Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter July 23, 2016

The power, pitfalls and potential of the nanodisc system for NMR-based studies

  • Aldino Viegas ORCID logo , Thibault Viennet and Manuel Etzkorn ORCID logo EMAIL logo
From the journal Biological Chemistry

Abstract

The choice of a suitable membrane mimicking environment is of fundamental importance for the characterization of structure and function of membrane proteins. In this respect, usage of the lipid bilayer nanodisc technology provides a unique potential for nuclear magnetic resonance (NMR)-based studies. This review summarizes the recent advances in this field, focusing on (i) the strengths of the system, (ii) the bottlenecks that may be faced, and (iii) promising capabilities that may be explored in future studies.

Acknowledgments

The authors acknowledge access to the Jülich-Düsseldorf Biomolecular NMR Center, support by Dr. Fabien Aussenac (Bruker Biospin) and thank the DFG for support through the Emmy Noether grants ET103/2-1 to M.E. as well as the Marie Sklodowska-Curie Grant No. 660258 to A.V. T.V. acknowledges support from the International NRW Research School iGRASPseed.

References

Ajees, A.A., Anantharamaiah, G.M., Mishra, V.K., Hussain, M.M., and Murthy, H.M. (2006). Crystal structure of human apolipoprotein A-I: insights into its protective effect against cardiovascular diseases. Proc. Natl. Acad. Sci. USA 103, 2126–2131.10.1073/pnas.0506877103Search in Google Scholar PubMed PubMed Central

Alami, M., Dalal, K., Lelj-Garolla, B., Sligar, S.G., and Duong, F. (2007). Nanodiscs unravel the interaction between the SecYEG channel and its cytosolic partner SecA. EMBO J. 26, 1995–2004.10.1038/sj.emboj.7601661Search in Google Scholar PubMed PubMed Central

Anantharamaiah, G.M., Jones, J.L., Brouillette, C.G., Schmidt, C.F., Chung, B.H., Hughes, T.A., Bhown, A.S., and Segrest, J.P. (1985). Studies of synthetic peptide analogs of the amphipathic helix. Structure of complexes with dimyristoyl phosphatidylcholine. J. Biol. Chem. 260, 10248–10255.10.1016/S0021-9258(17)39238-4Search in Google Scholar

Baas, B.J., Denisov, I.G., and Sligar, S.G. (2004). Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch. Biochem. Biophys. 430, 218–228.10.1016/j.abb.2004.07.003Search in Google Scholar PubMed

Baker, S.E., Hopkins, R.C., Blanchette, C.D., Walsworth, V.L., Sumbad, R., Fischer, N.O., Kuhn, E.A., Coleman, M., Chromy, B.A., Letant, S.E., et al. (2009). Hydrogen production by a hyperthermophilic membrane-bound hydrogenase in water-soluble nanolipoprotein particles. J. Am. Chem. Soc. 131, 7508–7509.10.1021/ja809251fSearch in Google Scholar PubMed

Banerjee, S., Huber, T., and Sakmar, T.P. (2008). Rapid incorporation of functional rhodopsin into nanoscale apolipoprotein bound bilayer (NABB) particles. J. Mol. Biol. 377, 1067–1081.10.1016/j.jmb.2008.01.066Search in Google Scholar PubMed

Bao, H., Goldschen-Ohm, M., Jeggle, P., Chanda, B., Edwardson, J.M., and Chapman, E.R. (2016). Exocytotic fusion pores are composed of both lipids and proteins. Nat. Struct. Mol. Biol. 23, 67–73.10.1038/nsmb.3141Search in Google Scholar PubMed PubMed Central

Bayburt, T.H. and Sligar, S.G. (2003). Self-assembly of single integral membrane proteins into soluble nanoscale phospholipid bilayers. Protein Sci. 12, 2476–2481.10.1110/ps.03267503Search in Google Scholar PubMed PubMed Central

Bayburt, T.H. and Sligar, S.G. (2010). Membrane protein assembly into Nanodiscs. FEBS Lett. 584, 1721–1727.10.1016/j.febslet.2009.10.024Search in Google Scholar PubMed PubMed Central

Bayburt, T.H., Carlson, J.W., and Sligar, S.G. (1998). Reconstitution and imaging of a membrane protein in a nanometer-size phospholipid bilayer. J. Struct. Biol. 123, 37–44.10.1006/jsbi.1998.4007Search in Google Scholar PubMed

Bayburt, T.H., Grinkova, Y.V., and Sligar, S.G. (2002). Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett. 2, 853–856.10.1021/nl025623kSearch in Google Scholar

Bayburt, T.H., Grinkova, Y.V., and Sligar, S.G. (2006). Assembly of single bacteriorhodopsin trimers in bilayer nanodiscs. Arch. Biochem. Biophys. 450, 215–222.10.1016/j.abb.2006.03.013Search in Google Scholar PubMed

Bayburt, T.H., Leitz, A.J., Xie, G., Oprian, D.D., and Sligar, S.G. (2007). Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J. Biol. Chem. 282, 14875–14881.10.1074/jbc.M701433200Search in Google Scholar PubMed

Bhat, S., Sorci-Thomas, M.G., Tuladhar, R., Samuel, M.P., and Thomas, M.J. (2007). Conformational adaptation of apolipoprotein A-I to discretely sized phospholipid complexes. Biochemistry 46, 7811–7821.10.1021/bi700384tSearch in Google Scholar PubMed PubMed Central

Bibow, S., Carneiro, M.G., Sabo, T.M., Schwiegk, C., Becker, S., Riek, R., and Lee, D. (2014). Measuring membrane protein bond orientations in nanodiscs via residual dipolar couplings. Protein Sci. 23, 851–856.10.1002/pro.2482Search in Google Scholar PubMed PubMed Central

Bocquet, N., Kohler, J., Hug, M.N., Kusznir, E.A., Rufer, A.C., Dawson, R.J., Hennig, M., Ruf, A., Huber, W., and Huber, S. (2015). Real-time monitoring of binding events on a thermostabilized human A2A receptor embedded in a lipid bilayer by surface plasmon resonance. Biochim. Biophys. Acta 1848, 1224–1233.10.1016/j.bbamem.2015.02.014Search in Google Scholar PubMed

