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Alternatives to Detergents for Handling Membrane Proteins in Aqueous Solutions

  • Jean-Luc Popot
Chapter
Part of the Biological and Medical Physics, Biomedical Engineering book series (BIOMEDICAL)

Summary

Attempts at substituting detergents with other surfactants for handling membrane proteins (MPs) in aqueous solutions have a long history. They are based on three main incentives: (i) trying to improve the stability of solubilized MPs; (ii) providing them with an environment that, in its physical characteristics and/or its chemical composition, is closer to the natural environment; and (iii) making them accessible to technologies that are difficult or impossible to implement in the presence of detergents. A first route is to reinsert the protein in a lipid bilayer, most often closed upon itself in the form of lipid vesicles, sometimes forming a planar “black lipid membrane.” This approach is obligatory when functional assays require the protein to have access to two distinct aqueous compartments, but the objects formed are large, if not macroscopic, and do not lend themselves well to most biophysical investigations. A second route is to substitute totally or partially the detergent with other surfactants while forming water-soluble particles of nanometric dimensions. The use of specially developed amphipathic polymers called amphipols is one such approach, which will be described in detail in Chaps.   4 and   5 , but it is far from being the only one. In order to provide a broader view of which systems are available to the experimenter, the present chapter reviews the four principal alternatives to detergents and amphipols: (i) bicelles, which are mixtures of lipids and detergents or short-chain lipids that, under appropriate conditions, form disc-shaped bilayer fragments into which MPs can integrate; (ii) nanodiscs, whose basic concept is similar to that of bicelles, but in which the rim of the bilayer disc is stabilized by specially engineered proteins; (iii) peptides or lipopeptides, which can either interact directly with the MP to be solubilized or stabilize MP/lipid complexes; and (iv) fluorinated surfactants, which resemble detergents in their chemical structure but whose hydrophobic chains contain fluorine atoms, which make them lyophobic (poorly miscible with hydrocarbons); this renders them less disruptive of the protein/protein and protein/lipid interactions that stabilize MPs.

References

  1. Abla, M., Durand, G., Breyton, C., Raynal, S., Ebel, C., Pucci, B. (2012) A diglucosylated fluorinated surfactant to handle integral membrane proteins in aqueous solution. J. Fluor Chem. 134:63–71.CrossRefGoogle Scholar
  2. Abla, M., Durand, G., Pucci, B. (2008) Glucose-based surfactants with hydrogenated, fluorinated, or hemifluorinated tails: synthesis and comparative physical-chemical characterization. J. Org. Chem. 73:8142–8153.CrossRefGoogle Scholar
  3. Abla, M., Unger, S., Keller, S., Bonneté, F., Ebel, C., Pucci, B., Breyton, C., Durand, G. (2015) Micellar and biochemical properties of a propyl-ended fluorinated surfactant designed for membrane-protein study. J. Colloid Interface Sci. 445:127–136.CrossRefADSGoogle Scholar
  4. Agah, S., Faham, S. (2012) Crystallization of membrane proteins in bicelles. Methods Mol. Biol. 914:3–16.Google Scholar
  5. Ahn, V.E., Leyko, P., Alattia, J.-R., Chen, L., Privé, G.G. (2006) Crystal structures of saposins A and C. Protein Sci. 15:1849–1857.CrossRefGoogle Scholar
  6. Akkaladevi, N., Mukherjee, S., Katayama, H., Janowiak, B., Patel, D., Gogol, E.P., Pentelute, B.L., Collier, R.J., Fisher, M.T. (2015) Following Nature’s lead: On the construction of membrane-inserted toxins in lipid bilayer nanodiscs. J. Membr. Biol. 248:595–607.CrossRefGoogle Scholar
  7. Alvarez, F.J., Orelle, C., Huang, Y., Bajaj, R., Everly, R.M., Klug, C., Davidson, A.L. (2015) Full engagement of liganded maltose-binding protein stabilizes a semi-open ATP-binding cassette dimer in the maltose transporter. Mol. Microbiol. 98:878–894.CrossRefGoogle Scholar
  8. Anantharamaiah, G.M., Brouillette, C.G., Engler, J.A., De Loof, H., Venkatachalapathi, Y.V., Boogaerts, J., Segrest, J.P. (1990) Role of amphipathic helices in HDL structure/function. Adv. Exp. Med. Biol. 285:131–140.CrossRefGoogle Scholar
  9. Anantharamaiah, G.M., Jones, J.L., Brouillette, C.G., Schmidt, C.F., Chung, B.H., Hughes, T.A., Bhown, A.S., Segrest, J.P. (1985) Studies of synthetic peptide analogs of the amphipathic helix. Structure of complexes with dimyristoyl phosphatidylcholine. J. Biol. Chem. 260:10248–10255.Google Scholar
  10. Baas, B.J., Denisov, I.G., Sligar, S.G. (2004) Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch. Biochem. Biophys. 430:218–228.CrossRefGoogle Scholar
  11. Banerjee, S., Huber, T., Sakmar, T.P. (2008) Rapid incorporation of functional rhodopsin into nanoscale apolipoprotein-bound bilayer (NABB) particles. J. Mol. Biol. 377:1067–1081.CrossRefGoogle Scholar
  12. Barrett, P.J., Song, Y., Van Horn, W.D., Hustedt, E.J., Schafer, J.M., Hadziselimovic, A.H., Beel, A.J., Sanders, C.R. (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 336:1168–1171.CrossRefADSGoogle Scholar
  13. Barthélémy, P., Améduri, B., Chabaud, E., Popot, J.-L., Pucci, B. (1999) Synthesis and preliminary assessment of ethyl-terminated perfluoroalkyl slowdown surfactants derived from tris(hydroxymethyl)acrylamidomethane. Org. Lett. 1:1689–1692.CrossRefGoogle Scholar
  14. Barthélémy, P., Tomao, V., Selb, J., Chaudier, Y., Pucci, B. (2002) Fluorocarbon-hydrocarbon non-ionic surfactant mixtures: a study of their miscibility. Langmuir 18:2557–2563.CrossRefGoogle Scholar
  15. Bavec, A., Juréus, A., Cigić, B., Langel, U., Zorko, M. (1999) Peptitergent PD1 affects the GTPase activity of rat brain cortical membranes. Peptides 20:177–184.CrossRefGoogle Scholar
  16. Bayburt, T.H., Carlson, J.W., Sligar, S.G. (1998) Reconstitution and imaging of a membrane protein in a nanometer-size phospholipid bilayer. J. Struct. Biol. 123:37–44.CrossRefGoogle Scholar
  17. Bayburt, T.H., Grinkova, Y.V., Sligar, S.G. (2002) Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett. 2:853–856.CrossRefADSGoogle Scholar
  18. Bayburt, T.H., Grinkova, Y.V., Sligar, S.G. (2006) Assembly of single bacteriorhodopsin trimers in bilayer nanodiscs. Arch. Biochem. Biophys. 450:215–222.CrossRefGoogle Scholar
  19. Bayburt, T.H., Leitz, A.J., Xie, G., Oprian, D.D., Sligar, S.G. (2007) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J. Biol. Chem. 282:14875–14881.CrossRefGoogle Scholar
  20. Bayburt, T.H., Sligar, S.G. (2002) Single-molecule height measurements on microsomal cytochrome P450 in nanometer-scale phospholipid bilayer disks. Proc. Natl. Acad. Sci. USA 99:6725–6730.CrossRefADSGoogle Scholar
  21. Bayburt, T.H., Sligar, S.G. (2010) Membrane protein assembly into nanodiscs. FEBS Lett. 584:1721–1727.CrossRefGoogle Scholar
  22. Bayburt, T.H., Vishnivetskiy, S.A., McLean, M.A., Morizumi, T., Huang, C.-C., Tesmer, J.J.G., Ernst, O.P., Sligar, S.G., Gurevich, V.V. (2011) Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding. J. Biol. Chem. 286:1420–1428.CrossRefGoogle Scholar
  23. Beaugrand, M., Arnold, A.A., Juneau, A., Balieiro Gambaro, A., Warschawski, D.E., Williamson, P.T.F., Marcotte, I. (2016) Magnetically oriented bicelles with monoalkylphosphocholines: versatile membrane mimetics for nuclear magnetic resonance applications. Langmuir 32:13244–13251.CrossRefGoogle Scholar
  24. Bibow, S., Polyhach, Y., Eichmann, C., Chi, C.N., Kowal, J., Albiez, S., McLeod, R.A., Stahlberg, H., Jeschke, G., Güntert, P., Riek, R. (2017) Solution structure of discoidal high-density lipoprotein particles with a shortened apolipoprotein A-I. Nat. Struct. Mol. Biol. 24:187–193.CrossRefGoogle Scholar
  25. Blesneac, I., Ravaud, S., Juillan-Binard, C., Barret, L.A., 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 1818:798–805.CrossRefGoogle Scholar
  26. Bocharov, E.V., Pustovalova, Y.E., Pavlov, K.V., Volynsky, P.E., Goncharuk, M.V., Ermolyuk, Y.S., Karpunin, D.V., Schulga, A.A., Kirpichnikov, M.P., Efremov, R.G., Maslennikov, I.V., Arseniev, A.S. (2007) Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger. J. Biol. Chem. 282:16256–16265.CrossRefGoogle Scholar
  27. Bocharov, E.V., Volynsky, P.E., Pavlov, K.V., Efremov, R.G., Arseniev, A.S. (2010) Structure elucidation of dimeric transmembrane domains of bitopic proteins. Cell Adh. Migr. 4:284–298.CrossRefGoogle Scholar
  28. Boldog, T., Grimme, S., Li, M., Sligar, S.G., Hazelbauer, G.L. (2006) Nanodiscs separate chemoreceptor oligomeric states and reveal their signaling properties. Proc. Natl. Acad. Sci. USA 103:11509–11514.CrossRefADSGoogle Scholar
  29. Borch, J., Hamann, T. (2009) The nanodisc: a novel tool for membrane protein studies. Biol. Chem. 390:805–814.CrossRefGoogle Scholar
  30. Breyton, C., Chabaud, E., Chaudier, Y., Pucci, B., Popot, J.-L. (2004) Hemifluorinated surfactants: a non-dissociating environment for handling membrane proteins in aqueous solutions? FEBS Lett. 564:312–318.CrossRefGoogle Scholar
  31. Breyton, C., Flayhan, A., Gabel, F., Lethier, M., Durand, G., Boulanger, P., Chamig, M., Ebel, C. (2013a) Assessing the conformation changes of pb5, the receptor binding protein of phage T5, upon binding to its E. coli receptor FhuA. J. Biol. Chem. 288:30763–30772.CrossRefGoogle Scholar
  32. Breyton, C., Gabel, F., Abla, M., Pierre, Y., Lebaupain, F., Durand, G., Popot, J.-L., Ebel, C., Pucci, B. (2009) Micellar and biochemical properties of (hemi)fluorinated surfactants are controlled by the size of the polar head. Biophys. J. 97:1077–1086.CrossRefADSGoogle Scholar
  33. Breyton, C., Gabel, F., Lethier, M., Flayhan, A., Durand, G., Jault, J.-M., Juillan-Binard, C., Imbert, Moulin, M., Ravaud S., Härtlein M., Ebel C. (2013b) Small angle neutron scattering for the study of solubilised membrane proteins. Eur. Phys. J. E 36:71–86.CrossRefGoogle Scholar
  34. Breyton, C., Pucci, B., Popot, J.-L. (2010) Amphipols and fluorinated surfactants: two alternatives to detergents for studying membrane proteins in vitro in: Mus-Veteau, I., ed., Heterologous expression of membrane proteins: Methods and protocols. The Humana Press, Totowa, New Jersey, USA, pp. 219–245.CrossRefGoogle Scholar
