poget SF, Harris R, Cahill SM, Girvin ME. 1H, 13C, 15N backbone NMR assignments of the Staphylococcus aureus small multidrug-resistance pump (Smr) in a functionally active conformation. Biomol. NMR Assign. 2010, 4, 139–142.Google Scholar

  • [136]

    Dev J, Park D, Fu Q, Chen J, Ha HJ, Ghantous F, Herrmann T, Chang W, Liu Z, Frey G, Seaman MS, Chen B, Chou JJ. Structural basis for membrane anchoring of HIV-1 envelope spike. Science 2016, 353, 172–175.Google Scholar

  • [137]

    Denisov IG, Grinkova YV, Lazarides AA, Sligar SG. Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size. J. Am. Chem. Soc. 2004, 126, 3477–3487.Google Scholar

  • [138]

    Midtgaard SR, Pedersen MC, Kirkensgaard JJK, Sørensen KK, Mortensen K, Jensen KJ, Arleth L. Self-assembling peptides form nanodiscs that stabilize membrane proteins. Soft Matter 2014, 10, 738–752.Google Scholar

  • [139]

    Kondo H, Ikeda K, Nakano M. Formation of size-controlled, denaturation-resistant lipid nanodiscs by an amphiphilic self-polymerizing peptide. Colloids Surf. B. Biointerfaces 2016, 146, 423–430.Google Scholar

  • [140]

    Denisov IG, McLean MA, Shaw AW, Grinkova YV, Sligar SG. Thermotropic phase transition in soluble nanoscale lipid bilayers. J. Phys. Chem. B. 2005, 109, 15580–15588.Google Scholar

  • [141]

    Nakano M, Fukuda M, Kudo T, Miyazaki M, Wada Y, Matsuzaki N, Endo H, Handa T. Static and dynamic properties of phospholipid bilayer nanodiscs. J. Am. Chem. Soc. 2009, 131, 8308–8312.Google Scholar

  • [142]

    Stepien P, Polit A, Wisniewska-Becker A. Comparative EPR studies on lipid bilayer properties in nanodiscs and liposomes. Biochim. Biophys. Acta 2015, 1848, 60–66.Google Scholar

  • [143]

    Mörs K, Roos C, Scholz F, Wachtveitl J, Dötsch V, Bernhard F, Glaubitz C. Modified lipid and protein dynamics in nanodiscs. Biochim. Biophys. Acta 2013, 1828, 1222–1229.Google Scholar

  • [144]

    Dörr JM, Koorengevel MC, Schäfer M, Prokofyev AV, Scheidelaar S, van der Cruijsen EAW, Dafforn TR, Baldus M, Killian JA. Detergent-free isolation, characterization, and functional reconstitution of a tetrameric K+ channel: the power of native nanodiscs. Proc. Natl. Acad. Sci. USA 2014, 111, 18607–18612.Google Scholar

  • [145]

    Lyukmanova EN, Shenkarev ZO, Paramonov AS, Sobol AG, Ovchinnikova TV, Chupin VV, Kirpichnikov MP, Blommers MJJ, Arseniev AS. Lipid-protein nanoscale bilayers: a versatile medium for NMR investigations of membrane proteins and membrane-active peptides. J. Am. Chem. Soc. 2008, 130, 2140–2141.Google Scholar

  • [146]

    Shenkarev ZO, Paramonov AS, Lyukmanova EN, Gizatullina AK, Zhuravleva AV, Tagaev AA, Yakimenko ZA, Telezhinskaya IN, Kirpichnikov MP, Ovchinnikova TV, Arseniev AS. 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. 2013, 10, 838–863.Google Scholar

  • [147]

    Shenkarev ZO, Lyukmanova EN, Paramonov AS, Panteleev PV, Balandin SV, Shulepko MA, Mineev KS, Ovchinnikova TV, Kirpichnikov MP, Arseniev AS. Lipid-protein nanodiscs offer new perspectives for structural and functional studies of water-soluble membrane-active peptides. Acta Naturae. 2014, 6, 84–94.Google Scholar

  • [148]

    Tzitzilonis C, Eichmann C, Maslennikov I, Choe S, Riek R. Detergent/nanodisc screening for high-resolution NMR studies of an integral membrane protein containing a cytoplasmic domain. PLoS One 2013, 8, e54378.Google Scholar