Boettcher, J.M., Davis-Harrison, R.L., Clay, M.C., Nieuwkoop, A.J., Ohkubo, Y.Z., Tajkhorshid, E., Morrissey, J.H., and Rienstra, C.M. (2011). Atomic view of calcium-induced clustering of phosphatidylserine in mixed lipid bilayers. Biochemistry 50, 2264–2273.10.1021/bi1013694Search in Google Scholar PubMed PubMed Central

Boldog, T., Li, M., and Hazelbauer, G.L. (2007) Using nanodiscs to create water-soluble transmembrane chemoreceptors inserted in lipid bilayers. In: Methods Enzymol., Vol. 423, Melvin, I. Simon, Crane, Alexandrine, eds. (New York: Elsevier Inc.), pp. 317–335.10.1016/S0076-6879(07)23014-9Search in Google Scholar PubMed

Borch, J. and Hamann, T. (2009). The nanodisc: a novel tool for membrane protein studies. Biol. Chem. 390, 805–814.10.1515/BC.2009.091Search in Google Scholar PubMed

Borch, J., Torta, F., Sligar, S.G., and Roepstorff, P. (2008). Nanodiscs for immobilization of lipid bilayers and membrane receptors: kinetic analysis of cholera toxin binding to a glycolipid receptor. Anal. Chem. 80, 6245–6252.10.1021/ac8000644Search in Google Scholar PubMed

Borhani, D.W., Rogers, D.P., Engler, J.A., and Brouillette, C.G. (1997). Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation. Proc. Natl. Acad. Sci. USA 94, 12291–12296.10.1073/pnas.94.23.12291Search in Google Scholar PubMed PubMed Central

Brewer, K.D., Li, W., Horne, B.E., and Rizo, J. (2011). Reluctance to membrane binding enables accessibility of the synaptobrevin SNARE motif for SNARE complex formation. Proc. Natl. Acad. Sci. USA 108, 12723–12728.10.1073/pnas.1105128108Search in Google Scholar PubMed PubMed Central

Brouillette, C.G. and Anantharamaiah, G.M. (1995). Structural models of human apolipoprotein A-I. Biochim. Biophys. Acta 1256, 103–129.10.1016/0005-2760(95)00018-8Search in Google Scholar PubMed

Brouillette, C.G., Anantharamaiah, G.M., Engler, J.A., and Borhani, D.W. (2001). Structural models of human apolipoprotein A-I: a critical analysis and review. Biochim. Biophys. Acta 1531, 4–46.10.1016/S1388-1981(01)00081-6Search in Google Scholar

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., et al. (2008). Cell-free co-expression of functional membrane proteins and apolipoprotein, forming soluble nanolipoprotein particles. Mol. Cell. Proteomics 7, 2246–2253.10.1074/mcp.M800191-MCP200Search in Google Scholar PubMed PubMed Central

Catoire, L.J., Warnet, X.L., and Warschawski, D.E. (2014). Micelles, bicelles, amphipols, nanodiscs, liposomes, or intact cells: the hitchhiker’s guide to the study of membrane proteins by NMR. In: Membrane Proteins Production for Structural Analysis. Isabelle Mus-Veteau, ed. (New York: Springer), pp. 315–345.10.1007/978-1-4939-0662-8_12Search in Google Scholar

Chromy, B.A., Arroyo, E., Blanchette, C.D., Bench, G., Benner, H., Cappuccio, J.A., Coleman, M.A., Henderson, P.T., Hinz, A.K., Kuhn, E.A., et al. (2007). Different apolipoproteins impact nanolipoprotein particle formation. J. Am. Chem. Soc. 129, 14348–14354.10.1021/ja074753ySearch in Google Scholar PubMed

Civjan, N.R., Bayburt, T.H., Schuler, M.A., and Sligar, S.G. (2003). Direct solubilization of heterologously expressed membrane proteins by incorporation into nanoscale lipid bilayers. BioTechniques 35, 556–560, 562–563.10.2144/03353rr02Search in Google Scholar PubMed

D’Antona, A.M., Xie, G., Sligar, S.G., and Oprian, D.D. (2014). Assembly of an activated rhodopsin-transducin complex in nanoscale lipid bilayers. Biochemistry 53, 127–134.10.1021/bi4012995Search in Google Scholar PubMed PubMed Central

Dalal, K., Nguyen, N., Alami, M., Tan, J., Moraes, T.F., Lee, W.C., Maurus, R., Sligar, S.S., Brayer, G.D., and Duong, F. (2009). Structure, binding, and activity of Syd, a SecY-interacting protein. J. Biol. Chem. 284, 7897–7902.10.1074/jbc.M808305200Search in Google Scholar PubMed PubMed Central

Denisov, I.G. and Sligar, S.G. (2016). Nanodiscs for structural and functional studies of membrane proteins. Nat Struct Mol Biol 23, 481–486.10.1038/nsmb.3195Search in Google Scholar PubMed PubMed Central

Denisov, I.G., Grinkova, Y.V., Lazarides, A.A., and Sligar, S.G. (2004). Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J. Am. Chem. Soc. 126, 3477–3487.10.1021/ja0393574Search in Google Scholar PubMed

Denisov, I.G., McLean, M.A., Shaw, A.W., Grinkova, Y.V., and Sligar, S.G. (2005). Thermotropic phase transition in soluble nanoscale lipid bilayers. J. Phys. Chem. B 109, 15580–15588.10.1021/jp051385gSearch in Google Scholar PubMed PubMed Central

Ding, Y., Yao, Y., and Marassi, F.M. (2013). Membrane protein structure determination in membrana. Acc. Chem. Res. 46, 2182–2190.10.1021/ar400041aSearch in Google Scholar PubMed PubMed Central

Ding, Y., Fujimoto, L.M., Yao, Y., and Marassi, F.M. (2015a). Solid-state NMR of the Yersinia pestis outer membrane protein Ail in lipid bilayer nanodiscs sedimented by ultracentrifugation. J. Biomol. NMR 61, 275–286.10.1007/s10858-014-9893-4Search in Google Scholar PubMed PubMed Central

Ding, Y., Fujimoto, L.M., Yao, Y., Plano, G.V., and Marassi, F.M. (2015b). Influence of the lipid membrane environment on structure and activity of the outer membrane protein Ail from Yersinia pestis. Biochim. Biophys. Acta 1848, 712–720.10.1016/j.bbamem.2014.11.021Search in Google Scholar PubMed PubMed Central