  35. Broecker, J., Eger, B.T., Ernst, O.P. (2017) Crystallogenesis of membrane proteins mediated by polymer-bounded lipid nanodiscs. Structure 25:384–392.CrossRefGoogle Scholar
  36. Brouillette, C.G., Anantharamaiah, G.M., Engler, J.A., Borhani, D.W. (2001) Structural models of human apolipoprotein A-I: a critical analysis and review. Biochim. Biophys. Acta 1531:4–46.CrossRefGoogle Scholar
  37. Cappuccio, J.A., Blanchette, C.D., Sulchek, T.A., Arroyo, E.S., Kralj, J.M., Hinz, A.K., Kuhn, E.A., Chromy, B.A., Segelke, B.W., Rothschild, K.J., Fletcher, J.E., Katzen, F., Peterson, T.C., Kudlicki, W.A., Bench, G., Hoeprich, P.D., Coleman, M.A. (2008) Cell-free co-expression of functional membrane proteins and apolipoprotein, forming soluble nanolipoprotein particles. Mol. Cell. Proteom. 7:2246–2253.CrossRefGoogle Scholar
  38. Carey, M.C., Small, D.M. (1972) Micelle formation by bile salts. Physical-chemical and thermodynamic considerations. Arch. Intern. Med. 130:506–527.CrossRefGoogle Scholar
  39. Carlson, J.W., Jonas, A., Sligar, S.G. (1997) Imaging and manipulation of high-density lipoproteins. Biophys. J. 73:1184–1189.CrossRefGoogle Scholar
  40. Casiraghi, M., Damian, M., Lescop, E., Point, E., Moncoq, K., Morellet, N., Levy, D., Marie, J., Guittet, E., Banères, J.-L., Catoire, L.J. (2016) Functional modulation of a GPCR conformational landscape in a lipid bilayer. J. Am. Chem. Soc. 138:11170–11175CrossRefGoogle Scholar
  41. Catoire, L.J., Damian, M., Giusti, F., Martin, A., van Heijenoort, C., Popot, J.-L., Guittet, E., Banères, J.-L. (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. 132:9049–9057.CrossRefGoogle Scholar
  42. Catoire, L.J., Warnet, X.L., Warschawski, D.E. (2014) Micelles, bicelles, amphipols, nanodiscs, liposomes or intact cells: The hitch-hiker guide to the study of membrane proteins by NMR, in: Mus-Veteau, I., ed., Membrane protein production for structural analysis. Springer, pp. 315–346.Google Scholar
  43. Catte, A., Patterson, J.C., Jones, M.K., Jerome, W.G., Bashtovyy, D., Su, Z., Gu, F., Chen, J., Aliste, M.P., Harvey, S.C., Li, L., Weinstein, G., Segrest, J.P. (2006) Novel changes in discoidal high density lipoprotein morphology: a molecular dynamics study. Biophys. J. 90:4345–4360.CrossRefADSGoogle Scholar
  44. Chabaud, E. (1997) Application des tensioactifs fluorés à la manipulation in vitro des protéines membranaires. Rapport de D.E.A., Université Paris-VI.Google Scholar
  45. Chabaud, E., Barthélémy, P., Mora, N., Popot, J.-L., Pucci, B. (1998) Stabilization of integral membrane proteins in aqueous solution using fluorinated surfactants. Biochimie 80:515–530.CrossRefGoogle Scholar
  46. Chaudier, Y., Barthélémy, P., Pucci, B. (2001) Synthesis and preliminary assessment of hybrid hydrocarbon-fluorocarbon anionic and non-ionic surfactants. Tetrahedron Lett. 42:3583–3585.CrossRefGoogle Scholar
  47. Chaudier, Y., Zito, F., Barthélémy, P., Stroebel, D., Améduri, B., Popot, J.-L., Pucci, B. (2002) Synthesis and preliminary biochemical assessment of ethyl-terminated perfluoroalkylamine oxide surfactants. Bioorg. Med. Chem. Lett. 12:1587–1590.CrossRefGoogle Scholar
  48. Cho, K.H., Byrne, B., Chae, P.S. (2013) Hemifluorinated maltose-neopentyl glycol (HF-MNG) amphiphiles for membrane protein stabilisation. ChemBioChem 14:452–455.CrossRefGoogle Scholar
  49. Chung, B.H., Anantharamaiah, G.M., Brouillette, C.G., Nishida, T., Segrest, J.P. (1985) Studies of synthetic peptide analogs of the amphipathic helix. Correlation of structure with function. J. Biol. Chem. 260:10256–10262.Google Scholar
  50. Chung, J., Prestegard, J.H. (1993) Characterization of field-ordered aqueous liquid crystals by NMR diffusion measurements. J. Phys. Chem. 97:9837–9843.CrossRefGoogle Scholar
  51. Civjan, N.R., Bayburt, T.H., Schuler, M.A., Sligar, S.G. (2003) Direct solubilization of heterologously expressed membrane proteins by incorporation into nanoscale lipid bilayers. BioTechniques 35:556–560, 562–563.Google Scholar
  52. Corin, K., Baaske, P., Ravel, D.B., Song, J., Brown, E., Wang, X., Wienken, C.J., Jerabek-Willemsen, M., Duhr, S., Luo, Y., Braun, D., Zhang, S. (2011) Designer lipid-like peptides: a class of detergents for studying functional olfactory receptors using commercial cell-free systems. PLoS ONE 6:e25067.CrossRefADSGoogle Scholar
  53. Cui, T.X., Canlas, C.G., Xu, Y., Tang, P. (2010) Anesthetic effects on the structure and dynamics of the second transmembrane domains of nAChR α4β2. Biochim. Biophys. Acta 1798:161–166.CrossRefGoogle Scholar
  54. Czerski, L., Sanders, C.R. (2000) Functionality of a membrane protein in bicelles. Anal. Biochem. 284:327–333.CrossRefGoogle Scholar
  55. Daury, L., Orange, F., Taveau, J.-C., Verchère, A., Monlezun, L., Gounou, C., Marreddy, R.K.R., Picard, M., Broutin, I., Pos, K.M., Lambert, O. (2016) Tripartite assembly of RND multidrug efflux pumps. Nat. Commun. 7:10731.CrossRefADSGoogle Scholar
  56. Dauvergne, J., Polidori, A., Vénien-Bryan, C., Pucci, B. (2008) Synthesis of a hemifluorinated amphiphile designed for self-assembly and two-dimensional crystallization of membrane proteins. Tet. Lett. 49:2247–2250.CrossRefGoogle Scholar
  57. De Angelis, A., Nevzorov, A., Park, S.H., Howell, S.C., Mrse, A.A., Opella, S.J. (2004) High-resolution NMR spectroscopy of membrane proteins in “aligned” bicelles. J. Am. Chem. Soc. 126:15340–15341.CrossRefGoogle Scholar
  58. De Angelis, A.A., Opella, S.J. (2007) Bicelle samples for solid-state NMR of membrane proteins. Nat. Protoc. 2:2332–2338.CrossRefGoogle Scholar
  59. Debnath, A., Schäfer, L.V. (2015) Structure and dynamics of phospholipid nanodiscs from all-atom and coarse-grained simulations. J. Phys. Chem. B 119:6991–7002.CrossRefGoogle Scholar
  60. Dempsey, C.E., Sternberg, B. (1991) Reversible disc-micellization of dimyristoylphosphatidylcholine bilayers induced by melittin and [Ala-14]melittin. Biochim. Biophys. Acta 1061:175–184.CrossRefGoogle Scholar
  61. Denisov, I.G., Baas, B.J., Grinkova, Y.V., Sligar, S.G. (2007) Cooperativity in cytochrome P450 3A4: linkages in substrate binding, spin state, uncoupling, and product formation. J. Biol. Chem. 282:7066–7076.CrossRefGoogle Scholar
  62. Denisov, I.G., Grinkova, Y.V., Lazarides, A.A., Sligar, S.G. (2004) Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J. Am. Chem. Soc. 126:3477–3487.CrossRefGoogle Scholar
  63. Denisov, I.G., McLean, M.A., Shaw, A.W., Grinkova, Y.V., Sligar, S.G. (2005) Thermotropic phase transitions in soluble nanoscale lipid bilayers. J. Phys. Chem. B. 109:15580–15588.CrossRefGoogle Scholar
  64. Denisov, I.G., Sligar, S.G. (2016) Nanodiscs for structural and functional studies of membrane proteins. Nat. Struct. Mol. Biol. 23:481–486.CrossRefGoogle Scholar
  65. Denisov, I.G., Sligar, S.G. (2017) Nanodiscs in membrane biochemistry and biophysics. Chem. Rev. 117:4669–4713.CrossRefGoogle Scholar
  66. Der Mardirossian, C., Krafft, M.-P., Gulik-Krzywicki, T., le Maire, M., Lederer, F. (1998) On the lack of protein-solubilizing properties of two perfluoroalkylated detergents, as tested with neutrophil plasma membranes. Biochimie 80:531–541.CrossRefGoogle Scholar
  67. Duan, H., Civjan, N.R., Sligar, S.G., Schuler, M.A. (2004) Co-incorporation of heterologously expressed Arabidopsis cytochrome P450 and P450 reductase into soluble nanoscale lipid bilayers. Arch. Biochem. Biophys. 424:141–153.CrossRefGoogle Scholar
  68. Durand, G., Abla, M., Ebel, C., Breyton, C. (2014) New amphiphiles to handle membrane proteins: “Ménage à Trois” between chemistry, physical chemistry, and biochemistry, in: Mus-Veteau, I., ed., Membrane Proteins Production for Structural Analysis. Springer, New York, Heidelberg, Dordrecht, London, pp. 205–251.Google Scholar
  69. Durbin, D.M., Jonas, A. (1997) The effect of apolipoprotein A-II on the structure and function of apolipoprotein A-I in a homogeneous reconstituted high density lipoprotein particle. J. Biol. Chem. 272:31333–31339.CrossRefGoogle Scholar
  70. Dürr, U.H., Gildenberg, M., Ramamoorthy, A. (2012) The magic of bicelles lights up membrane protein structure. Chem. Rev. 112:6054–6074.CrossRefGoogle Scholar
  71. Dürr, U.H.N., Soong, R., Ramamoorthy, A. (2013) When detergent meets bilayer: Birth and coming of age of lipid bicelles. Prog. Nucl. Magn. Reson. Spectrosc. 69:1–22.CrossRefGoogle Scholar
  72. Efremov, R.G., Baradaran, R., Sazanov, L.A. (2010) The architecture of respiratory complex I. Nature 465:441–445.CrossRefADSGoogle Scholar
  73. Efremov, R.G., Leitner, A., Aebersold, R., Raunser, S. (2015) Architecture and conformational switch mechanism of the ryanodine receptor. Nature 517:39–43.CrossRefADSGoogle Scholar
  74. Eichmann, C., Bibow, S., Riek, R. (2017) α-Synuclein lipoprotein nanoparticles. Nanotech. Rev. 6:105–110.Google Scholar
  75. Eichmann, C., Campioni, S., Kowal, J., Maslennikov, I., Gerez, J., Liu, X., Verasdonck, J., Nespovitaya, N., Choe, S., Meier, B.H., Picotti, P., Rizo, J., Stahlberg, H., Riek, R. (2016) Preparation and characterization of stable α-synuclein lipoprotein particles. J. Biol. Chem. 291:8516–8527.CrossRefGoogle Scholar
  76. Elter, S., Raschle, T., Arens, S., Viegas, A., Gelev, V., Etzkorn, M., Wagner, G. (2014) The use of amphipols for NMR structural characterization of 7-TM proteins. J. Membr. Biol. 247:957–964.CrossRefGoogle Scholar
  77. Etzkorn, M., Raschle, T., Hagn, F., Gelev, V., Rice, A.J., Walz, T., Wagner, G. (2013) Cell-free expressed bacteriorhodopsin in different soluble membrane mimetics: biophysical properties and NMR accessibility. Structure 21:394–401.CrossRefGoogle Scholar
  78. Faham, S., Boulting, G.L., Massey, E.A., Yohannan, S., Yang, D., Bowie, J.U. (2005) Crystallization of bacteriorhodopsin from bicelle formulations at room temperature. Protein Sci. 14:836–840.CrossRefGoogle Scholar
  79. Faham, S., Bowie, J.U. (2002) Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure. J. Mol. Biol. 316:1–6.CrossRefGoogle Scholar
  80. Fanucci, G.E., Lee, J.Y., Cafiso, D.S. (2003) Membrane mimetic environments alter the conformation of the outer membrane protein BtuB. J. Am. Chem. Soc. 125:13932–13933.CrossRefGoogle Scholar
  81. Flayhan, A., Mertens, H.D.T., Ural-Blimke, Y., Molledo, M.M., Svergun, D.I., Loew, C. (2018) Saposin lipid nanoparticles: A highly versatile and modular tool for membrane protein research. Structure 26:345–355.e345.CrossRefGoogle Scholar