  • [149]

    Kucharska I, Edrington TC, Liang B, Tamm LK. Optimizing nanodiscs and bicelles for solution NMR studies of two β-barrel membrane proteins. J. Biomol. NMR. 2015, 61, 261–274.Google Scholar

  • [150]

    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, 1562–1569.Google Scholar

  • [151]

    Raschle T, Hiller S, Yu T-Y, Rice AJ, 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, 17777–17779.Google Scholar

  • [152]

    Glück JM, Wittlich M, Feuerstein S, Hoffmann S, Willbold D, Koenig BW. Integral membrane proteins in nanodiscs can be studied by solution NMR spectroscopy. J. Am. Chem. Soc. 2009, 131, 12060–12061.Google Scholar

  • [153]

    Hagn F, Wagner G. Structure refinement and membrane positioning of selectively labeled OmpX in phospholipid nanodiscs. J. Biomol. NMR. 2015, 61, 249–260.Google Scholar

  • [154]

    Fox DA, Larsson P, Lo RH, Kroncke BM, Kasson PM, Columbus L. Structure of the Neisserial outer membrane protein Opa60: loop flexibility essential to receptor recognition and bacterial engulfment. J. Am. Chem. Soc. 2014, 136, 9938–9946.Google Scholar

  • [155]

    Bibow S, Carneiro MG, Sabo TM, Schwiegk C, Becker S, Riek R, Lee D. Measuring membrane protein bond orientations in nanodiscs via residual dipolar couplings. Protein Sci. 2014, 23, 851–856.Google Scholar

  • [156]

    Mineev KS, Goncharuk SA, Kuzmichev PK, Vilar M, Arseniev AS. NMR Dynamics of transmembrane and intracellular domains of p75NTR in lipid-protein nanodiscs. Biophys. J. 2015, 109, 772–782.Google Scholar

  • [157]

    Zhang M, Huang R, Ackermann R, Im S-C, Waskell L, Schwendeman A, Ramamoorthy A. Reconstitution of the Cytb5-CytP450 complex in nanodiscs for structural studies using NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 2016, 55, 4497–4499.Google Scholar

  • [158]

    Denisov IG, Sligar SG. Nanodiscs for structural and functional studies of membrane proteins. Nat. Struct. Mol. Biol. 2016, 23, 481–486.Google Scholar

  • [159]

    Knowles TJ, Finka R, Smith C, Lin Y-P, Dafforn T, Overduin M. Membrane proteins solubilized intact in lipid containing nanoparticles bounded by styrene maleic acid copolymer. J. Am. Chem. Soc. 2009, 131, 7484–7485.Google Scholar

  • [160]

    Orwick-Rydmark M, Lovett JE, Graziadei A, Lindholm L, Hicks MR, Watts A. Detergent-free incorporation of a seven-transmembrane receptor protein into nanosized bilayer Lipodisq particles for functional and biophysical studies. Nano Lett. 2012, 12, 4687–4692.Google Scholar

  • [161]

    Sahu ID, McCarrick RM, Troxel KR, Zhang R, Smith HJ, Dunagan MM, Swartz MS, Rajan PV, Kroncke BM, Sanders CR, Lorigan GA. DEER EPR measurements for membrane protein structures via bifunctional spin labels and lipodisq nanoparticles. Biochemistry 2013, 52, 6627–6632.Google Scholar

  • [162]

    Zhang R, Sahu ID, Liu L, Osatuke A, Comer RG, Dabney-Smith C, Lorigan GA. Characterizing the structure of lipodisq nanoparticles for membrane protein spectroscopic studies. Biochim. Biophys. Acta 2015, 1848, 329–333.Google Scholar

  • [163]

    Craig AF, Clark EE, Sahu ID, Zhang R, Frantz ND, Al-Abdul-Wahid MS, Dabney-Smith C, Konkolewicz D, Lorigan GA. Tuning the size of styrene-maleic acid copolymer-lipid nanoparticles (SMALPs) using RAFT polymerization for biophysical studies. Biochim. Biophys. Acta 2016, 1858, 2931–2939.Google Scholar

  • [164]