Dorr, J.M., Koorengevel, M.C., Schafer, M., Prokofyev, A.V., Scheidelaar, S., van der Cruijsen, E.A., Dafforn, T.R., Baldus, M., and Killian, J.A. (2014). Detergent-free isolation, characterization, and functional reconstitution of a tetrameric K+ channel: the power of native nanodiscs. Proc. Natl. Acad. Sci. USA 111, 18607–18612.10.1073/pnas.1416205112Search in Google Scholar PubMed PubMed Central

Dorr, J.M., Scheidelaar, S., Koorengevel, M.C., Dominguez, J.J., Schafer, M., van Walree, C.A., and Killian, J.A. (2016). The styrene-maleic acid copolymer: a versatile tool in membrane research. Eur. Biophys. J. 45, 3–21.10.1007/s00249-015-1093-ySearch in Google Scholar PubMed PubMed Central

Duan, H., Civjan, N.R., Sligar, S.G., and Schuler, M.A. (2004). Co-incorporation of heterologously expressed Arabidopsis cytochrome P450 and P450 reductase into soluble nanoscale lipid bilayers. Arch. Biochem. Biophys. 424, 141–153.10.1016/j.abb.2004.02.010Search in Google Scholar PubMed

Eggensperger, S., Fisette, O., Parcej, D., Schafer, L.V., and Tampe, R. (2014). An annular lipid belt is essential for allosteric coupling and viral inhibition of the antigen translocation complex TAP (transporter associated with antigen processing). J. Biol. Chem. 289, 33098–33108.10.1074/jbc.M114.592832Search in Google Scholar PubMed PubMed Central

Etzkorn, M., Raschle, T., Hagn, F., Gelev, V., Rice, A.J., Walz, T., and Wagner, G. (2013). Cell-free expressed bacteriorhodopsin in different soluble membrane mimetics: biophysical properties and NMR accessibility. Structure 21, 394–401.10.1016/j.str.2013.01.005Search in Google Scholar PubMed PubMed Central

Fernandez, C., Hilty, C., Wider, G., Guntert, P., and Wuthrich, K. (2004). NMR structure of the integral membrane protein OmpX. J. Mol. Biol. 336, 1211–1221.10.1016/j.jmb.2003.09.014Search in Google Scholar PubMed

Fox, D.A., Larsson, P., Lo, R.H., Kroncke, B.M., Kasson, P.M., and Columbus, L. (2014). Structure of the Neisserial outer membrane protein Opa60: loop flexibility essential to receptor recognition and bacterial engulfment. J. Am. Chem. Soc. 136, 9938–9946.10.1021/ja503093ySearch in Google Scholar PubMed PubMed Central

Frauenfeld, J., Gumbart, J., Sluis, E.O., Funes, S., Gartmann, M., Beatrix, B., Mielke, T., Berninghausen, O., Becker, T., Schulten, K., et al. (2011). Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nat. Struct. Mol. Biol. 18, 614–621.10.1038/nsmb.2026Search in Google Scholar PubMed PubMed Central

Frauenfeld, J., Loving, R., Armache, J.P., Sonnen, A.F., Guettou, F., Moberg, P., Zhu, L., Jegerschold, C., Flayhan, A., Briggs, J.A., et al. (2016). A saposin-lipoprotein nanoparticle system for membrane proteins. Nat. Methods 13, 345–351.10.1038/nmeth.3801Search in Google Scholar PubMed PubMed Central

Gao, T., Petrlova, J., He, W., Huser, T., Kudlick, W., Voss, J., and Coleman, M.A. (2012). Characterization of de novo synthesized GPCRs supported in nanolipoprotein discs. PLoS One 7, e44911.10.1371/journal.pone.0044911Search in Google Scholar PubMed PubMed Central

Gao, Y., Cao, E., Julius, D., and Cheng, Y. (2016). TRPV1 structures in nanodiscs reveal mechanisms of ligand and lipid action. Nature 534, 347–351.10.1038/nature17964Search in Google Scholar PubMed PubMed Central

Gluck, J.M., Wittlich, M., Feuerstein, S., Hoffmann, S., Willbold, D., and Koenig, B.W. (2009). Integral membrane proteins in nanodiscs can be studied by solution NMR spectroscopy. J. Am. Chem. Soc. 131, 12060–12061.10.1021/ja904897pSearch in Google Scholar PubMed

Grinkova, Y.V., Denisov, I.G., and Sligar, S.G. (2010). Engineering extended membrane scaffold proteins for self-assembly of soluble nanoscale lipid bilayers. Protein Eng. Des. Sel. 23, 843–848.10.1093/protein/gzq060Search in Google Scholar PubMed PubMed Central

Guo, C., Zhang, D., and Tugarinov, V. (2008). An NMR experiment for simultaneous TROSY-based detection of amide and methyl groups in large proteins. J. Am. Chem. Soc. 130, 10872–10873.10.1021/ja8036178Search in Google Scholar PubMed

Hagn, F. and Wagner, G. (2015). Structure refinement and membrane positioning of selectively labeled OmpX in phospholipid nanodiscs. J. Biomol. NMR 61, 249–260.10.1007/s10858-014-9883-6Search in Google Scholar PubMed PubMed Central

Hagn, F., Etzkorn, M., Raschle, T., and Wagner, G. (2013). Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J. Am. Chem. Soc. 135, 1919–1925.10.1021/ja310901fSearch in Google Scholar PubMed PubMed Central

Hartley, M.D., Schneggenburger, P.E., and Imperiali, B. (2013). Lipid bilayer nanodisc platform for investigating polyprenol-dependent enzyme interactions and activities. Proc. Natl. Acad. Sci. USA 110, 20863–20870.10.1073/pnas.1320852110Search in Google Scholar PubMed PubMed Central

Hiller, S. and Wagner, G. (2012) Solution NMR spectroscopy of integral membrane proteins. In: Comprehensive Biophysics, Vol 5, Egelman, Tamm. eds. (Burlington: Elsevier Inc.), pp 120–138.10.1016/B978-0-12-374920-8.00508-7Search in Google Scholar

Imai, S., Osawa, M., Mita, K., Toyonaga, S., Machiyama, A., Ueda, T., Takeuchi, K., Oiki, S., and Shimada, I. (2012). Functional equilibrium of the KcsA structure revealed by NMR. J. Biol. Chem. 287, 39634–39641.10.1074/jbc.M112.401265Search in Google Scholar PubMed PubMed Central