  82. Forrest, B.J., Reeves, L.W. (1981) New lyotropic liquid crystals composed of finite nonspherical micelles. Chem. Rev. 81:1–14.CrossRefGoogle Scholar
  83. Fotinou, C., Aittoniemi, J., de Wet, H., Polidori, A., Pucci, B., Sansom, M.S.P., Vénien-Bryan, C., Ashcroft, F.M. (2013) Tetrameric structure of SUR2B revealed by electron microscopy of oriented single particles. FEBS J. 280:1051–1063.CrossRefGoogle Scholar
  84. Frauenfeld, J., Gumbart, J., van der Sluis, E.O., Funes, S., Gartmann, M., Beatrix, B., Mielke, T., Berninghausen, O., Becker, T., Schulten, K., Beckmann, R. (2011) Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nat. Struct. Mol. Biol. 18:614–621.CrossRefGoogle Scholar
  85. Frauenfeld, J., Löving, R., Armache, J.-P., Sonnen, A.F.-P., Guettou, F., Moberg, P., Zhu, L., Jegerschöld, C., Flayhan, A., Briggs, J.A.G., Garoff, H., Löw, C., Cheng, Y., Nordlund, P. (2016) A saposin-lipoprotein nanoparticle system for membrane proteins. Nat. Meth. 13:345–351.CrossRefGoogle Scholar
  86. Frey, L., Lakomek, N.-A., Riek, R., Bibow, S. (2017) Micelles, bicelles, and nanodiscs: Comparing the impact of membrane mimetics on membrane protein backbone dynamics. Angew. Chem. Int. Ed. 56:380–383.CrossRefGoogle Scholar
  87. Frotscher, E., Danielczak, B., Vargas, C., Meister, A., Durand, G., Keller, S. (2015) A fluorinated detergent for membrane-protein applications. Angew. Chem. Int. Ed. 17:5069–5073.CrossRefGoogle Scholar
  88. Früh, V., IJzerman, A.P., Siegal, G. (2011) How to catch a membrane protein in action: a review of functional membrane protein immobilization strategies and their applications. Chem. Rev. 111:640–656.CrossRefGoogle Scholar
  89. Gao, T., Petrlova, J., He, W., Huser, T., Kudlick, W., Voss, J., Coleman, M.A. (2012) Characterization of de novo synthesized GPCRs supported in nanolipoprotein discs. PLoS ONE 7:e44911.CrossRefADSGoogle Scholar
  90. Gao, Y., Cao, E., Julius, D., Cheng, Y. (2016) TRPV1 structures in nanodiscs reveal mechanisms of ligand and lipid action. Nature 534:347–351.CrossRefADSGoogle Scholar
  91. Gatsogiannis, C., Merino, F., Prumbaum, D., Roderer, D., Leidreiter, F., Meusch, D., Raunser, S. (2016) Membrane insertion of a Tc toxin in near-atomic detail. Nat. Struct. Mol. Biol. 23:884–890.CrossRefGoogle Scholar
  92. Gautier, A., Mott, H.R., Bostock, M.J., Kirkpatrick, J.P., Nietlispach, D. (2010) Structure determination of the seven-helix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat. Struct. Mol. Biol. 17:768–774.CrossRefGoogle Scholar
  93. Georgieva, E.R. (2017) Nanoscale lipid membrane mimetics in spin-labeling and electron paramagnetic resonance spectroscopy studies of protein structure and function. Nanotech. Rev. 6:75–92.Google Scholar
  94. Ghimire, H., Abu-Baker, S., Sahu, I.D., Zhou, A., Mayo, D.J., Lee, R.T., Lorigan, G.A. (2011) Probing the helical tilt and dynamic properties of membrane-bound phospholamban in magnetically aligned bicelles using electron paramagnetic resonance spectroscopy. Biochim. Biophys. Acta 1818:645–650.CrossRefGoogle Scholar
  95. Gillette, W.K., Esposito, D., Abreu Blanco, M., Alexander, P., Bindu, L., Bittner, C., Chertov, O., Frank, P.H., Grose, C., Jones, J.E., Meng, Z., Perkins, S., Van, Q., Ghirlando, R., Fivash, M., Nissley, D.V., McCormick, F., Holderfield, M., Stephen, A.G. (2015) Farnesylated and methylated KRAS4b: high yield production of protein suitable for biophysical studies of prenylated protein-lipid interactions. Sci. Rep. 5:15916.CrossRefADSGoogle Scholar
  96. Goddard, A.D., Dijkman, P.M., Adamson, R.J., Inácio dos Reis, R., Watts, A. (2015) Reconstitution of membrane proteins: A GPCR as an example. Meth. Enzymol. 556:405–424.CrossRefGoogle Scholar
  97. Gogol, E.P., Akkaladevi, N., Szerszen, L., Mukherjee, S., Chollet-Hinton, L., Katayama, H., Pentelute, B.L., Collier, R.J., Fisher, M.T. (2013) Three dimensional structure of the anthrax toxin translocon-lethal factor complex by cryo-electron microscopy. Prot. Sci. 22:586–594.CrossRefGoogle Scholar
  98. Gogonea, V. (2016) Structural insights into high-density lipoprotein: Old models and new facts. Front. Pharmacol. 6:1–30.CrossRefGoogle Scholar
  99. Gogonea, V., Gerstenecker, G.S., Wu, Z., Lee, X., Topbas, C., Wagner, M.A., Tallant, T.C., Smith, J.D., Callow, P., Pipich, V., Malet, H., Schoehn, G., DiDonato, J.A., Hazen, S.L. (2013) The low-resolution structure of nHDL reconstituted with DMPC with and without cholesterol reveals a mechanism for particle expansion. J. Lipid Res. 54:966–983.CrossRefGoogle Scholar
  100. Gregersen, J.L., Fedosova, N.U., Nissen, P., Boesen, T. (2016) Reconstitution of Na+,K+-ATPase in nanodiscs. Methods Mol. Biol. 1377:403–409.Google Scholar
  101. Grigorieff, N., Ceska, T.A., Downing, K.H., Baldwin, J.M., Henderson, R. (1996) Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259:393–421.CrossRefGoogle Scholar
  102. Grinkova, Y.V., Denisov, I.G., Sligar, S.G. (2010) Engineering extended membrane scaffold proteins for self-assembly of soluble nanoscale lipid bilayers. Protein Eng. Des. Sel. 23:843–848.CrossRefGoogle Scholar
  103. Gruene, T., Cho, M.-K., Karyagina, I., Kim, H.-Y., Grosse, C., Giller, K., Zweckstetter, M., Becker, S. (2011) Integrated analysis of the conformation of a protein-linked spin label by crystallography, EPR and NMR spectroscopy. J. Biomol. NMR 49:111–119.CrossRefGoogle Scholar
  104. Grushin, K., Miller, J., Dalm, D., Stoilova-McPhie, S. (2015) Factor VIII organisation on nanodiscs with different lipid composition. Thromb. Haemost. 113:741–749.CrossRefGoogle Scholar
  105. Gustavsson, M., Traaseth, N.J., Veglia, G. (2012) Probing ground and excited states of phospholamban in model and native lipid membranes by magic angle spinning NMR spectroscopy. Biochim. Biophys. Acta 1818:146–153.CrossRefGoogle Scholar
  106. 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. 135:1919–1925.CrossRefGoogle Scholar
  107. Hagn, F., Wagner, G. (2015) Structure refinement and membrane positioning of selectively labeled OmpX in phospholipid nanodiscs. J. Biomol. NMR 61:249–260.CrossRefGoogle Scholar
  108. Han, S.G., Na, J.H., Lee, W.K., Park, D., Oh, J., Yoon, S.H., Lee, C.K., Sung, M.H., Shin, Y.K., Yu, Y.G. (2014) An amphipathic polypeptide derived from poly-γ-glutamic acid for the stabilization of membrane proteins. Prot. Sci. 23:1800–1807.CrossRefGoogle Scholar
  109. Hansen, R.W., Wang, X., Golab, A., Bornert, O., Oswald, C., Wagner, R., Martinez, K.L. (2016) Functional stability of the human κ-opioid receptor reconstituted in nanodiscs revealed by a time-resolved scintillation proximity assay. PLoS ONE 11:e0150658.CrossRefGoogle Scholar
  110. Harroun, T.A., Koslowsky, M., Nieh, M.P., de Lannoy, C.F., Raghunathan, V.A., Katsaras, J. (2005) Comprehensive examination of mesophases formed by DMPC and DHPC mixtures. Langmuir 21:5356–5361.CrossRefGoogle Scholar
  111. Held, P., Lach, F., Lebeau, L., Mioskowski, C. (1997) Synthesis and preliminary evaluation of a new class of fluorinated amphiphiles designed for in-plane immobilisation of biological macromolecules. Tetrahedron Lett. 38:1937–1940.CrossRefGoogle Scholar
  112. Henrich, E., Dötsch, V., Bernhard, F. (2015) Screening for lipid requirements of membrane proteins by combining cell-free expression with nanodiscs. Meth. Enzymol. 556:351–369.CrossRefGoogle Scholar
  113. Henrich, E., Ma, Y., Engels, I., Münch, D., Otten, C., Schneider, T., Henrichfreise, B., Sahl, H.G., Dötsch, V., Bernhard, F. (2016) Lipid requirements for the enzymatic activity of MraY translocases and in vitro reconstitution of Lipid II synthesis pathway. J. Biol. Chem. 291:2535–2546.CrossRefGoogle Scholar
  114. Henrich, E., Peetz, O., Hein, C., LaGuerre, A., Hoffmann, B., Hoffmann, J., Dötsch, V., Bernhard, F., Morgner, N. (2017) Analyzing native membrane protein assembly in nanodiscs by combined non-covalent mass spectrometry and synthetic biology. eLife 6:e20954.CrossRefGoogle Scholar
  115. Ho, D.N., Pomroy, N.C., Cuesta-Seijo, J.A., Privé, G.G. (2008) Crystal structure of a self-assembling lipopeptide detergent at 1.20 Å. Proc. Natl. Acad. Sci. USA 105:12861–12866.CrossRefADSGoogle Scholar
  116. Hopper, J.T.S., Yu, Y.T.-C., Li, D., Raymond, A., Bostock, M., Liko, I., Mikhailov, V., Laganowsky, A., Benesch, J.L.P., Caffrey, M., Nietlispach, D., Robinson, C.V. (2013) Detergent-free mass spectrometry of membrane protein complexes. Nat. Meth. 10:1206–1208.CrossRefGoogle Scholar
  117. Howell, S.C., Mesleh, M.F., Opella, S.J. (2005) NMR structure determination of a membrane protein with two transmembrane helices in micelles: MerF of the bacterial mercury detoxification system. Biochemistry 44:5196–5206.CrossRefGoogle Scholar
  118. Imura, T., Tsukui, Y., Sakai, K., Sakai, H., Taira, T., Kitamoto, D. (2014a) Minimum amino acid residues of an α-helical peptide leading to lipid nanodisc formation. J. Oleo Sci. 63:1203–1208.CrossRefGoogle Scholar
  119. Imura, T., Tsukui, Y., Taira, T., Aburai, K., Sakai, K., Sakai, H., Abe, M., Kitamoto, D. (2014b) Surfactant-like properties of an amphiphilic α-helical peptide leading to lipid nanodisc formation. Langmuir 30:4752–4759.CrossRefGoogle Scholar
  120. Inagaki, S., Ghirlando, R. (2017) Nanodisc characterization by analytical ultracentrifugation. Nanotech. Rev. 6:3–14.Google Scholar
  121. Israelachvili, J.N. (2011) Intermolecular and surface forces, 3rd edition. Academic Press, London, 706 p.Google Scholar
  122. Israelachvili, J.N., Mitchell, D.J., Ninham, B.W. (1977) Theory of self-assembly of lipid bilayers and vesicles. Biochim. Biophys. Acta 470:185–201.CrossRefGoogle Scholar
  123. Johansson, L.C., Wöhri, A.B., Katona, G., Engström, S., Neutze, R. (2009) Membrane protein crystallization from lipidic phases. Curr. Opin. Struct. Biol. 19:372–378.CrossRefGoogle Scholar
  124. Johnson, P.J., Halpin, A., Morizumi, T., Brown, L.S., Prokhorenko, V.I., Ernst, O.P., Dwayne Miller, R.J. (2014) The photocycle and ultrafast vibrational dynamics of bacteriorhodopsin in lipid nanodiscs. Phys. Chem. Chem. Phys. 16:21310–21320CrossRefGoogle Scholar
  125. Johnson, Z.L., Chen, J. (2017) Structural basis of substrate recognition by the multidrug resistance protein MRP1. Cell 168:1075–1085.CrossRefGoogle Scholar
  126. Jonas, A. (1986) Reconstitution of high-density lipoproteins. Methods Enzymol. 128:553–582.CrossRefGoogle Scholar