    Gohon Y, Dahmane T, Ruigrok RWH, Schuck P, Charvolin D, Rappaport F, Timmins P, Engelman DM, Tribet C, Popot J-L, Ebel C. Bacteriorhodopsin/amphipol complexes: structural and functional properties. Biophys. J. 2008, 94, 3523–3537.Google Scholar

  • [165]

    Popot J-L, Althoff T, Bagnard D, Banères J-L, Bazzacco P, Billon-Denis E, Catoire LJ, Champeil P, Charvolin D, Cocco MJ, Crémel G, Dahmane T, de la Maza LM, Ebel C, Gabel F, Giusti F, Gohon Y, Goormaghtigh E, Guittet E, Kleinschmidt JH, Kühlbrandt W, Le Bon C, Martinez KL, Picard M, Pucci B, Sachs JN, Tribet C, van Heijenoort C, Wien F, Zito F, Zoonens M. Amphipols from A to Z. Annu. Rev. Biophys. 2011, 40, 379–408.Google Scholar

  • [166]

    Planchard N, Point É, Dahmane T, Giusti F, Renault M, Le Bon C, Durand G, Milon A, Guittet É, Zoonens M, Popot J-L, Catoire LJ. The use of amphipols for solution NMR studies of membrane proteins: advantages and constraints as compared to other solubilizing media. J. Membr. Biol. 2014, 247, 827–842.Google Scholar

  • [167]

    Zoonens M, Catoire LJ, Giusti F, Popot J-L. NMR study of a membrane protein in detergent-free aqueous solution. Proc. Natl. Acad. Sci. USA 2005, 102, 8893–8898.Google Scholar

  • [168]

    Catoire LJ, Zoonens M, van Heijenoort C, Giusti F, Popot J-L, Guittet E. Inter- and intramolecular contacts in a membrane protein/surfactant complex observed by heteronuclear dipole-to-dipole cross-relaxation. J. Magn. Reson. 2009, 197, 91–95.Google Scholar

  • [169]

    Catoire LJ, Damian M, Giusti F, Martin A, van Heijenoort C, Popot J-L, Guittet E, Banères J-L. 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. 2010, 132, 9049–9057.Google Scholar

  • [170]

    Catoire LJ, 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, 623–630.Google Scholar

  • [171]

    Catoire LJ, Damian M, Baaden M, Guittet E, Banères J-L. Electrostatically-driven fast association and perdeuteration allow detection of transferred cross-relaxation for G protein-coupled receptor ligands with equilibrium dissociation constants in the high-to-low nanomolar range. J. Biomol. NMR 2011, 50, 191–195.Google Scholar

  • [172]

    Etzkorn M, Zoonens M, Catoire LJ, Popot J-L, Hiller S. How amphipols embed membrane proteins: global solvent accessibility and interaction with a flexible protein terminus. J. Membr. Biol. 2014, 247, 965–970.Google Scholar

  • [173]

    Elter S, Raschle T, Arens S, Viegas A, Gelev V, Etzkorn M, Wagner G. The use of amphipols for NMR structural characterization of 7-TM proteins. J. Membr. Biol. 2014, 247, 957–964.Google Scholar

  • [174]

    Dahmane T, Giusti F, Catoire LJ, Popot J-L. Sulfonated amphipols: synthesis, properties, and applications. Biopolymers 2011, 95, 811–823.Google Scholar

  • [175]

    Bazzacco P, Billon-Denis E, Sharma KS, Catoire LJ, Mary S, Le Bon C, Point E, Banères J-L, Durand G, Zito F, Pucci B, Popot J-L. Nonionic homopolymeric amphipols: application to membrane protein folding, cell-free synthesis, and solution nuclear magnetic resonance. Biochemistry 2012, 51, 1416–1430.Google Scholar

  • [176]

    Feinstein HE, Tifrea D, Sun G, Popot J-L, de la Maza LM, Cocco MJ. Long-term stability of a vaccine formulated with the amphipol-trapped major outer membrane protein from Chlamydia trachomatis. J. Membr. Biol. 2014, 247, 1053–1065.Google Scholar

  • [177]