Inagaki, S., Ghirlando, R., White, J.F., Gvozdenovic-Jeremic, J., Northup, J.K., and Grisshammer, R. (2012). Modulation of the interaction between neurotensin receptor NTS1 and Gq protein by lipid. J. Mol. Biol. 417, 95–111.10.1016/j.jmb.2012.01.023Search in Google Scholar PubMed PubMed Central

Inagaki, S., Ghirlando, R., and Grisshammer, R. (2013). Biophysical characterization of membrane proteins in nanodiscs. Methods 59, 287–300.10.1016/j.ymeth.2012.11.006Search in Google Scholar PubMed PubMed Central

Katayama, H., Wang, J., Tama, F., Chollet, L., Gogol, E.P., Collier, R.J., and 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, 3453–3457.10.1073/pnas.1000100107Search in Google Scholar PubMed PubMed Central

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., et al. (2008). Insertion of membrane proteins into discoidal membranes using a cell-free protein expression approach. J. Proteome Res. 7, 3535–3542.10.1021/pr800265fSearch in Google Scholar PubMed

Kawai, T., Caaveiro, J.M., Abe, R., Katagiri, T., and Tsumoto, K. (2011). Catalytic activity of MsbA reconstituted in nanodisc particles is modulated by remote interactions with the bilayer. FEBS Lett. 585, 3533–3537.10.1016/j.febslet.2011.10.015Search in Google Scholar PubMed

Kedrov, A., Sustarsic, M., de Keyzer, J., Caumanns, J.J., Wu, Z.C., and Driessen, A.J. (2013). Elucidating the native architecture of the YidC: ribosome complex. J. Mol. Biol. 425, 4112–4124.10.1016/j.jmb.2013.07.042Search in Google Scholar PubMed

Kijac, A.Z., Li, Y., Sligar, S.G., and Rienstra, C.M. (2007). Magic-angle spinning solid-state NMR spectroscopy of nanodisc-embedded human CYP3A4. Biochemistry 46, 13696–13703.10.1021/bi701411gSearch in Google Scholar PubMed PubMed Central

Kijac, A., Shih, A.Y., Nieuwkoop, A.J., Schulten, K., Sligar, S.G., and Rienstra, C.M. (2010). Lipid-protein correlations in nanoscale phospholipid bilayers determined by solid-state nuclear magnetic resonance. Biochemistry 49, 9190–9198.10.1021/bi1013722Search in Google Scholar PubMed PubMed Central

Klammt, C., Maslennikov, I., Bayrhuber, M., Eichmann, C., Vajpai, N., Chiu, E.J., Blain, K.Y., Esquivies, L., Kwon, J.H., Balana, B., et al. (2012). Facile backbone structure determination of human membrane proteins by NMR spectroscopy. Nat. Methods 9, 834–839.10.1038/nmeth.2033Search in Google Scholar PubMed PubMed Central

Knowles, T.J., Finka, R., Smith, C., Lin, Y.P., Dafforn, T., and Overduin, M. (2009). Membrane proteins solubilized intact in lipid containing nanoparticles bounded by styrene maleic acid copolymer. J. Am. Chem. Soc. 131, 7484–7485.10.1021/ja810046qSearch in Google Scholar PubMed

Kobashigawa, Y., Harada, K., Yoshida, N., Ogura, K., and Inagaki, F. (2011). Phosphoinositide-incorporated lipid-protein nanodiscs: a tool for studying protein-lipid interactions. Anal. Biochem. 410, 77–83.10.1016/j.ab.2010.11.021Search in Google Scholar PubMed

Kofuku, Y., Ueda, T., Okude, J., Shiraishi, Y., Kondo, K., Mizumura, T., Suzuki, S., and Shimada, I. (2014). Functional dynamics of deuterated β2-adrenergic receptor in lipid bilayers revealed by NMR spectroscopy. Angew. Chem. Int. Ed. 53, 13376–13379.10.1002/anie.201406603Search in Google Scholar PubMed

Kucharska, I., Edrington, T.C., Liang, B., and Tamm, L.K. (2015). Optimizing nanodiscs and bicelles for solution NMR studies of two β-barrel membrane proteins. J. Biomol. NMR 61, 261–274.10.1007/s10858-015-9905-zSearch in Google Scholar PubMed PubMed Central

Lee, T.Y., Yeh, V., Chuang, J., Chung Chan, J.C., Chu, L.K., and Yu, T.Y. (2015). Tuning the photocycle kinetics of bacteriorhodopsin in lipid nanodiscs. Biophys. J. 109, 1899–1906.10.1016/j.bpj.2015.09.012Search in Google Scholar PubMed PubMed Central

Lee, S.C., Knowles, T.J., Postis, V.L., Jamshad, M., Parslow, R.A., Lin, Y.P., Goldman, A., Sridhar, P., Overduin, M., Muench, S.P., et al. (2016). A method for detergent-free isolation of membrane proteins in their local lipid environment. Nat. Protoc. 11, 1149–1162.10.1038/nprot.2016.070Search in Google Scholar PubMed

Leitz, A., Bayburt, T., Barnakov, A., Springer, B., and Sligar, S. (2006). Functional reconstitution of β2-adrenergic receptors utilizing self-assembling Nanodisc technology. BioTechniques 40, 601–612.10.2144/000112169Search in Google Scholar PubMed

Leney, A.C., Fan, X., Kitova, E.N., and Klassen, J.S. (2014). Nanodiscs and electrospray ionization mass spectrometry: a tool for screening glycolipids against proteins. Anal. Chem. 86, 5271–5277.10.1021/ac4041179Search in Google Scholar PubMed

Li, Y., Kijac, A.Z., Sligar, S.G., and Rienstra, C.M. (2006). Structural analysis of nanoscale self-assembled discoidal lipid bilayers by solid-state NMR spectroscopy. Biophys. J. 91, 3819–3828.10.1529/biophysj.106.087072Search in Google Scholar PubMed PubMed Central

Liang, B. and Tamm, L.K. (2016). NMR as a tool to investigate the structure, dynamics and function of membrane proteins. Nat. Struct. Mol. Biol. 23, 468–474.10.1038/nsmb.3226Search in Google Scholar PubMed PubMed Central