  127. Jonas, A., Kezdy, K.E., Wald, J.H. (1989) Defined apolipoprotein A-I conformations in reconstituted high-density lipoprotein discs. J. Biol. Chem. 264:4818–4824.Google Scholar
  128. Jonas, A., von Eckardstein, A., Kézdy, K.E., Steinmetz, A., Assmann, G. (1991) Structural and functional properties of reconstituted high-density lipoprotein discs prepared with six apolipoprotein A-I variants. J. Lipid Res. 32:97–106.Google Scholar
  129. Jonas, A., Wald, J.H., Toohill, K.L., Krul, E.S., Kézdy, K.E. (1990) Apolipoprotein A-I structure and lipid properties in homogeneous, reconstituted spherical and discoidal high density lipoproteins. J. Biol. Chem. 265:22123–22129.Google Scholar
  130. Joubert, O., Nehmé, R., Bidet, M., Mus-Veteau, I. (2010) Heterologous expression of human membrane receptors in the yeast Saccharomyces cerevisiae, in: Mus-Veteau, I., ed., Heterologous expression of membrane proteins. Humana Press, New York, pp. 87–103.CrossRefGoogle Scholar
  131. Kang, C., Vanoye, C.G., Welch, R.C., Van Horn, W.D., Sanders, C.R. (2010) Functional delivery of a membrane protein into oocyte membranes using bicelles. Biochemistry 49:653–655.CrossRefGoogle Scholar
  132. Kang, Y., Zhou, X.E., Gao, X., He, Y., Liu, W., Ishchenko, A., Barty, A., White, T.A., Yefanov, O., Han, G.W., Xu, Q., deWaal, P.W., Ke, J., Tan, M.H.E., Zhang, C., Moeller, A., West, G.M., Pascal, B.D., Van Eps, N., Caro, L.N., Vishnivetskiy, S.A., Lee, R.J., Suino-Powell, K.M., Gu, X., Pal, K., Ma, J., Zhi, X., Boutet, S., Williams, G.J., Messerschmidt, M., Gati, C., Zatsepin, N.A., Wang, D., James, D., Basu, S., Roy-Chowdhury, S., Conrad, C.E., Coe, J., Liu, H., Lisova, S., Kupitz, C., Grotjohann, I., Fromme, R., Jiang, Y., Tan, M., Yang, H., Li, J., Wang, M., Zheng, Z., Li, D., Howe, N., Zhao, Y., Standfuss, J., Diederichs, K., Dong, Y., Potter, C.S., Carragher, B., Caffrey, M., Jiang, H., Chapman, H.N., Spence, J.C.H., Fromme, P., Weierstall, U., Ernst, O.P., Katritch, V., Gurevich, V.V., Griffin, P.R., Hubbell, W.L., Stevens, R.C., Cherezov, V., Melcher, K., Xu, E. (2015) Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523:561–567.CrossRefADSGoogle Scholar
  133. Kariyazono, H., Nadai, R., Miyajima, R., Takechi-Haraya, Y., Baba, T., Shigenaga, A., Okuhira, K., Otaka, A., Saito, H. (2016) Formation of stable nanodiscs by bihelical apolipoprotein A-I mimetic peptide. J. Pept. Sci. 22:116–122.CrossRefGoogle Scholar
  134. Katayama, H., Wang, J., Tama, F., Chollet, L., Gogol, E.P., Collier, R.J., Fisher, M.T. (2010) Three-dimensional structure of the anthrax toxin pore inserted into lipid nanodiscs and lipid vesicles. Proc. Natl. Acad. Sci. USA 107:3453–3457.CrossRefADSGoogle Scholar
  135. Katzen, F., Fletcher, J.E., Yang, J.P., Kang, D., Peterson, T.C., Cappuccio, J.A., Blanchette, C.D., Sulchek, T., Chromy, B.A., Hoeprich, P.D., Coleman, M.A., Kudlicki, W. (2008) Insertion of membrane proteins into discoidal membranes using a cell-free protein expression approach. J. Proteome Res. 7:3535–3542.CrossRefGoogle Scholar
  136. Kedrov, A., Wickles, S., Crevenna, A.H., van der Sluis, E.O., Buschauer, R., Berninghausen, O., Lamb, D.C., Beckmann, R. (2016) Structural dynamics of the YidC:ribosome complex during membrane protein biogenesis. Cell Rep. 17:2934–2954.CrossRefGoogle Scholar
  137. Kelly, E., Privé, G.G., Tieleman, P.D. (2005) Molecular models of lipopeptide detergents: large coiled-coils with hydrocarbon interiors. J. Am. Chem. Soc. 127:13446–13447.CrossRefGoogle Scholar
  138. Kennedy, G.L., Butenhoff, J.L., Olsen, G.W., O’Connor, J.C., Seacat, A.M., Perkins, R.G., Biegel, L.B., Murphy, S.R., Farrar, D.G. (2004) The toxicology of perfluorooctanoate. Crit. Rev. Toxicol. 34:351–384.CrossRefGoogle Scholar
  139. Ketchem, R., Hu, W., Cross, T.A. (1993) High-resolution conformation of gramicidin A in a lipid bilayer by solid state NMR. Science 261:1457–1460.CrossRefADSGoogle Scholar
  140. Kijac, A., Shih, A.Y., Nieuwkoop, A.J., Schulten, K., Sligar, S.G., Rienstra, C.M. (2010) Lipid-protein correlations in nanoscale phospholipid bilayers determined by solid-state nuclear magnetic resonance. Biochemistry 49:9190–9198.CrossRefGoogle Scholar
  141. Kijac, A.Z., Li, Y., Sligar, S.G., Rienstra, C.M. (2007) Magic-angle spinning solid-state NMR spectroscopy of nanodisc-embedded human CYP3A4. Biochemistry 46:13696–13703.CrossRefGoogle Scholar
  142. Kiley, P., Zhao, X., Vaughn, M., Baldo, M.A., Bruce, B.D., Zhang, S. (2005) Self-assembling peptide detergents stabilize isolated Photosystem I on a dry surface for an extended time. PLoS Biol. 3:e230.CrossRefGoogle Scholar
  143. Kim, H.M., Howell, S.C., Van Horn, W.D., Jeon, Y.H., Sanders, C.R. (2009) Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins. Progr. Nucl. Magn. Reson. Spectrosc. 55:335–360.CrossRefGoogle Scholar
  144. Kirsch, P. (2004) Modern fluoroorganic chemistry: synthesis, reactivity, applications. Wiley-VCH, Weinheim, 308 p.CrossRefGoogle Scholar
  145. Kissa, E. (1994) Structure of micelles and mesophases, in: Kissa, E., ed., Fluorinated Surfactants: Synthesis, Properties, Applications. Marcel Dekker, Inc., New York, pp. 264–282.Google Scholar
  146. Kissa, E. (2001) Fluorinated Surfactants and Repellents, 2nd ed.. Marcel Dekker, New York, 615 p.Google Scholar
  147. Koch, S., de Wit, J.G., Vos, I., Birkner, J.P., Gordiichuk, P., Herrmann, A., van Oijen, A.M., Driessen, A.J. (2016) Lipids activate SecA for high affinity binding to the SecYEG complex. J. Biol. Chem. 291:22534–22543.CrossRefGoogle Scholar
  148. Kolter, T., Sandhoff, K. (2005) Principles of lysosomal membrane digestion: Stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids. Annu. Rev. Cell Dev. Biol. 21:81–103.CrossRefGoogle Scholar
  149. Kondo, H., Ikeda, K., Nakano, M. (2016) Formation of size-controlled, denaturation-resistant lipid nanodiscs by an amphiphilic self-polymerizing peptide. Colloids Surf. B 146:423–430.CrossRefGoogle Scholar
  150. Koppaka, V., Silvestro, L., Engler, J.A., Brouillette, C.G., Axelsen, P.H. (1999) The structure of human lipoprotein A-I. Evidence for the “belt” model. J. Biol. Chem. 274:14541–14544.CrossRefGoogle Scholar
  151. Koutsopoulos, S., Kaiser, L., Eriksson, H.M., Zhang, S. (2012) Designer peptide surfactants stabilize diverse functional membrane proteins. Chem. Soc. Rev. 41:1721–1728.CrossRefGoogle Scholar
  152. Kraft, T.E., Hresko, R.C., Hruz, P.W. (2015) Expression, purification, and functional characterization of the insulin-responsive facilitative glucose transporter GLUT4. Protein Sci. 24:2008–2019.CrossRefGoogle Scholar
  153. Kreutz, J.E., Li, L., Roach, L.S., Hatakeyama, T., Ismagilov, R.F., Rustem, F. (2009) Laterally mobile, functionalized self-assembled monolayers at the fluorous-aqueous interface in a plug-based microfluidic system: Characterization and testing with membrane protein crystallization. J. Am. Chem. Soc. 131:6042–6043.CrossRefGoogle Scholar
  154. Kucharska, I., Edrington, T.C., Liang, B., Tamm, L.K. (2015) Optimizing nanodiscs and bicelles for solution NMR studies of two β-barrel membrane proteins. J. Biomol. NMR 61:261–274.CrossRefGoogle Scholar
  155. Kumar, R.B., Zhu, L., Idborg, H., Radmark, O., Jakobsson, P., Rinaldo-Matthis, A., Hebert, H., Jegerschold, C. (2016) Structural and functional analysis of calcium ion mediated binding of 5-lipoxygenase to nanodiscs. PLoS One 11:e0152116.CrossRefGoogle Scholar
  156. Kuszak, A.J., Pitchiaya, S., Anand, J.P., Mosberg, H.I., Walter, N.G., Sunahara, R.K. (2009) Purification and functional reconstitution of monomeric μ-opioid receptors: Allosteric modulation of agonist binding by Gi2. J. Biol. Chem. 284:26732–26741.CrossRefGoogle Scholar
  157. Kyrychenko, A., Rodnin, M.V., Posokhov, Y.O., Holt, A., Pucci, B., Killian, J.A., Ladokhin, A.S. (2012a) Thermodynamic measurements of bilayer insertion of a single transmembrane helix chaperoned by fluorinated surfactants. J. Mol. Biol. 416:328–334.CrossRefGoogle Scholar
  158. Kyrychenko, A., Rodnin, M.V., Vargas, M.U., Sharma, S.K., Durand, G., Pucci, B., Popot, J.-L., Ladokhin, A.S. (2012b) Folding of diphteria toxin T-domain in the presence of amphipols and fluorinated surfactants: Toward thermodynamic measurements of membrane protein folding. Biochim. Biophys. Acta 1818:1006–1012.CrossRefGoogle Scholar
  159. Lai, G., Forti, K.M., Renthal, R. (2015) Kinetics of lipid mixing between bicelles and nanolipoprotein particles. Biophys. J. 197:47–52.Google Scholar
  160. Lamichhane, R., Liu, J.J., Pljevaljcic, G., White, K.L., van der Schans, E., Katritch, V., Stevens, R.C., Wüthrich, K., Millar, D.P. (2015) Single-molecule view of basal activity and activation mechanisms of the G protein-coupled receptor β2AR. Proc. Natl. Acad. Sci. USA 112:14254–14259.CrossRefADSGoogle Scholar
  161. Landreh, M., Robinson, C.V. (2015) A new window into the molecular physiology of membrane proteins. J. Physiol. 593:355–362.CrossRefGoogle Scholar
  162. Larsen, A.N., Sorensen, K.K., Johansen, N.T., Martel, A., Kirkensgaard, J.J., Jensen, K.J., Arleth, L., Midtgaard, S.R. (2016) Dimeric peptides with three different linkers self-assemble with phospholipids to form peptide nanodiscs that stabilize membrane proteins. Soft Matter 12:5937–5949.CrossRefADSGoogle Scholar
  163. Lau, T.L., Partridge, A.W., Ginsberg, M.H., Ulmer, T.S. (2008) Structure of the integrin β3 transmembrane segment in phospholipid bicelles and detergent micelles. Biochemistry 47:4008–4016.CrossRefGoogle Scholar
  164. Laursen, T., Singha, A., Rantzau, N., Tutkus, M., Borch, J., Hedegård, P., Stamou, D., Møller, B.L., Hatzakis, N.S. (2014) Single molecule activity measurements of cytochrome P450 oxidoreductase reveal the existence of two discrete functional states. ACS Chem. Biol. 9:630–634.CrossRefGoogle Scholar
  165. Lebaupain, F. (2007) Développement de l’utilisation des tensioactifs fluorés pour la biochimie des protéines membranaires. Thèse de Doctorat, Université Paris-7, Paris, 254 p.Google Scholar
  166. Lebaupain, F., Salvay, A.G., Olivier, B., Durand, G., Fabiano, A.-S., Michel, N., Popot, J.-L., Ebel, C., Breyton, C., Pucci, B. (2006) Lactobionamide surfactants with hydrogenated, hemifluorinated or perfluorinated tails: Physical-chemical and biochemical characterization. Langmuir 22:8881–8890.CrossRefGoogle Scholar