    Focke PJ, Hein C, Hoffmann B, Matulef K, Bernhard F, Dötsch V, Valiyaveetil FI. Combining in Vitro Folding with Cell Free Protein Synthesis for Membrane Protein Expression. Biochemistry 2016, 55, 4212–4219.Google Scholar

  • [178]

    Roos C, Kai L, Haberstock S, Proverbio D, Ghoshdastider U, Ma Y, Filipek S, Wang X, Dötsch V, Bernhard F. High-level cell-free production of membrane proteins with nanodiscs. Methods Mol. Biol. 2014, 1118, 109–130.Google Scholar

  • [179]

    Shenkarev ZO, Lyukmanova EN, Butenko IO, Petrovskaya LE, Paramonov AS, Shulepko MA, Nekrasova OV, Kirpichnikov MP, Arseniev AS. Lipid-protein nanodiscs promote in vitro folding of transmembrane domains of multi-helical and multimeric membrane proteins. Biochim. Biophys. Acta 2013, 1828, 776–784.Google Scholar

  • [180]

    Serebryany E, Zhu GA, Yan ECY. Artificial membrane-like environments for in vitro studies of purified G-protein coupled receptors. Biochim. Biophys. Acta 2012, 1818, 225–233.Google Scholar

  • [181]

    Zhang Q, Ma X, Ward A, Hong W-X, Jaakola V-P, Stevens RC, Finn MG, Chang G. Designing facial amphiphiles for the stabilization of integral membrane proteins. Angew. Chem. Int. Ed. Engl. 2007, 46, 7023–7025.Google Scholar

  • [182]

    Tribet C, Audebert R, Popot JL. Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc. Natl. Acad. Sci. USA 1996, 93, 15047–15050.Google Scholar

  • [183]

    Kroncke BM, Columbus L. Identification and removal of nitroxide spin label contaminant: impact on PRE studies of α-helical membrane proteins in detergent. Protein Sci. 2012, 21, 589–595.Google Scholar

  • [184]

    Thiagarajan-Rosenkranz P, Draney AW, Smrt ST, Lorieau JL. A Positively Charged Liquid Crystalline Medium for Measuring Residual Dipolar Couplings in Membrane Proteins by NMR. J. Am. Chem. Soc. 2015, 137, 11932–11934.Google Scholar

  • [185]

    Warner LR, Varga K, Lange OF, Baker SL, Baker D, Sousa MC, Pardi A. Structure of the BamC two-domain protein obtained by Rosetta with a limited NMR data set. J. Mol. Biol. 2011, 411, 83–95.Google Scholar

  • [186]

    Mineev KS, Goncharuk SA, Arseniev AS. Toll-like receptor 3 transmembrane domain is able to perform various homotypic interactions: an NMR structural study. FEBS Lett. 2014, 588, 3802–3807.Google Scholar

  • [187]

    Stanczak P, Horst R, Serrano P, Wüthrich K. NMR characterization of membrane protein-detergent micelle solutions by use of microcoil equipment. J. Am. Chem. Soc. 2009, 131, 18450–18456.Google Scholar

  • [188]

    Singer SJ, Nicolson GL. The fluid mosaic model of the structure of cell membranes. Science 1972, 175, 720–731.Google Scholar

  • [189]

    Ruysschaert J-M, Lonez C. Role of lipid microdomains in TLR-mediated signalling. Biochim. Biophys. Acta 2015, 1848, 1860–1867.Google Scholar

  • [190]

    Risselada HJ, Marrink SJ. The molecular face of lipid rafts in model membranes. Proc. Natl. Acad. Sci. USA 2008, 105, 17367–17372.Google Scholar

  • [191]

    Hedger G, Sansom MSP. Lipid interaction sites on channels, transporters and receptors: recent insights from molecular dynamics simulations. Biochim. Biophys. Acta 2016, 1858, 2390–2400.Google Scholar

  • [192]

    Hedger G, Sansom MSP, Koldsø H. The juxtamembrane regions of human receptor tyrosine kinases exhibit conserved interaction sites with anionic lipids. Sci. Rep. 2015, 5, 9198.Google Scholar

  • [193]

    Saotome K, Duong-Ly KC, Howard KP. Influenza A M2 protein conformation depends on choice of model membrane: conformation of M2 Protein in Lipid Bilayers. Biopolymers 2015, 104, 405–411.Google Scholar