Long, A.R., O’Brien, C.C., Malhotra, K., Schwall, C.T., Albert, A.D., Watts, A., and Alder, N.N. (2013). A detergent-free strategy for the reconstitution of active enzyme complexes from native biological membranes into nanoscale discs. BMC Biotechnol. 13, 41.10.1186/1472-6750-13-41Search in Google Scholar PubMed PubMed Central

Lyukmanova, E.N., Shenkarev, Z.O., Paramonov, A.S., Sobol, A.G., Ovchinnikova, T.V., Chupin, V.V., Kirpichnikov, M.P., Blommers, M.J., and Arseniev, A.S. (2008). Lipid-protein nanoscale bilayers: a versatile medium for NMR investigations of membrane proteins and membrane-active peptides. J. Am. Chem. Soc. 130, 2140–2141.10.1021/ja0777988Search in Google Scholar PubMed

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., et al. (2012). 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 1818, 349–358.10.1016/j.bbamem.2011.10.020Search in Google Scholar PubMed

Mazhab-Jafari, M.T., Marshall, C.B., Stathopulos, P.B., Kobashigawa, Y., Stambolic, V., Kay, L.E., Inagaki, F., and Ikura, M. (2013). Membrane-dependent modulation of the mTOR activator Rheb: NMR observations of a GTPase tethered to a lipid-bilayer nanodisc. J. Am. Chem. Soc. 135, 3367–3370.10.1021/ja312508wSearch in Google Scholar PubMed

Mazhab-Jafari, M.T., Marshall, C.B., Smith, M.J., Gasmi-Seabrook, G.M., Stathopulos, P.B., Inagaki, F., Kay, L.E., Neel, B.G., and Ikura, M. (2015). Oncogenic and RASopathy-associated K-RAS mutations relieve membrane-dependent occlusion of the effector-binding site. Proc. Natl. Acad. Sci. USA 112, 6625–6630.10.1073/pnas.1419895112Search in Google Scholar PubMed PubMed Central

Mi, L.Z., Grey, M.J., Nishida, N., Walz, T., Lu, C., and Springer, T.A. (2008). Functional and structural stability of the epidermal growth factor receptor in detergent micelles and phospholipid nanodiscs. Biochemistry 47, 10314–10323.10.1021/bi801006sSearch in Google Scholar PubMed PubMed Central

Mineev, K.S., Goncharuk, S.A., Kuzmichev, P.K., Vilar, M., and Arseniev, A.S. (2015). NMR dynamics of transmembrane and intracellular domains of p75NTR in lipid-protein nanodiscs. Biophys. J. 109, 772–782.10.1016/j.bpj.2015.07.009Search in Google Scholar PubMed PubMed Central

Mitra, N., Liu, Y., Liu, J., Serebryany, E., Mooney, V., DeVree, B.T., Sunahara, R.K., Yan, E.C. (2013). Calcium-dependent ligand binding and G-protein signaling of family B GPCR parathyroid hormone 1 receptor purified in nanodiscs. ACS Chem. Biol. 8, 617–625.10.1021/cb300466nSearch in Google Scholar PubMed PubMed Central

Morgado, L., Zeth, K., Burmann, B.M., Maier, T., and Hiller, S. (2015). Characterization of the insertase BamA in three different membrane mimetics by solution NMR spectroscopy. J. Biomol. NMR 61, 333–345.10.1007/s10858-015-9906-ySearch in Google Scholar PubMed

Mors, K., Roos, C., Scholz, F., Wachtveitl, J., Dotsch, V., Bernhard, F., and Glaubitz, C. (2013). Modified lipid and protein dynamics in nanodiscs. Biochim. Biophys. Acta 1828, 1222–1229.10.1016/j.bbamem.2012.12.011Search in Google Scholar PubMed

Nasvik Ojemyr, L., von Ballmoos, C., Gennis, R.B., Sligar, S.G., and Brzezinski, P. (2012). Reconstitution of respiratory oxidases in membrane nanodiscs for investigation of proton-coupled electron transfer. FEBS Lett. 586, 640–645.10.1016/j.febslet.2011.12.023Search in Google Scholar PubMed PubMed Central

Ni, D., Wang, Y., Yang, X., Zhou, H., Hou, X., Cao, B., Lu, Z., Zhao, X., Yang, K., and Huang, Y. (2014). Structural and functional analysis of the β-barrel domain of BamA from Escherichia coli. FASEB J. 28, 2677–2685.10.1096/fj.13-248450Search in Google Scholar PubMed

Okude, J., Ueda, T., Kofuku, Y., Sato, M., Nobuyama, N., Kondo, K., Shiraishi, Y., Mizumura, T., Onishi, K., Natsume, M., et al. (2015). Identification of a conformational equilibrium that determines the efficacy and functional selectivity of the μ-opioid receptor. Angew. Chem. Int. Ed. 54, 15771–15776.10.1002/anie.201508794Search in Google Scholar PubMed PubMed Central

Opella, S.J. (2013). Structure determination of membrane proteins by nuclear magnetic resonance spectroscopy. Annu. Rev. Anal. Chem. 6, 305–328.10.1146/annurev-anchem-062012-092631Search in Google Scholar PubMed PubMed Central

Orwick, M.C., Judge, P.J., Procek, J., Lindholm, L., Graziadei, A., Engel, A., Grobner, G., and Watts, A. (2012). Detergent-free formation and physicochemical characterization of nanosized lipid-polymer complexes: Lipodisq. Angew. Chem. Int. Ed. 51, 4653–4657.10.1002/anie.201201355Search in Google Scholar PubMed

Orwick-Rydmark, M., Lovett, J.E., Graziadei, A., Lindholm, L., Hicks, M.R., and Watts, A. (2012). Detergent-free incorporation of a seven-transmembrane receptor protein into nanosized bilayer Lipodisq particles for functional and biophysical studies. Nano Lett. 12, 4687–4692.10.1021/nl3020395Search in Google Scholar PubMed

Park, S.H., Berkamp, S., Cook, G.A., Chan, M.K., Viadiu, H., and Opella, S.J. (2011). Nanodiscs versus macrodiscs for NMR of membrane proteins. Biochemistry 50, 8983–8985.10.1021/bi201289cSearch in Google Scholar PubMed PubMed Central