  167. Lebeau, L., Lach, F., Venien-Bryan, C., Renault, A., Dietrich, J., Jahn, T., Palmgren, M.G., Kühlbrandt, W., Mioskowski, C. (2001) Two-dimensional crystallization of a membrane protein on a detergent-resistant lipid monolayer. J. Mol. Biol. 308:639–647.CrossRefGoogle Scholar
  168. Lee, D., Walter, K.F., Brückner, A.K., Hilty, C., Becker, S., Griesinger, C. (2008) Bilayer in small bicelles revealed by lipid-protein interactions using NMR spectroscopy. J. Am. Chem. Soc. 130:13822–13823.CrossRefGoogle Scholar
  169. Lee, H., Shingler, K.L., Organtini, L.J., Ashley, R.E., Makhov, A.M., Conway, J.F., Hafenstein, S. (2016) The novel asymmetric entry intermediate of a picornavirus captured with nanodiscs. Sci. Adv. 2:e1501929.CrossRefADSGoogle Scholar
  170. Legrand, F., Breyton, C., Guillet, P., Ebel, C., Durand, G. (2016) Hybrid fluorinated and hydrogenated double-chain surfactants for handling membrane proteins. J. Org. Chem. 81:681–688.CrossRefGoogle Scholar
  171. Leney, A.C., Rezaei Darestani, R., Li, J., Nikjah, S., Kitova, E.N., Zou, C., Cairo, C.W., Xiong, Z.J., Privé, G.G., Klassen, J.S. (2015) Picodiscs for facile protein-glycolipid interaction analysis. Anal. Chem. 87:4402–4408.CrossRefGoogle Scholar
  172. Lewis, B.A., Engelman, D.M. (1983) Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J. Mol. Biol. 166:211–217.CrossRefGoogle Scholar
  173. Li, J., Fan, X., Kitova, E.N., Zou, C., Cairo, C.W., Eugenio, L., Ng, K.K.S., Xiong, Z.J., Privé, G.G., Klassen, J.S. (2016a) Screening glycolipids against proteins in vitro using picodiscs and catch-and-release electrospray ionization-mass spectrometry. Anal. Chem. 88:4742–4750.CrossRefGoogle Scholar
  174. Li, J., Richards, M.R., Bagal, D., Campuzano, I.D.G., Kitova, E.N., Xiong, Z.J., Privé, G.G., Klassen, J.S. (2016b) Characterizing the size and composition of saposin A lipoprotein picodiscs. Anal. Chem. 88:9524–9531.CrossRefGoogle Scholar
  175. Li, L., Chen, J., Mishra, V.K., Kurtz, J.A., Cao, D., Klon, A.E., Harvey, S.C., Anantharamaiah, G.M., Segrest, J.P. (2004) Double belt structure of discoidal high density lipoproteins: molecular basis for size heterogeneity. J. Mol. Biol. 343:1293–1311.CrossRefGoogle Scholar
  176. Li, Y., Kijac, A.Z., Sligar, S.G., Rienstra, C.M. (2006) Structural analysis of nanoscale self-assembled discoidal lipid bilayers by solid-state NMR spectroscopy. Biophys. J. 91:3819–3828.CrossRefADSGoogle Scholar
  177. Liebau, J., Ye, W., Mäler, L. (2016) Characterization of fast-tumbling isotropic bicelles by PFG diffusion NMR. Magn. Reson. Chem. 55:395–404.CrossRefGoogle Scholar
  178. Lindberg, M., Biverståhl, H., Gräslund, A., Mäler, L. (2003) Structure and positioning comparison of two variants of penetratin in two different membrane mimicking systems by NMR. Eur. J. Biochem. 270:3055–3063.CrossRefGoogle Scholar
  179. Loll, P.J. (2014) Membrane proteins, detergents and crystals: what is the state of the art? Acta Crystallogr. F 70:1576–1583.CrossRefGoogle Scholar
  180. Luecke, H., Schobert, B., Stagno, J., Imasheva, E.S., Wang, J.M., Balashov, S.P., Lanyi, J.K. (2008) Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore. Proc. Natl. Acad. Sci. USA 105:16561–16565.CrossRefADSGoogle Scholar
  181. Lyukmanova, E.N., Shenkarev, Z.O., Khabibullina, N.F., Kopeina, G.S., Shulepko, M.A., Paramonov, A.S., Mineev, K.S., Tikhonov, R.V., Shingarova, L.N., Petrovskaya, L.E., Dolgikh, D.A., Arseniev, A.S., Kirpichnikov, M.P. (2011) Lipid-protein nanodisks for cell-free production of integral membrane proteins in a soluble and folded state: Comparison with detergent micelles, bicelles and liposomes. Biochim. Biophys. Acta 1818:349–358.CrossRefGoogle Scholar
  182. Mabrey, S., Sturtevant, J.M. (1976) Investigation of phase transitions of lipids and lipid mixtures by high-sensitivity differential scanning calorimetry. Proc. Natl. Acad. Sci. USA 73:3862–3866.CrossRefADSGoogle Scholar
  183. Mahalakshmi, R., Marassi, F.M. (2008) Orientation of the Escherichia coli outer membrane protein OmpX in phospholipid bilayer membranes determined by solid-State NMR. Biochemistry 47:6531–6538.CrossRefGoogle Scholar
  184. Mak, P.J., Gregory, M.C., Denisov, I.G., Sligar, S.G., Kincaid, J.R. (2015) Unveiling the crucial intermediates in androgen production. Proc. Natl. Acad. Sci. USA 112:15856–15861.CrossRefADSGoogle Scholar
  185. Mäler, L., Gräslund, A. (2009) Artificial membrane models for the study of macromolecular delivery. Meth. Mol. Biol. 480:129–139.CrossRefGoogle Scholar
  186. Malhotra, K., Alder, N.N. (2014) Advances in the use of nanoscale bilayers to study membrane protein structure and function. Biotechnol. Genet. Eng. Rev. 30:79–93.CrossRefGoogle Scholar
  187. Marcotte, I., Auger, M. (2005) Bicelles as model membranes for solid- and solution-state NMR studies of membrane peptides and proteins. Concepts Magn. Reson. 24A:17–37.CrossRefGoogle Scholar
  188. Marty, M.T., Hoi, K.K., Robinson, C.V. (2016) Interfacing membrane mimetics with mass spectrometry. Acc. Chem. Res. 49:2459–2467.CrossRefGoogle Scholar
  189. Marty, M.T., Wilcox, K.C., Klein, W.L., Sligar, S.G. (2013) Nanodisc-solubilized membrane protein library reflects the membrane proteome. Anal. Bioanal. Chem. 405:4009–4016.CrossRefGoogle Scholar
  190. Matsumoto, K., Vaughn, M., Bruce, B.D., Koutsopoulos, S., Zhang, S. (2009) Designer peptide surfactants stabilize functional photosystem I membrane complex in aqueous solution for extended time. J. Phys. Chem. B 113:75–83.CrossRefGoogle Scholar
  191. Matthies, D., Dalmas, O., Borgnia, M.J., Dominik, P.K., Merk, A., Rao, P., Reddy, B.G., Islam, S., Bartesaghi, A., Perozo, E., Subramaniam, S. (2016) Cryo-EM structures of the magnesium channel CorA reveal symmetry break upon gating. Cell 164:747–756.CrossRefGoogle Scholar
  192. McGregor, C.-L., Chen, L., Pomroy, N.C., Hwang, P., Go, S., Chakrabartty, A., Privé, G.G. (2003) Lipopeptide detergents designed for the structural study of membrane proteins. Nat. Biotechnol. 21:171–176.CrossRefGoogle Scholar
  193. McKibbin, C., Farmer, N.A., Edwards, P.C., Villa, C., Booth, P.J. (2009) Urea unfolding of opsin in phospholipid bicelles. Photochem. Photobiol. 85:494–500.CrossRefGoogle Scholar
  194. McKibbin, C., Farmer, N.A., Jeans, C., Reeves, P.J., Khorana, H.G., Wallace, B.A., Edwards, P.C., Villa, C., Booth, P.J. (2007) Opsin stability and folding: modulation by phospholipid bicelles. J. Mol. Biol. 374:1319–1332.CrossRefGoogle Scholar
  195. Midtgaard, S.R., Pedersen, M.C., Kirkensgaard, J.J.K., Sorensen, K.K., Mortensen, K., Jensen, K.J., Arleth, L. (2014) Self-assembling peptides form nanodiscs that stabilize membrane proteins. Soft Matter 10:738–752.CrossRefADSGoogle Scholar
  196. Mineev, K.S., Goncharuk, S.A., Kuzmichev, P.K., Vilar, M., Arseniev, A.S. (2015) NMR dynamics of transmembrane and intracellular domains of p75NTR in lipid-protein nanodiscs. Biophys. J. 109:772–782.CrossRefADSGoogle Scholar
  197. Mineev, K.S., Nadezhdin, K.D. (2017) Membrane mimetics for solution NMR studies of membrane proteins. Nanotech. Rev. 6:15–32.Google Scholar
  198. Mineev, K.S., Nadezhdin, K.D., Goncharuk, S.A., Arseniev, A.S. (2017) Facade detergents as bicelle rim-forming agents for solution NMR spectroscopy. Nanotech. Rev. 6:93–103.Google Scholar
  199. Mitra, N., Liu, Y., Liu, J., Serebryany, E., Mooney, V., DeVree, B.T., Sunahara, R.K., Yan, E.C.Y. (2013) Calcium-dependent ligand binding and G protein signaling of family B GPCR parathyroid hormone 1 receptor purified in nanodiscs. ACS Chem. Biol. 8:617–625.CrossRefGoogle Scholar
  200. Miyazaki, M., Nakano, M., Fukuda, M., Handa, T. (2009) Smaller discoidal high-density lipoprotein particles form saddle surfaces, but not planar bilayers. Biochemistry 48:7756–7763.CrossRefGoogle Scholar
  201. Mizrachi, D., Robinson, M.-P., Ren, G., Ke, N., Berkmen, M., DeLisa, M.P. (2017) A water-soluble DsbB variant that catalyzes disulfide-bond formation in vivo. Nat. Chem. Biol. 13:1022–1028.CrossRefGoogle Scholar
  202. Morgado, L., Zeth, K., Burmann, B.M., Maier, T., Hiller, S. (2015) Characterization of the insertase BamA in three different membrane mimetics by solution NMR spectroscopy. J. Biomol. NMR 61:333–345.CrossRefGoogle Scholar
  203. Morrison, E.A., DeKoster, G.T., Dutta, S., Vafabakhsh, R., Clarkson, M.W., Bahl, A., Kern, D., Ha, T., Henzler-Wildman, K.A. (2011) Antiparallel EmrE exports drugs by exchanging between asymmetric structures. Nature 481:45–50.CrossRefADSGoogle Scholar
  204. Morrison, E.A., Henzler-Wildman, K.A. (2012) Reconstitution of integral membrane proteins into isotropic bicelles with improved sample stability and expanded lipid composition profile. Biochim. Biophys. Acta 1818:814–820.CrossRefGoogle Scholar
  205. Mörs, K., Roos, C., Scholz, F., Wachtveitl, J., Dötsch, V., Bernhard, F., Glaubitz, C. (2013) Modified lipid and protein dynamics in nanodiscs. Biochim. Biophys. Acta 1828:1222–1229.CrossRefGoogle Scholar
  206. Mukerjee, P. (1994) Fluorocarbon-hydrocarbon interactions in micelles and other lipid assemblies, at interfaces, and in solutions. Colloids Surf. A 84:1–10.CrossRefGoogle Scholar
  207. Muller, K. (1981) Structural dimorphism in bile salt/lecithin mixed micelles. X-ray structural analysis. Biochemistry 20:404–414.CrossRefGoogle Scholar
  208. Nakano, T.Y., Sugihara, G., Nakashima, T., Yu, S.C. (2002) Thermodynamic study of mixed hydrocarbon/fluorocarbon surfactant system by conductometric and fluorimetric techniques. Langmuir 18:8777–8785.CrossRefGoogle Scholar
  209. Nasr, M.L., Baptista, D., Strauss, M., Sun, Z.J., Grigoriu, S., Huser, S., Plückthun, A., Hagn, F., Walz, T., Hogle, J.M., Wagner, G. (2017) Covalently circularized nanodiscs for studying membrane proteins and viral entry. Nat. Meth. 14:49–52.CrossRefGoogle Scholar
  210. Nath, A., Atkins, W.M., Sligar, S.G. (2007) Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins. Biochemistry 46:2059–2069.CrossRefGoogle Scholar
  211. Nath, A., Koo, P.K., Rhoades, E., Atkins, W.M. (2008) Allosteric effects on substrate dissociation from cytochrome P450 3A4 in nanodiscs observed by ensemble and single-molecule fluorescence spectroscopy. J. Am. Chem. Soc. 130:15746–15747.CrossRefGoogle Scholar
  212. Nehmé, 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 1786:1100–1110.CrossRefGoogle Scholar
  213. Nietlispach, D., Gautier, A. (2011) Solution NMR studies of polytopic alpha-helical membrane proteins. Curr. Opin. Struct. Biol. 21:497–508.CrossRefGoogle Scholar