  • [194]

    Chou JJ, Kaufman JD, Stahl SJ, Wingfield PT, Bax A. Micelle-induced curvature in a water-insoluble HIV-1 Env peptide revealed by NMR dipolar coupling measurement in stretched polyacrylamide gel. J. Am. Chem. Soc. 2002, 124, 2450–2451.Google Scholar

  • [195]

    Mineev KS, Panova SV, Bocharova OV, Bocharov EV, Arseniev AS. The membrane mimetic affects the spatial structure and mobility of EGFR transmembrane and juxtamembrane domains. Biochemistry 2015, 54, 6295–6298.Google Scholar

  • [196]

    Bragin PE, Mineev KS, Bocharova OV, Volynsky PE, Bocharov EV, Arseniev AS. HER2 Transmembrane domain dimerization coupled with self-association of membrane-embedded cytoplasmic juxtamembrane regions. J. Mol. Biol. 2016, 428, 52–61.Google Scholar

  • [197]

    Mineev KS, Bocharov EV, Volynsky PE, Goncharuk MV, Tkach EN, Ermolyuk YS, Schulga AA, Chupin VV, Maslennikov IV, Efremov RG, Arseniev AS. Dimeric structure of the transmembrane domain of glycophorin a in lipidic and detergent environments. Acta Naturae 2011, 3, 90–98.Google Scholar

  • [198]

    Smith SO, Song D, Shekar S, Groesbeek M, Ziliox M, Aimoto S. Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry 2001, 40, 6553–6558.Google Scholar

  • [199]

    Trenker R, Call ME, Call MJ. Crystal structure of the glycophorin A transmembrane dimer in lipidic cubic phase. J. Am. Chem. Soc. 2015, 137, 15676–15679.Google Scholar

  • [200]

    Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, MacKinnon R. X-ray structure of a voltage-dependent K+ channel. Nature 2003, 423, 33–41.Google Scholar

  • [201]

    Vogt J, Schulz GE. The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence. Structure 1999, 7, 1301–1309.Google Scholar

  • [202]

    Li D, Lyons JA, Pye VE, Vogeley L, Aragão D, Kenyon CP, Shah STA, Doherty C, Aherne M, Caffrey M. Crystal structure of the integral membrane diacylglycerol kinase. Nature 2013, 497, 521–524.Google Scholar

  • [203]

    Chen Y, Zhang Z, Tang X, Li J, Glaubitz C, Yang J. Conformation and topology of diacylglycerol kinase in E. coli membranes revealed by solid-state NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 2014, 53, 5624–5628.Google Scholar

About the article

Konstantin S. Mineev

Konstantin S. Mineev is a senior research scientist in the laboratory of biomolecular NMR spectroscopy at the Shemyakin-Ovchnnikov Institute of Bioorganic Chemistry, Moscow. He received his master’s degree at the Moscow Institute of Physics and Technology (MIPT) in 2007 and his PhD in Biophysics at the Lomonosov Moscow State University in 2010. He is working as an adjunct professor in MIPT since 2014. The current research of Dr. Mineev is focused on elucidating the structural basis of the activation mechanisms of type I integral membrane proteins and development and characterization of various membrane mimetics.

Kirill D. Nadezhdin

Kirill D. Nadezhdin is a research fellow in the laboratory of biomolecular NMR spectroscopy at the Shemyakin-Ovchnnikov Institute of Bioorganic Chemistry, Moscow. He received his master’s degree at the Moscow Institute of Physics and Technology (MIPT) in 2006 and his PhD in Biophysics at the Lomonosov Moscow State University in 2012. He is working as an assistant professor and deputy dean at the Department of Biological and Medical Physics in MIPT since 2015. Scientific interests of Dr. Nadezhdin are focused in the area of structural investigations of amyloid precursor protein and membrane-active peptides.


Received: 2016-08-30

Accepted: 2016-11-01

Published Online: 2016-12-20

Published in Print: 2017-02-01


Citation Information: Nanotechnology Reviews, Volume 6, Issue 1, Pages 15–32, ISSN (Online) 2191-9097, ISSN (Print) 2191-9089, DOI: https://doi.org/10.1515/ntrev-2016-0074.

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