Phillips, J.C., Wriggers, W., Li, Z., Jonas, A., and Schulten, K. (1997). Predicting the structure of apolipoprotein A-I in reconstituted high-density lipoprotein disks. Biophys. J. 73, 2337–2346.10.1016/S0006-3495(97)78264-XSearch in Google Scholar PubMed PubMed Central

Popot, J.L. (2010). Amphipols, nanodiscs, and fluorinated surfactants: three nonconventional approaches to studying membrane proteins in aqueous solutions. Annu. Rev. Biochem. 79, 737–775.10.1146/annurev.biochem.052208.114057Search in Google Scholar PubMed

Postis, V., Rawson, S., Mitchell, J.K., Lee, S.C., Parslow, R.A., Dafforn, T.R., Baldwin, S.A., and Muench, S.P. (2015). The use of SMALPs as a novel membrane protein scaffold for structure study by negative stain electron microscopy. Biochim Biophys Acta 1848, 496–501.10.1016/j.bbamem.2014.10.018Search in Google Scholar PubMed PubMed Central

Proverbio, D., Roos, C., Beyermann, M., Orban, E., Dotsch, V., and Bernhard, F. (2013). Functional properties of cell-free expressed human endothelin A and endothelin B receptors in artificial membrane environments. Biochim. Biophys. Acta 1828, 2182–2192.10.1016/j.bbamem.2013.05.031Search in Google Scholar PubMed

Puthenveetil, R. and Vinogradova, O. (2013). Optimization of the design and preparation of nanoscale phospholipid bilayers for its application to solution NMR. Proteins: Struct. Funct. Bioinf. 81, 1222–1231.10.1002/prot.24271Search in Google Scholar PubMed PubMed Central

Rajesh, S., Knowles, T., and Overduin, M. (2011). Production of membrane proteins without cells or detergents. Nat. Biotechnol. 28, 250–254.10.1016/j.nbt.2010.07.011Search in Google Scholar PubMed

Raschle, T., Hiller, S., Yu, T.Y., Rice, A.J., Walz, T., and Wagner, G. (2009). Structural and functional characterization of the integral membrane protein VDAC-1 in lipid bilayer nanodiscs. J. Am. Chem. Soc. 131, 17777–17779.10.1021/ja907918rSearch in Google Scholar PubMed PubMed Central

Raschle, T., Hiller, S., Etzkorn, M., and Wagner, G. (2010). Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Curr. Opin. Struct. Biol. 20, 471–479.10.1016/j.sbi.2010.05.006Search in Google Scholar PubMed PubMed Central

Raschle, T., Lin, C., Jungmann, R., Shih, W.M., and Wagner, G. (2015). Controlled Co-reconstitution of multiple membrane proteins in lipid bilayer nanodiscs using DNA as a scaffold. ACS Chem. Biol. 10, 2448–2454.10.1021/acschembio.5b00627Search in Google Scholar PubMed PubMed Central

Reichart, T.M., Baksh, M.M., Rhee, J.K., Fiedler, J.D., Sligar, S.G., Finn, M.G., Zwick, M.B., and Dawson, P.E. (2016). Trimerization of the HIV transmembrane domain in lipid bilayers modulates broadly neutralizing antibody binding. Angew. Chem. Int. Ed. 55, 2688–2692.10.1002/anie.201508421Search in Google Scholar PubMed PubMed Central

Ritchie, T.K., Grinkova, Y.V., Bayburt, T.H., Denisov, I.G., Zolnerciks, J.K., Atkins, W.M., and Sligar, S.G. (2009) Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. In: Methods Enzymol., Vol. 464, Nejat. eds. (New York: Elsevier Inc.), pp. 211–231.10.1016/S0076-6879(09)64011-8Search in Google Scholar PubMed PubMed Central

Roos, C., Zocher, M., Muller, D., Munch, D., Schneider, T., Sahl, H.G., Scholz, F., Wachtveitl, J., Ma, Y., Proverbio, D., et al. (2012). Characterization of co-translationally formed nanodisc complexes with small multidrug transporters, proteorhodopsin and with the E. coli MraY translocase. Biochim. Biophys. Acta 1818, 3098–3106.10.1016/j.bbamem.2012.08.007Search in Google Scholar PubMed

Roos, C., Kai, L., Proverbio, D., Ghoshdastider, U., Filipek, S., Dotsch, V., and Bernhard, F. (2013). Co-translational association of cell-free expressed membrane proteins with supplied lipid bilayers. Mol. Membr. Biol. 30, 75–89.10.3109/09687688.2012.693212Search in Google Scholar PubMed

Roy, J., Pondenis, H., Fan, T.M., and Das, A. (2015). Direct capture of functional proteins from mammalian plasma membranes into nanodiscs. Biochemistry 54, 6299–6302.10.1021/acs.biochem.5b00954Search in Google Scholar PubMed

Rues, R.-B., Dötsch, V., and Bernhard, F. (2016). Co-translational formation and pharmacological characterization of beta1-adrenergic receptor/nanodisc complexes with different lipid environments. Biochim. Biophys. Acta 1858, 1306–1316.10.1016/j.bbamem.2016.02.031Search in Google Scholar PubMed

Salzmann, M., Pervushin, K., Wider, G., Senn, H., and Wuthrich, K. (1998). TROSY in triple-resonance experiments: new perspectives for sequential NMR assignment of large proteins. Proc. Natl. Acad. Sci. USA 95, 13585–13590.10.1073/pnas.95.23.13585Search in Google Scholar PubMed PubMed Central

Schuler, M.A., Denisov, I.G., and Sligar, S.G. (2013) Nanodiscs as a new tool to examine lipid-protein interactions. In: Lipid-Protein Interactions, Vol. 974, Kleinschmidt. eds. (New York: Springer), pp. 415–433.10.1007/978-1-62703-275-9_18Search in Google Scholar PubMed PubMed Central

Schwarz, D., Junge, F., Durst, F., Frolich, N., Schneider, B., Reckel, S., Sobhanifar, S., Dotsch, V., and Bernhard, F. (2007). Preparative scale expression of membrane proteins in Escherichia coli-based continuous exchange cell-free systems. Nat. Protoc. 2, 2945–2957.10.1038/nprot.2007.426Search in Google Scholar PubMed

Segrest, J.P. (1977). Amphipathic helixes and plasma lipoproteins: thermodynamic and geometric considerations. Chem. Phys. Lipids 18, 7–22.10.1016/0009-3084(77)90023-8Search in Google Scholar PubMed