  214. Nikolaev, M., Round, E., Gushchin, I., Polovinkin, V., Balandin, T., Kuzmichev, P., Shevchenko, V., Borshchevskiy, V., Kuklin, A., Round, A., Bernhard, F., Willbold, D., Büldt, G., Gordeliy, V. (2017) Integral membrane proteins can be crystallized directly from nanodiscs. Cryst. Growth Des. 17:945–948.CrossRefGoogle Scholar
  215. Noinaj, N., Kuszak, A.J., Gumbart, J.C., Lukacik, P., Chang, H., Easley, N.C., Lithgow, T., Buchanan, S.K. (2013) Structural insight into the biogenesis of β-barrel membrane proteins. Nature 501:385–390.CrossRefADSGoogle Scholar
  216. Nolte, R.T., Atkinson, D. (1992) Conformational analysis of apolipoproteins A-I and E-3 based on primary sequence and circular dichroism. Biophys. J. 63:1221–1239.CrossRefADSGoogle Scholar
  217. Nusair, N.A., Mayo, D.J., Dorozenski, T.D., Cardon, T.B., Inbaraj, J.J., Karp, E.S., Newstadt, J.P., Grosser, S.M., Lorigan, G.A. (2012) Time-resolved EPR immersion depth studies of a transmembrane peptide incorporated into bicelles. Biochim. Biophys. Acta 1818:821–828.CrossRefGoogle Scholar
  218. Opella, S.J., Marassi, F.M. (2004) Structure determination of membrane proteins by NMR spectroscopy. Chem. Rev. 104:3587–3606.CrossRefGoogle Scholar
  219. Otzen, D.E. (2015) Proteins in a brave new surfactant world. Curr. Opin. Colloid Interface Sci. 20:161–169.CrossRefGoogle Scholar
  220. Palchevskyy, S.S., Posokhov, Y.O., Olivier, B., Popot, J.-L., Pucci, B., Ladokhin, A.S. (2006) Chaperoning of membrane protein insertion into lipid bilayers by hemifluorinated surfactants: application to diphtheria toxin. Biochemistry 45:2629–2635.CrossRefGoogle Scholar
  221. Park, K.-H., Berrier, C., Lebaupain, F., Pucci, B., Popot, J.-L., Ghazi, A., Zito, F. (2007) Fluorinated and hemifluorinated surfactants as alternatives to detergents for membrane protein cell-free synthesis. Biochem. J. 403:183–187.CrossRefGoogle Scholar
  222. Park, K.-H., 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. New Biotech. 28:255–261.CrossRefGoogle Scholar
  223. Park, S.H., Berkamp, S., Cook, G.A., Chan, M.K., Viadiu, H., Opella, S.J. (2011a) Nanodiscs versus macrodiscs for NMR of membrane proteins. Biochemistry 50:8983–8985.CrossRefGoogle Scholar
  224. Park, S.H., Casagrande, F., Cho, L., Albrecht, L., Opella, S.J. (2011b) Interactions of interleukin-8 with the human chemokine receptor CXCR1 in phospholipid bilayers by NMR spectroscopy. J. Mol. Biol. 414:194–203.CrossRefGoogle Scholar
  225. Park, S.H., Casagrande, F., Das, B.B., Albrecht, L., Chu, M., Opella, S.J. (2011c) Local and global dynamics of the G protein-coupled receptor CXCR1. Biochemistry 50:2371–2380.CrossRefGoogle Scholar
  226. Park, S.H., Das, B.B., Casagrande, F., Tian, Y., Nothnagel, H.J., Chu, M., Kiefer, H., Maier, K., De Angelis, A.A., Marassi, F.M., Opella, S.J. (2012) Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491:770–783.ADSGoogle Scholar
  227. Park, S.H., Prytulla, S., De Angelis, A.A., Brown, J.M., Kiefer, H., Opella, S.J. (2006) High-resolution NMR spectroscopy of a GPCR in aligned bicelles. J. Am. Chem. Soc. 128:7402–7403.CrossRefGoogle Scholar
  228. Pavia, A.A., Pucci, B., Riess, J.G., Zarif, L. (1991) New fluorinated biocompatible non-ionic telomeric amphiphiles bearing trishydroxymethyl groups. Bioorg. Med. Chem. Letters 1:103–106.CrossRefGoogle Scholar
  229. Periasamy, A., Shadiac, N., Amalraj, A., Garajová, S., Nagarajan, Y., Waters, S., Mertens, H.D.T., Hrmova, M. (2013) Cell-free protein synthesis of membrane (1,3)-β-d-glucan (curdlan) synthase: co-translational insertion in liposomes and reconstitution in nanodiscs. Biochim. Biophys. Acta 1828:743–757.CrossRefGoogle Scholar
  230. Peters, B.M., Shirtliff, M.E., Jabra-Rizk, M.A. (2010) Antimicrobial peptides: Primeval molecules or future drugs? PLoS Pathog. 6:e1001067.CrossRefGoogle Scholar
  231. Petkova, V., Benattar, J.J., Zoonens, M., Zito, F., Popot, J.-L., Polidori, A., Jasseron, S., Pucci, B. (2007) Free-standing films of fluorinated surfactants as 2D matrices for organizing detergent-solubilized membrane proteins. Langmuir 23:4303–4309.CrossRefGoogle Scholar
  232. Phillips, J.C., Wriggers, W., Li, Z., Jonas, A., Schulten, K. (1997) Predicting the structure of apolipoprotein A-I in reconstituted high-density lipoprotein disks. Biophys. J. 73:2337–2346.CrossRefGoogle Scholar
  233. Phillips, M.C. (2013) New insights into the determination of HDL structure by apolipoproteins. J. Lipid Res. 54:2034–2048.CrossRefGoogle Scholar
  234. Poget, S.F., Cahill, S.M., Girvin, M.E. (2007) Isotropic bicelles stabilize the functional form of a small multidrug-resistance pump for NMR structural studies. J. Am. Chem. Soc. 129:2432–2433.CrossRefGoogle Scholar
  235. Poget, S.F., Girvin, M.E. (2007) Solution NMR of membrane proteins in bilayer mimics: small is beautiful, but sometimes bigger is better. Biochim. Biophys. Acta 1768:3098–3106.CrossRefGoogle Scholar
  236. Polidori, A., Presset, M., Lebaupain, F., Améduri, B., Popot, J.-L., Breyton, C., Pucci, B. (2006) Fluorinated and hemifluorinated surfactants derived from maltose: Synthesis and application to handling membrane proteins in aqueous solution. Bioorg. Med. Chem. Lett. 16:5827–5831.CrossRefGoogle Scholar
  237. Polidori, A., Raynal, S., Barret, L.-A., Dahani, M., Barrot-Ivolot, C., Jungas, C., Frotscher, E., Keller, S., Ebel, C., Breyton, C., Bonneté, F. (2016) Sparingly fluorinated maltoside-based surfactants for membrane-protein stabilization. New J. Chem. 40:5364–5378.CrossRefGoogle Scholar
  238. Polovinkin, V., Gushchin, I., Balandin, T., Chervakov, P., Round, E., Shevchenko, V., Popov, A., Borshchevskiy, V., Popot, J.-L., Gordeliy, V. (2014) High-resolution structure of a membrane protein transferred from amphipol to a lipidic mesophase. J. Membr. Biol. 247:997–1004.CrossRefGoogle Scholar
  239. Popot, J.-L. (2010) Amphipols, nanodiscs, and fluorinated surfactants: Three non-conventional approaches to studying membrane proteins in aqueous solutions. Annu. Rev. Biochem. 79:737–775.CrossRefGoogle Scholar
  240. Popot, J.-L., Engelman, D.M. (2000) Helical membrane protein folding, stability and evolution. Annu. Rev. Biochem. 69:881–923.CrossRefGoogle Scholar
  241. Popovic, K., Holyoake, J., Pomès, R., Privé, G.G. (2012) Structure of saposin A lipoprotein discs. Proc. Natl. Acad. Sci. USA 109:2908–2912.CrossRefADSGoogle Scholar
  242. Posokhov, Y.O., Rodnin, M.V., Das, S.K., Pucci, B., Ladokhin, A.S. (2008) FCS study of the thermodynamics of membrane protein insertion into the lipid bilayer chaperoned by fluorinated surfactants. Biophys. J. 95:L54-L56.CrossRefGoogle Scholar
  243. Poulos, S., Morgan, J.L., Zimmer, J., Faham, S. (2015) Bicelles coming of age: an empirical approach to bicelle crystallization. Meth. Enzymol. 557:393–416.CrossRefGoogle Scholar
  244. Privé, G. (2009) Lipopeptide detergents for membrane protein studies. Curr. Opin. Struct. Biol. 19:1–7.CrossRefGoogle Scholar
  245. Prosser, R.S., Evanics, F., Kitevski, J.L., Al-Abdul-Wahid, M.S. (2006) Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins. Biochemistry 45:8453–8465.CrossRefGoogle Scholar
  246. Prosser, R.S., Hunt, S.A., DiNatale, J.A., Vold, R.R. (1996) Magnetically aligned membrane model systems with positive order parameters: switching the sign of Szz with paramagnetic ions. J. Am. Chem. Soc. 118:269–270.CrossRefGoogle Scholar
  247. Prosser, R.S., Hwang, J.S., Vold, R.R. (1998) Magnetically aligned phospholipid bilayers with positive ordering: a new model membrane system. Biophys. J. 74:2405–2418.CrossRefADSGoogle Scholar
  248. Proverbio, D., Roos, C., Beyermann, M., Orbán, E., Dötsch, V., Bernhard, F. (2013) Functional properties of cell-free expressed human endothelin A and endothelin B receptors in artificial membrane environments. Biochim. Biophys. Acta 1828:2182–2192.CrossRefGoogle Scholar
  249. Puthenveetil, R., Nguyen, K., Vinogradova, O. (2017) Nanodiscs and solution NMR: preparation, application and challenges. Nanotech. Rev. 6:111–126.Google Scholar
  250. Puthenveetil, R., Vinogradova, O. (2013) Optimization of the design and preparation of nanoscale phospholipid bilayers for its application to solution NMR. Proteins: Struct. Funct. Bioinf. 81:1222–1231.CrossRefGoogle Scholar
  251. Qureshi, T., Goto, N.K. (2011) Contemporary methods in structure determination of membrane proteins by solution NMR. Top. Curr. Chem. 326:123–185.CrossRefGoogle Scholar
  252. Ram, P., Prestegard, J.H. (1988) Magnetic field-induced ordering of bile salt/phospholipid micelles: new media for NMR structural investigations. Biochim. Biophys. Acta 940:289–294.CrossRefGoogle Scholar
  253. Ramjeesingh, M., Huan, L.J., Garami, E., Bear, C.E. (1999) Novel method for evaluation of the oligomeric structure of membrane proteins. Biochem. J. 342.CrossRefGoogle Scholar
  254. Ranaghan, M.J., Schwall, C.T., Alder, N.N., Birge, R.R. (2011) Green proteorhodopsin reconstituted into nanoscale phospholipid bilayers (nanodiscs) as photoactive monomers. J. Am. Chem. Soc. 133:18318–18327.CrossRefGoogle Scholar
  255. Raschle, T., Hiller, S., Etzkorn, M., Wagner, G. (2010) Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Curr. Opin. Struct. Biol. 20:471–479.CrossRefGoogle Scholar
  256. Raschle, T., Hiller, S., Yu, T.Y., Rice, A.J., Walz, T., Wagner, G. (2009) Structural and functional characterization of the integral membrane protein VDAC-1 in lipid bilayer nanodiscs. J. Am. Chem. Soc. 131:17777–17779.CrossRefGoogle Scholar
  257. Rasmussen, S.G., Choi, H.J., Rosenbaum, D.M., Kobilka, T.S., Thian, F.S., Edwards, P.C., Burghammer, M., Ratnala, V.R., Sanishvili, R., Fischetti, R.F., Schertler, G.F., Weis, W.I., Kobilka, B.K. (2007) Crystal structure of the human β2 adrenergic G protein-coupled receptor. Nature 450:383–387.CrossRefADSGoogle Scholar
  258. Raychaudhuri, P., Li, Q., Mason, A., Mikhailova, E., Heron, A.J., Bayley, H. (2011) Fluorinated amphiphiles control the insertion of α-hemolysin pores into lipid bilayers. Biochemistry 50:1599–1606.CrossRefGoogle Scholar
  259. Reichart, T.M., Baksh, M.M., Rhee, J.-K., Fiedler, J.D., Sligar, S.G., Finn, M.G., Zwick, M.B., Dawson, P.E. (2016) Trimerization of the HIV transmembrane domain in lipid bilayers modulates broadly neutralizing antibody binding. Angew. Chem. Int. Ed. 55:2688–2692.CrossRefGoogle Scholar