Segrest, J.P., Jones, M.K., Klon, A.E., Sheldahl, C.J., Hellinger, M., De Loof, H., and Harvey, S.C. (1999). A detailed molecular belt model for apolipoprotein A-I in discoidal high density lipoprotein. J. Biol. Chem. 274, 31755–31758.10.1074/jbc.274.45.31755Search in Google Scholar PubMed

Shaw, A.W., McLean, M.A., and Sligar, S.G. (2004). Phospholipid phase transitions in homogeneous nanometer scale bilayer discs. FEBS Lett. 556, 260–264.10.1016/S0014-5793(03)01400-5Search in Google Scholar

Shaw, A.W., Pureza, V.S., Sligar, S.G., and Morrissey, J.H. (2007). The local phospholipid environment modulates the activation of blood clotting. J. Biol. Chem. 282, 6556–6563.10.1074/jbc.M607973200Search in Google Scholar PubMed

Shenkarev, Z.O., Lyukmanova, E.N., Solozhenkin, O.I., Gagnidze, I.E., Nekrasova, O.V., Chupin, V.V., Tagaev, A.A., Yakimenko, Z.A., Ovchinnikova, T.V., Kirpichnikov, M.P., et al. (2009). Lipid-protein nanodiscs: possible application in high-resolution NMR investigations of membrane proteins and membrane-active peptides. Biochemistry (Moscow) 74, 756–765.10.1134/S0006297909070086Search in Google Scholar PubMed

Shenkarev, Z.O., Lyukmanova, E.N., Paramonov, A.S., Shingarova, L.N., Chupin, V.V., Kirpichnikov, M.P., Blommers, M.J., and Arseniev, A.S. (2010a). Lipid-protein nanodiscs as reference medium in detergent screening for high-resolution NMR studies of integral membrane proteins. J. Am. Chem. Soc. 132, 5628–5629.10.1021/ja9097498Search in Google Scholar PubMed

Shenkarev, Z.O., Paramonov, A.S., Lyukmanova, E.N., Shingarova, L.N., Yakimov, S.A., Dubinnyi, M.A., Chupin, V.V., Kirpichnikov, M.P., Blommers, M.J., and Arseniev, A.S. (2010b). NMR structural and dynamical investigation of the isolated voltage-sensing domain of the potassium channel KvAP: implications for voltage gating. J. Am. Chem. Soc. 132, 5630–5637.10.1021/ja909752rSearch in Google Scholar PubMed

Shenkarev, Z.O., Lyukmanova, E.N., Paramonov, A.S., Panteleev, P.V., Balandin, S.V., Shulepko, M.A., Mineev, K.S., Ovchinnikova, T.V., Kirpichnikov, M.P., and Arseniev, A.S. (2014). Lipid-protein nanodiscs offer new perspectives for structural and functional studies of water-soluble membrane-active peptides. Acta Naturae 6, 84–94.10.32607/20758251-2014-6-2-84-94Search in Google Scholar

Shi, L., Shen, Q.T., Kiel, A., Wang, J., Wang, H.W., Melia, T.J., Rothman, J.E., and Pincet, F. (2012). SNARE proteins: one to fuse and three to keep the nascent fusion pore open. Science 335, 1355–1359.10.1126/science.1214984Search in Google Scholar PubMed PubMed Central

Shi, L., Howan, K., Shen, Q.T., Wang, Y.J., Rothman, J.E., and Pincet, F. (2013). Preparation and characterization of SNARE-containing nanodiscs and direct study of cargo release through fusion pores. Nat. Protoc. 8, 935–948.10.1038/nprot.2013.048Search in Google Scholar PubMed

Shih, A.Y., Denisov, I.G., Phillips, J.C., Sligar, S.G., and Schulten, K. (2005). Molecular dynamics simulations of discoidal bilayers assembled from truncated human lipoproteins. Biophys. J. 88, 548–556.10.1529/biophysj.104.046896Search in Google Scholar PubMed PubMed Central

Shih, A.Y., Arkhipov, A., Freddolino, P.L., Sligar, S.G., and Schulten, K. (2007a). Assembly of lipids and proteins into lipoprotein particles. J. Phys. Chem. B 111, 11095–11104.10.1021/jp072320bSearch in Google Scholar PubMed

Shih, A.Y., Freddolino, P.L., Arkhipov, A., and Schulten, K. (2007b). Assembly of lipoprotein particles revealed by coarse-grained molecular dynamics simulations. J. Struct. Biol. 157, 579–592.10.1016/j.jsb.2006.08.006Search in Google Scholar PubMed

Shih, A.Y., Sligar, S.G., and Schulten, K. (2009). Maturation of high-density lipoproteins. J. R. Soc. Interface 6, 863–871.10.1098/rsif.2009.0173Search in Google Scholar PubMed PubMed Central

Skar-Gislinge, N., Simonsen, J.B., Mortensen, K., Feidenhans’l R., Sligar, S.G., Lindberg Moller, B., Bjornholm, T., and Arleth, L. (2010). Elliptical structure of phospholipid bilayer nanodiscs encapsulated by scaffold proteins: casting the roles of the lipids and the protein. J. Am. Chem. Soc. 132, 13713–13722.10.1021/ja1030613Search in Google Scholar PubMed PubMed Central

Susac, L., Horst, R., and Wuthrich, K. (2014). Solution-NMR characterization of outer-membrane protein A from E. coli in lipid bilayer nanodiscs and detergent micelles. ChemBioChem 15, 995–1000.10.1002/cbic.201300729Search in Google Scholar PubMed PubMed Central

Thomas, M.J., Bhat, S., and Sorci-Thomas, M.G. (2008). Three-dimensional models of HDL apoA-I: implications for its assembly and function. J. Lipid Res. 49, 1875–1883.10.1194/jlr.R800010-JLR200Search in Google Scholar PubMed PubMed Central

Tsukamoto, H., Sinha, A., DeWitt, M., and Farrens, D.L. (2010). Monomeric rhodopsin is the minimal functional unit required for arrestin binding. J. Mol. Biol. 399, 501–511.10.1016/j.jmb.2010.04.029Search in Google Scholar PubMed PubMed Central

Tzitzilonis, C., Eichmann, C., Maslennikov, I., Choe, S., and Riek, R. (2013). Detergent/nanodisc screening for high-resolution NMR studies of an integral membrane protein containing a cytoplasmic domain. PLoS One 8, e54378.10.1371/journal.pone.0054378Search in Google Scholar PubMed PubMed Central