  260. Riess, J.G. (2005) Fluorous materials for biomedical uses, in: Gladysz, J.A., Curran, D.P., Horváth, I.T., eds., Handbook of fluorous chemistry. Wiley-VCH, Weinheim, pp. 521–573.CrossRefGoogle Scholar
  261. Ritchie, T.K., Grinkova, Y.V., Bayburt, T.H., Denisov, I.G., Zolnerciks, J.K., Atkins, W.M., Sligar, S.G. (2009) Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Meth. Enzymol. 464:211–231.CrossRefGoogle Scholar
  262. Ritchie, T.K., Kwon, H., Atkins, W.M. (2011) Conformational analysis of human ATP-binding cassette transporter ABCB1 in lipid nanodiscs and inhibition by the antibodies MRK16 and UIC2. J. Biol. Chem. 286:39489–39496.CrossRefGoogle Scholar
  263. Rodnin, M.V., Posokhov, Y.O., Contino-Pépin, C., Brettmann, J., Kyrychenko, A., Palchevskyy, S.S., Pucci, B., Ladokhin, A.S. (2008) Interactions of fluorinated surfactants with diphtheria toxin T-domain: testing new media for studies of membrane proteins. Biophys. J. 94:4348–4357.CrossRefADSGoogle Scholar
  264. Roos, C., Zocher, M., Müller, D., Münch, D., Schneider, T., Sahl, H.G., Scholz, F., Wachtveitl, J., Ma, Y., Proverbio, D., Henrich, E., Dötsch, V., Bernhard, F. (2012) Characterization of co-translationally formed nanodisc complexes with small multidrug transporters, proteorhodopsin and with the E. coli MraY translocase. Biochim. Biophys. Acta 1818:3898–3106.Google Scholar
  265. Roy, J., Pondenis, H., Fan, T.M., Das, A. (2015) Direct capture of functional proteins from mammalian plasma membranes into nanodiscs. Biochemistry 54:6299–6302.CrossRefGoogle Scholar
  266. Rues, R.-B., Dötsch, V., Bernhard, F. (2016) Co-translational formation and pharmacological characterization of β-adrenergic receptor/nanodisc complexes with different lipid environments. Biochim. Biophys. Acta 1858:1306–1316.CrossRefGoogle Scholar
  267. Sanders, C.R. (2008) Development and application of bicelles for use in biological NMR and other biophysical studies, in: Webb, G.A., ed., Modern Magnetic Resonance. Springer, Dordrecht, pp. 233–239.Google Scholar
  268. Sanders, C.R., Prosser, R.S. (1998) Bicelles: a model membrane system for all seasons? Structure 6:1227–1234.CrossRefGoogle Scholar
  269. Sanders, C.R., Schwonek, J.P. (1992) Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry 31:8898–8905.CrossRefGoogle Scholar
  270. Sanders, C.R., Sönnichsen, F. (2006) Solution NMR of membrane proteins: practice and challenges. Magn. Reson. Chem. 44:S24–S40.CrossRefGoogle Scholar
  271. Sanders II, C.R., Hare, B.J., Howard, K.P., Prestegard, J.H. (1994) Magnetically-oriented phospholipid micelles as a tool for the study of membrane-associated molecules. Prog. NMR Spectrosc. 26:421–444.CrossRefGoogle Scholar
  272. Sanders II, C.R., Landis, G.C. (1995) Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies. Biochemistry 34:4030–4040.CrossRefGoogle Scholar
  273. Sanders II, C.R., Prestegard, J.H. (1990) Magnetically orientable phospholipid bilayers containing small amounts of a bile salt analogue, CHAPSO. Biophys. J. 58:447–460.CrossRefGoogle Scholar
  274. Sanii, L.S., El-Sayed, M.A. (2005) Partial dehydration of the retinal binding pocket and proof for photochemical deprotonation of the retinal Schiff base in bicelle bacteriorhodopsin crystals. Photochem. Photobiol. 81:1356–1360.CrossRefGoogle Scholar
  275. Sanii, L.S., Schill, A.W., Moran, C.E., El-Sayed, M.A. (2005) The protonation-deprotonation kinetics of the protonated Schiff base in bicelle bacteriorhodopsin crystals. Biophys. J. 89:444–451.CrossRefADSGoogle Scholar
  276. Santoso, S., Hwang, W., Hartman, H., Zhang, S. (2002) Self-assembly of surfactant-like peptides with variable glycine tails to form nanotubes and nanovesicles. Nano Lett. 2:687–691.CrossRefADSGoogle Scholar
  277. Schafmeister, C.E., Miercke, L.J.W., Stroud, R.A. (1993) Structure at 2.5 Å of a designed peptide that maintains solubility of membrane proteins. Science 262:734–738.CrossRefADSGoogle Scholar
  278. Schoch, G.A., Attias, R., Belghazi, M., Dansette, P.M., Werck-Reichhart, D. (2003) Engineering of a water-soluble plant cytochrome P450, CYP73A1, and NMR-based orientation of natural and alternate substrates in the active site. Plant Physiol. 133:1198–1208.CrossRefGoogle Scholar
  279. Segrest, J.P., Jones, M.K., Klon, A.E., Sheldahl, C.J., Hellinger, M., De Loof, H., Harvey, S.C. (1999) A detailed molecular belt model for apolipoprotein A-I in discoidal high-density lipoprotein. J. Biol. Chem. 274:31755–31758.CrossRefGoogle Scholar
  280. Serebryany, E., Zhu, G.A., Yan, E.C.Y. (2012) Artificial membrane-like environments for in vitro studies of purified G-protein coupled receptors. Biochim. Biophys. Acta 1818:225–233.CrossRefGoogle Scholar
  281. Sevugan Chetty, P., Mayne, L., Kan, Z.Y., Lund-Katz, S., Englander, S.W., Phillips, M.C. (2012) Apolipoprotein A-I helical structure and stability in discoidal high density lipoprotein (HDL) particles by hydrogen exchange and mass spectrometry. Proc. Natl. Acad. Sci. USA 109:11687–11692.CrossRefADSGoogle Scholar
  282. Shaw, A.W., McLean, M.A., Sligar, S.G. (2004) Phospholipid phase transitions in homogeneous nanometer scale bilayers discs. FEBS Lett. 556:260–264.CrossRefGoogle Scholar
  283. Shaw, A.W., Pureza, V.S., Sligar, S.G., Morrissey, J.H. (2007) The local phospholipid environment modulates the activation of blood clotting. J. Biol. Chem. 282:6556–6563.CrossRefGoogle Scholar
  284. Shen, P.S., Yang, X., DeCaen, P.G., Liu, X., Bulkley, D., Clapham, D.E., Cao, E. (2016) The structure of the Polycystic Kidney Disease channel PKD2 in lipid nanodiscs. Cell 167:763–773.CrossRefGoogle Scholar
  285. Shenkarev, Z.O., Lyukmanova, E.N., Butenko, I.O., Petrovskaya, L.E., Paramonov, A.S., Shulepko, M.A., Nekrasova, O.V., Kirpichnikov, M.P., Arseniev, A.S. (2013) Lipid-protein nanodiscs promote in vitro folding of transmembrane domains of multi-helical and multimeric membrane proteins. Biochim. Biophys. Acta 1828:776–784.CrossRefGoogle Scholar
  286. Shenkarev, Z.O., Lyukmanova, E.N., Paramonov, A.S., Shingarova, L.N., Chupin, V.V., Kirpichnikov, M.P., Blommers, M.J., Arseniev, A.S. (2010) Lipid-protein nanodiscs as reference medium in detergent screening for high-resolution NMR studies of integral membrane proteins. J. Am. Chem. Soc. 132:5628–5629.CrossRefGoogle Scholar
  287. Shepherd, F.H., Holzenburg, A. (1995) The potential of fluorinated surfactants in membrane biochemistry. Anal. Biochem. 224:21–27.CrossRefGoogle Scholar
  288. Shi, L., Howan, K., Shen, Q.T., Wang, Y.J., Rothman, J.E., Pincet, F. (2013) Preparation and characterization of SNARE-containing nanodiscs and direct study of cargo release through fusion pores. Nat. Protoc. 8:935–948.CrossRefGoogle Scholar
  289. Shi, L., Shen, Q.T., Kiel, A., Wang, J., Wang, H.W., Melia, T.J., Rothman, J.E., Pincet, F. (2012) SNARE proteins: one to fuse and three to keep the nascent fusion pore open. Science 335:1355–1359.CrossRefADSGoogle Scholar
  290. Shih, A.Y., Denisov, I.G., Phillips, J.C., Sligar, S.G., Schulten, K. (2005) Molecular dynamics simulations of discoidal bilayers assembled from truncated human lipoproteins. Biophys. J. 88:548–556.CrossRefADSGoogle Scholar
  291. Shimada, S., Shinzawa-Itoh, K., Baba, J., Aoe, S., Shimada, A., Yamashita, E., Kang, J., Tateno, M., Yoshikawa, S., Tsukihara, T. (2017) Complex structure of cytochrome c-cytochrome c oxidase reveals a novel protein-protein interaction mode. EMBO J. 36:291–300.CrossRefGoogle Scholar
  292. Shin, J., Lou, X., Kweon, D.-H., Shin, Y.-K. (2014) Multiple conformations of a single SNAREpin between two nanodisc membranes reveal diverse pre-fusion states. Biochem. J. 459:95–102.CrossRefGoogle Scholar
  293. Shirzad-Wasei, N., Oostrum, J.V., Bovee-Geurts, P.H., Kusters, L.J., Bosman, G.J., DeGrip, W.J. (2015) Rapid transfer of overexpressed integral membrane protein from the host membrane into soluble lipid nanodiscs without previous purification. Biol. Chem. 396:903–916.CrossRefGoogle Scholar
  294. Singh, R., Flowers, R.A., II (2010) Efficient protein renaturation using tunable hemifluorinated anionic surfactants as additives. Chem. Commun. 46:276–278.CrossRefGoogle Scholar
  295. Siuda, I., Tieleman, D.P. (2015) Molecular models of nanodiscs. J. Chem. Theory Comput. 11:4923–4932.CrossRefGoogle Scholar
  296. Skar-Gislinge, N., Kynde, S.A., Denisov, I.G., Ye, X., Lenov, I., Sligar, S.G., Arleth, L. (2015) Small-angle scattering determination of the shape and localization of human cytochrome P450 embedded in a phospholipid nanodisc environment. Acta Crystallogr. D Biol. Crystallogr. 71:2412–2421.CrossRefGoogle Scholar
  297. Small, D.M. (1971) The physical chemistry of cholanic acids, in: P.P. Nair & D. Kritchevsky, eds., The Bile Acids, Plenum Press, pp. 249–356.CrossRefGoogle Scholar
  298. Smrt, S.T., Draney, A.W., Singaram, I., Lorieau, J.L. (2017) Structure and dynamics of membrane proteins and membrane associated proteins with native bicelles from eukaryotic tissues. Biochemistry 56:5318–5327.CrossRefGoogle Scholar
  299. Sobolev, V., Edelman, M., Dym, O., Unger, T., Albeck, S., Kirma, M., Galili, G. (2013) Structure of ALD1, a plant-specific homologue of the universal diaminopimelate aminotransferase enzyme of lysine biosynthesis. Acta Crystallogr. F 69:84–89.CrossRefGoogle Scholar
  300. Soomets, U., Kairane, C., Zilmer, M., Langel, U. (1997) Attempt to solubilize Na+/K+-exchanging ATPase with amphiphilic peptide PD1. Acta. Chem. Scand. 51:403–406.CrossRefGoogle Scholar
  301. Starita-Geribaldi, M., Thebault, P., Taffin de Givenchy, E., Guittard, F., Geribaldi, S. (2007) 2-DE using hemi-fluorinated surfactants. Electrophoresis 28:2489–2497.CrossRefGoogle Scholar
  302. Sternin, E., Nizza, D., Gawrisch, K. (2001) Temperature dependence of DMPC/DHPC mixing in a bicellar solution and its structural implications. Langmuir 17:2610–2616.CrossRefGoogle Scholar
  303. Talbot, J.-C., Dautant, A., Polidori, A., Pucci, B., Cohen-Bouhacina, T., Maali, A., Salin, B., Brèthes, D., Velours, J., Giraud, M.-F. (2009) Hydrogenated and fluorinated surfactants derived from tris(hydroxymethyl)-acrylamidomethane allow the purification of a highly active yeast F1FO ATP synthase with an enhanced stability. J. Bioenerg. Biomemb. 41:349–360.CrossRefGoogle Scholar
  304. Tanford, C. (1980) The hydrophobic effect: formation of micelles and biological membranes, 2nd ed.. John Wiley & Sons, New York, 233 p.Google Scholar
  305. Tao, H., Lee, S.C., Moeller, A., Roy, R.S., Siu, F.Y., Zimmermann, J., Stevens, R.C., Potter, C.S., Carragher, B., Zhang, Q. (2013) Engineered nanostructured β-sheet peptides protect membrane proteins. Nat. Methods 10:759–761.CrossRefGoogle Scholar
  306. Taufik, I., Kedrov, A., Exterkate, M., Driessen, A.J.M. (2013) Monitoring the activity of single translocons. J. Mol. Biol. 425:4145–4153.CrossRefGoogle Scholar
  307. Thebault, P., Taffin de Givenchy, E., Starita-Geribaldi, M., Guittard, F., Geribaldi, S. (2007) Synthesis and surface properties of new semifluorinated sulfobetaines potentially usable for 2D-electrophoresis. J. Fluorine Chem. 128:211–218.CrossRefGoogle Scholar
  308. Tiburu, E.K., Moton, D.M., Lorigan, G.A. (2001) Development of magnetically aligned phospholipid bilayers in mixtures of palmitoylstearoylphosphatidylcholine and dihexanoylphosphatidylcholine by solid-state NMR spectroscopy. Biochim. Biophys. Acta 1512:206–214.CrossRefGoogle Scholar
  309. Triba, M.N., Warschawski, D.E., Devaux, P.F. (2005) Reinvestigation by phosphorus NMR of lipid distribution in bicelles. Biophys. J. 88:1887–1901.CrossRefGoogle Scholar
  310. Triba, M.N., Zoonens, M., Popot, J.-L., Devaux, P.F., Warschawski, D.E. (2006) Reconstitution and alignment by a magnetic field of a β-barrel membrane protein in bicelles. Eur. Biophys. J. 35:268–275.CrossRefGoogle Scholar
  311. Tsukamoto, H., Szundi, I., Lewis, J.W., Farrens, D.L., Kliger, D.S. (2011) Rhodopsin in nanodiscs has native membrane-like photointermediates. Biochemistry 50:5086–5091.CrossRefGoogle Scholar
  312. Tu, Y., Peng, F., Adawy, A., Men, Y., Abdelmohsen, L.K.E.A., Wilson, D.A. (2016) Mimicking the cell: bio-Inspired functions of supramolecular assemblies. Chem. Rev. 116:2023–2078.CrossRefGoogle Scholar
  313. Tzitzilonis, C., Eichmann, C., Maslennikov, I., Choe, S., Riek, R. (2013) Detergent/nanodisc screening for high-resolution NMR studies of an integral membrane protein containing a cytoplasmic domain. PLoS One 8:e54378.CrossRefADSGoogle Scholar
  314. Uhlemann, E.M., Pierson, H.E., Fillingame, R.H., Dmitriev, O.Y. (2012) Cell-free synthesis of membrane subunits of ATP synthase in phospholipid bicelles: NMR shows subunit fold similar to the protein in the cell membrane. Prot. Sci. 21:279–288.CrossRefGoogle Scholar
  315. Ujwal, R., Bowie, J.U. (2011) Crystallizing membrane proteins using lipidic bicelles. Methods 55:337–341.CrossRefGoogle Scholar
  316. Ujwal, R., Cascio, D., Colletier, J.-P., Faham, S., Zhang, J., Toro, L., Ping, P., Abramson, J. (2008) The crystal structure of mouse VDAC1 at 2.3 Å resolution reveals mechanistic insights into metabolite gating. Proc. Natl. Acad. Sci. USA 105:17742–17747.CrossRefADSGoogle Scholar
  317. van Dam, L., Karlsson, G., Edwards, K. (2006) Morphology of magnetically aligning DMPC/DHPC aggregates – perforated sheets, not disks. Langmuir 22:3280–3285.CrossRefGoogle Scholar
  318. Vargas, C., Cuevas Arenas, R., Frotscher, E., Keller, S. (2015) Nanoparticle self-assembly in mixtures of phospholipids with styrene/maleic acid copolymers or fluorinated surfactants. Nanoscale 7:20685–20696.CrossRefADSGoogle Scholar
  319. Varkey, J., Mizuno, N., Hegde, B.G., Cheng, N., Steven, A.C., Langen, R. (2013) α-Synuclein oligomers with broken helical conformation form lipoprotein nanoparticles. J. Biol. Chem. 288:17620–17630.CrossRefGoogle Scholar
  320. Vauthey, S., Santoso, S., Gong, H., Watson, N., Zhang, S. (2002) Molecular self-assembly of surfactant-like peptides to form nanotubes and nanovesicles. Proc. Natl. Acad. Sci. USA 99:5355–5360.CrossRefADSGoogle Scholar
  321. Vénien-Bryan, C., Balavoine, F., Toussaint, B., Mioskowski, C., Hewat, E., Helme, B., Vignais, P. (1997) Structural study of the response regulator HupR from Rhodobacter capsulatus. Electron microscopy of 2D crystals on a nickel-chelating lipid. J. Mol. Biol. 274:687–692.CrossRefGoogle Scholar
  322. Vestergaard, M., Kraft, J.F., Vosegaard, T., Thøgersen, L., Schiøtt, B. (2015) Bicelles and other membrane mimics: Comparison of structure, properties, and dynamics from MD simulations. J. Phys. Chem. B 119:15831–15843.CrossRefGoogle Scholar
  323. Viegas, A., Viennet, T., Etzkorn, M. (2016) The power, pitfalls and potential of the nanodisc system for NMR-based studies. Biol. Chem. 397:1335–1354.CrossRefGoogle Scholar
  324. Vinothkumar, K.R. (2011) Structure of rhomboid protease in a lipid environment. J. Mol. Biol. 407:232–247.CrossRefGoogle Scholar
  325. Vold, R.R., Prosser, R.S. (1996) Magnetically oriented phospholipid bilayered micelles for structural studies of polypeptides. Does the ideal bicelle exist? J. Magn. Reson. B113:267–271.CrossRefGoogle Scholar
  326. von Maltzahn, G., Vauthey, S., Santoso, S., Zhang, S. (2003) Positively charged surfactant-like peptides self-assemble into nanostructures. Langmuir 19:4332–4337.CrossRefGoogle Scholar
  327. Wadsäter, M., Laursen, T., Singha, A., Hatzakis, N.S., Stamou, D., Barker, R., Mortensen, K., Feidenhans’l, R., Møller, B.L., Cárdenas, M. (2012) Monitoring shifts in the conformation equilibrium of the membrane protein cytochrome P450 reductase (POR) in nanodiscs. J. Biol. Chem. 287:34596–34603.CrossRefGoogle Scholar
  328. Wald, J.H., Goormaghtigh, E., De Meutter, J., Ruysschaert, J.M., Jonas, A. (1990a) Investigation of the lipid domains and apolipoprotein orientation in reconstituted high-density lipoproteins by fluorescence and IR methods. J. Biol. Chem.:20044–20050.Google Scholar
  329. Wald, J.H., Krul, E.S., Jonas, A. (1990b) Structure of apolipoprotein A-I in three homogeneous, reconstituted high-density lipoprotein particles. J. Biol. Chem. 265:20037–20043.Google Scholar
  330. Wang, G. (2008) NMR of membrane-associated peptides and proteins. Curr. Protein Pept. Sci. 9:50–69.CrossRefGoogle Scholar
  331. Wang, X., Mu, Z., Li, Y., Bi, Y., Wang, Y. (2015) Smaller nanodiscs are suitable for studying protein lipid interactions by solution NMR. Protein J. 34:205–211.CrossRefGoogle Scholar
  332. Wang, X.Q., Corin, K., Baaske, P., Wienken, C.J., Jerabek-Willemsen, M., Duhr, S., Braun, D., Zhang, S.G. (2011) Peptide surfactants for cell-free production of functional G protein-coupled receptors. Proc. Natl. Acad. Sci. USA 108:9049–9054.CrossRefADSGoogle Scholar
  333. Warschawski, D.E., Arnold, A.A., Beaugrand, M., Gravel, A., Chartrand, E., Marcotte, I. (2011) Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim. Biophys. Acta 1808:1957–1974.CrossRefGoogle Scholar
  334. Wilcox, K.C., Marunde, M.R., Das, A., Velasco, P.T., Kuhns, B.D., Marty, M.T., Jiang, H., Luan, C.H., Sligar, S.G., Klein, W.L. (2015) Nanoscale synaptic membrane mimetic allows unbiased high-throughput screen that targets binding sites for Alzheimer’s-associated Ab oligomers. PLoS One 10:e0125263.CrossRefGoogle Scholar
  335. Wlodawer, A., Segrest, J.P., Chung, B.H., Chiovetti, R., Jr., Weinstein, J.N. (1979) High-density lipoprotein recombinants: evidence for a bicycle tire micelle structure obtained by neutron scattering and electron microscopy. FEBS Lett. 104:231–235.CrossRefGoogle Scholar
  336. Xu, X.P., Zhai, D., Kim, E., Swift, M., Reed, J.C., Volkmann, N., Hanein, D. (2013) Three-dimensional structure of Bax-mediated pores in membrane bilayers. Cell Death Dis. 4:e683.CrossRefGoogle Scholar
  337. Yang, J.P., Cirico, T., Katzen, F., Peterson, T.C., Kudlicki, W. (2011) Cell-free synthesis of a functional G protein-coupled receptor complexed with nanometer scale bilayer discs. BMC Biotechnol. 11:57.CrossRefGoogle Scholar
  338. Yang, S.J., Zhang, S.G. (2006) Self-assembling behavior of designer lipid-like peptides. Supramol. Chem. 18:389–396.CrossRefGoogle Scholar
  339. Ye, F., Hu, G., Taylor, D., Ratnikov, B., Bobkov, A.A., McLean, M.A., Sligar, S.G., Taylor, K.A., Ginsberg, M.H. (2010) Recreation of the terminal events in physiological integrin activation. J. Cell Biol. 188:157–173.CrossRefGoogle Scholar
  340. Yeh, J.I., Du, S., Tortajada, A., Paulo, J., Zhang, S. (2005) Peptergents: peptide detergents that improve stability and functionality of a membrane protein, glycerol-3-phosphate dehydrogenase. Biochemistry 44:16912–16919.CrossRefGoogle Scholar
  341. Yoon, J.Y., Kim, J., An, D.R., Lee, S.J., Kim, H.S., Im, H.N., Yoon, H.J., Kim, J.Y., Kim, S.J., Han, B.W., Suh, S.W. (2013) Structural and functional characterization of HP0377, a thioredoxin-fold protein from Helicobacter pylori. Acta Crystallogr. D 69:735–746.CrossRefGoogle Scholar
  342. Zhang, M., Huang, R., Ackermann, R., Im, S.-C., Waskell, L., Schwendeman, A., Ramamoorthy, A. (2016) Reconstitution of the Cytb5-CytP450 complex in nanodiscs for structural studies using NMR. Angew. Chem. Int. Ed. Engl. 55:4497–4499.CrossRefGoogle Scholar
  343. Zhang, P., Ye, F., Bastidas, A.C., Kornev, A.P., Wu, J., Ginsberg, M.H., Taylor, S.S. (2015) An isoform-specific myristylation switch targets Type II PKA holoenzymes to membranes. Structure 23:1563–1572.CrossRefGoogle Scholar
  344. Zhang, Q., Tao, H., Hong, W.-X. (2011) New amphiphiles for membrane protein structural biology. Methods 55:318–323.CrossRefGoogle Scholar
  345. Zhang, Z., Chen, J. (2016) Atomic structure of the cystic fibrosis transmembrane conductance regulator. Cell 167:1586–1597.CrossRefGoogle Scholar
  346. Zhao, X., Nagai, Y., Reeves, P.J., Kiley, P., Khorana, H.G., Zhang, S. (2006) Designer short peptide surfactants stabilize G protein-coupled receptor bovine rhodopsin. Proc. Natl. Acad. Sci. USA 103:17707–17712.CrossRefADSGoogle Scholar
  347. Zhao, Y., Imura, T., Leman, L.J., Curtiss, L.K., Maryanoff, B.E., Ghadiri, M.R. (2013) Mimicry of high-density lipoprotein: functional peptide-lipid nanoparticles based on multivalent peptide constructs. J. Am. Chem. Soc. 133:13414–13424.CrossRefGoogle Scholar
  348. Zocher, M., Roos, C., Wegmann, S., Bosshart, P.D., Dötsch, V., Bernhard, F., Müller, D.J. (2012) Single-molecule force spectroscopy from nanodiscs: An assay to quantify folding, stability, and interactions of native membrane proteins. ACS Nano 6:961–971.CrossRefGoogle Scholar
  349. Zoghbi, M.E., Altenberg, G.A. (2017) Membrane protein reconstitution in nanodiscs for luminescence spectroscopy studies. Nanotech. Rev. 6:33–46.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Jean-Luc Popot
    • 1
  1. 1.Institut de Biologie Physico-ChimiqueParisFrance

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