Viegas, A., Viennet, T., Yu, T.Y., Schumann, F., Bermel, W., Wagner, G., and Etzkorn, M. (2016). UTOPIA NMR: activating unexploited magnetization using interleaved low-gamma detection. J. Biomol. NMR 64, 9–15.10.1007/s10858-015-0008-7Search in Google Scholar PubMed PubMed Central

Vilar, M., Charalampopoulos, I., Kenchappa, R.S., Simi, A., Karaca, E., Reversi, A., Choi, S., Bothwell, M., Mingarro, I., Friedman, W.J., Schiavo, G., Bastiaens, P.I., Verveer, P.J., Carter, B.D., and Ibanez, C.F. (2009). Activation of the p75 neurotrophin receptor through conformational rearrangement of disulphide-linked receptor dimers. Neuron 62, 72–83.10.1016/j.neuron.2009.02.020Search in Google Scholar PubMed PubMed Central

Vogt, J. and Schulz, G.E. (1999). The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence. Structure 7, 1301–1309.10.1016/S0969-2126(00)80063-5Search in Google Scholar PubMed

Wan, C., Wu, B., Song, Z., Zhang, J., Chu, H., Wang, A., Liu, Q., Shi, Y., Li, G., and Wang, J. (2015). Insights into the molecular recognition of the granuphilin C2A domain with PI(4, 5)P2. Chem. Phys. Lipids 186, 61–67.10.1016/j.chemphyslip.2015.01.003Search in Google Scholar PubMed

Wang, X., Mu, Z., Li, Y., Bi, Y., and Wang, Y. (2015). Smaller Nanodiscs are Suitable for Studying Protein Lipid Interactions by Solution NMR. Protein, J. 34, 205–211.10.1007/s10930-015-9613-2Search in Google Scholar PubMed

Whorton, M.R., Bokoch, M.P., Rasmussen, S.G., Huang, B., Zare, R.N., Kobilka, B., and Sunahara, R.K. (2007). A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc. Natl. Acad. Sci. USA 104, 7682–7687.10.1073/pnas.0611448104Search in Google Scholar PubMed PubMed Central

Wu, Z., Wagner, M.A., Zheng, L., Parks, J.S., Shy, J.M., 3rd, Smith, J.D., Gogonea, V., and Hazen, S.L. (2007). The refined structure of nascent HDL reveals a key functional domain for particle maturation and dysfunction. Nat. Struct. Mol. Biol. 14, 861–868.10.1038/nsmb1284Search in Google Scholar PubMed

Wu, Z., Gogonea, V., Lee, X., Wagner, M.A., Li, X.M., Huang, Y., Undurti, A., May, R.P., Haertlein, M., Moulin, M., Gutsche, I., Zaccai, G., Didonato, J.A., and Hazen, S.L. (2009). Double superhelix model of high density lipoprotein. J. Biol. Chem. 284, 36605–36619.10.1074/jbc.M109.039537Search in Google Scholar PubMed PubMed Central

Yang, J.P., Cirico, T., Katzen, F., Peterson, T.C., and Kudlicki, W. (2011). Cell-free synthesis of a functional G protein-coupled receptor complexed with nanometer scale bilayer discs. BMC Biotechnol. 11, 57.10.1186/1472-6750-11-57Search in Google Scholar PubMed PubMed Central

Yao, Y., Fujimoto, L.M., Hirshman, N., Bobkov, A.A., Antignani, A., Youle, R.J., and Marassi, F.M. (2015). Conformation of BCL-XL upon membrane integration. J. Mol. Biol. 427, 2262–2270.10.1016/j.jmb.2015.02.019Search in Google Scholar PubMed PubMed Central

Yao, Y., Nisan, D., Fujimoto, L.M., Antignani, A., Barnes, A., Tjandra, N., Youle, R.J., and Marassi, F.M. (2016). Characterization of the membrane-inserted C-terminus of cytoprotective BCL-XL. Protein Expr. Purif. 122, 56–63.10.1016/j.pep.2016.02.010Search in Google Scholar PubMed PubMed Central

Yokogawa, M., Kobashigawa, Y., Yoshida, N., Ogura, K., Harada, K., and Inagaki, F. (2012). NMR analyses of the interaction between the FYVE domain of early endosome antigen 1 (EEA1) and phosphoinositide embedded in a lipid bilayer. J. Biol. Chem. 287, 34936–34945.10.1074/jbc.M112.398255Search in Google Scholar PubMed PubMed Central

Yoshiura, C., Kofuku, Y., Ueda, T., Mase, Y., Yokogawa, M., Osawa, M., Terashima, Y., Matsushima, K., and Shimada, I. (2010). NMR analyses of the interaction between CCR5 and its ligand using functional reconstitution of CCR5 in lipid bilayers. J. Am. Chem. Soc. 132, 6768–6777.10.1021/ja100830fSearch in Google Scholar PubMed

Yu, T.Y., Raschle, T., Hiller, S., and Wagner, G. (2012). Solution NMR spectroscopic characterization of human VDAC-2 in detergent micelles and lipid bilayer nanodiscs. Biochim. Biophys. Acta 1818, 1562–1569.10.1016/j.bbamem.2011.11.012Search in Google Scholar PubMed PubMed Central

Zhang, Z., Dai, C., Bai, J., Xu, G., Liu, M., and Li, C. (2014). Ca2+ modulating α-synuclein membrane transient interactions revealed by solution NMR spectroscopy. Biochim. Biophys. Acta 1838, 853–858.10.1016/j.bbamem.2013.11.016Search in Google Scholar PubMed

Zhang, M., Huang, R., Ackermann, R., Im, S.C., Waskell, L., Schwendeman, A., and Ramamoorthy, A. (2016). Reconstitution of the Cytb5 -CytP450 complex in nanodiscs for structural studies using NMR spectroscopy. Angew. Chem. Int. Ed. 55, 4497–4499.10.1002/anie.201600073Search in Google Scholar PubMed

Received: 2016-6-6
Accepted: 2016-7-19
Published Online: 2016-7-23
Published in Print: 2016-12-1

©2016 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 25.4.2024 from https://www.degruyter.com/document/doi/10.1515/hsz-2016-0224/html
Scroll to top button