Diab, C., Winnik, F.M., Tribet, C. (2007b) Enthalpy of interaction and binding isotherms of non-ionic surfactants onto
micellar amphiphilic polymers (amphipols). Langmuir 23:3025–3035.
Dupont, M., Dé, E., Chollet, R., Chevalier, J., Pagès, J.-M. (2004) Enterobacter aerogenes OmpX, a cation-selective
channel mar- and osmo-regulated. FEBS Lett. 569:27–30.
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.
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.
Etzkorn, M., Zoonens, M., Catoire, L.J., Popot, J.-L., Hiller, S. (2014) How amphipols embed membrane proteins:
Global solvent accessibility and interaction with a flexible protein terminus. J. Membr. Biol. 247:965–970.
Feinstein, H.E., Tifrea, D., Sun, G., Popot, J.-L., de la Maza, L.M., Cocco, M.J. (2014) Long-term stability of a vaccine
formulated with the amphipol-trapped major outer membrane protein from Chlamydia trachomatis. J. Membr. Biol.
247:1053–1065.
Fernández, C., Adeishvili, K., Wüthrich, K. (2001a) Transverse relaxation-optimized NMR spectroscopy with the outer
membrane protein OmpX in dihexanoyl phosphatidylcholine micelles. Proc. Natl. Acad. Sci. USA 98:2358–2363.
Fernández, C., Hilty, C., Bonjour, S., Adeishvili, K., Pervushin, K., Wüthrich, K. (2001b) Solution NMR studies of the
integral membrane proteins OmpX and OmpA from Escherichia coli. FEBS Lett. 504:173–178.
Fernández, C., Hilty, C., Wider, G., Guntert, P., Wüthrich, K. (2004) NMR structure of the integral membrane protein
OmpX. J. Mol. Biol. 336:1211–1221.
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.
Gardner, K.H., Kay, L.E. (1998) The use of
2
H,
13
C,
15
N multidimensional NMR to study the structure and dynamics of
proteins. Annu. Rev. Biophys. Biomol. Struct. 27:357–406.
Gautier, A., Mott, H.R., Bostock, M.J., Kirkpatrick, J.P., Nietlispach, D. (2010) Structure determination of the sevenhelix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat. Struct. Mol. Biol.
17:768–774.
Giusti, F., Kessler, P., Westh Hansen, R., Della Pia, E.A., Le Bon, C., Mourier, G., Popot, J.-L., Martinez, K.L., Zoonens,
M. (2015) Synthesis of a polyhistidine-bearing amphipol and its use for immobilizing membrane proteins. Biomacromolecules 16:3751–3761.
Giusti, F., Rieger, J., Catoire, L., Qian, S., Calabrese, A.N., Watkinson, T.G., Casiraghi, M., Radford, S.E., Ashcroft, A.
E., Popot, J.-L. (2014) Synthesis, characterization and applications of a perdeuterated amphipol. J. Membr. Biol.
247:909–924.
Glück, J.M., Wittlich, M., Feuerstein, S., Hoffmann, S., Willbold, D., Koenig, B.W. (2009) Integral membrane proteins
in nanodiscs can be studied by solution NMR spectroscopy. J. Am. Chem. Soc. 131:12060–12061.
Gohon, Y., Dahmane, T., Ruigrok, R., Schuck, P., Charvolin, D., Rappaport, F., Timmins, P., Engelman, D.M., Tribet,
C., Popot, J.-L., Ebel, C. (2008) Bacteriorhodopsin/amphipol complexes: structural and functional properties.
Biophys. J. 94:3523–3537.
Gohon, Y., Giusti, F., Prata, C., Charvolin, D., Timmins, P., Ebel, C., Tribet, C., Popot, J.-L. (2006) Well-defined
nanoparticles formed by hydrophobic assembly of a short and polydisperse random terpolymer, amphipol A8-35.
Langmuir 22:1281–1290.
Gohon, Y., Pavlov, G., Timmins, P., Tribet, C., Popot, J.-L., Ebel, C. (2004) Partial specific volume and solvent
interactions of amphipol A8-35. Anal. Biochem. 334:318–334.
Griesinger, C., Bennati, M., Vieth, H.M., Luchinat, C., Parigi, G., Höfer, P., Engelke, F., Glaser, S.J., Denysenkov, V.,
Prisner, T.F. (2012) Dynamic nuclear polarization at high magnetic fields in liquids. Prog. Nucl. Magn. Reson.
Spectrosc. 64:4–28.
Hagn, F., Etzkorn, M., Raschle, T., Wagner, G. (2013) Optimized phospholipid bilayer nanodiscs facilitate highresolution structure determination of membrane proteins. J. Am. Chem. Soc. 135:1919–1925.
Hiller, S., Garces, R.G., Malia, T.J., Orekhov, V.Y., Colombini, M., Wagner, G. (2008) Solution structure of the integral
human membrane protein VDAC-1 in detergent micelles. Science 321:1206–1210.
Hilty, C., Wider, G., Fernández, C., Wüthrich, K. (2004) Membrane protein-lipid interactions in mixed micelles studied
by NMR spectroscopy with the use of paramagnetic reagents. ChemBioChem 5:467–473.
Hiruma-Shimizu, K., Shimizu, H., Thompson, G.S., Kalverda, A.P., Patching, S.G. (2015) Deuterated detergents for
structural and functional studies of membrane proteins: Properties, chemical synthesis and applications. Mol. Membr.
Biol. 32:139–155.
Hong, H., Szabo, G., Tamm, L.K. (2006) Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for
pore opening. Nat. Chem. Biol. 2:627–635.
492
10 Nuclear Magnetic Resonance Studies of Amphipol-Trapped Membrane Proteins
micellar amphiphilic polymers (amphipols). Langmuir 23:3025–3035.
Dupont, M., Dé, E., Chollet, R., Chevalier, J., Pagès, J.-M. (2004) Enterobacter aerogenes OmpX, a cation-selective
channel mar- and osmo-regulated. FEBS Lett. 569:27–30.
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.
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.
Etzkorn, M., Zoonens, M., Catoire, L.J., Popot, J.-L., Hiller, S. (2014) How amphipols embed membrane proteins:
Global solvent accessibility and interaction with a flexible protein terminus. J. Membr. Biol. 247:965–970.
Feinstein, H.E., Tifrea, D., Sun, G., Popot, J.-L., de la Maza, L.M., Cocco, M.J. (2014) Long-term stability of a vaccine
formulated with the amphipol-trapped major outer membrane protein from Chlamydia trachomatis. J. Membr. Biol.
247:1053–1065.
Fernández, C., Adeishvili, K., Wüthrich, K. (2001a) Transverse relaxation-optimized NMR spectroscopy with the outer
membrane protein OmpX in dihexanoyl phosphatidylcholine micelles. Proc. Natl. Acad. Sci. USA 98:2358–2363.
Fernández, C., Hilty, C., Bonjour, S., Adeishvili, K., Pervushin, K., Wüthrich, K. (2001b) Solution NMR studies of the
integral membrane proteins OmpX and OmpA from Escherichia coli. FEBS Lett. 504:173–178.
Fernández, C., Hilty, C., Wider, G., Guntert, P., Wüthrich, K. (2004) NMR structure of the integral membrane protein
OmpX. J. Mol. Biol. 336:1211–1221.
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.
Gardner, K.H., Kay, L.E. (1998) The use of
2
H,
13
C,
15
N multidimensional NMR to study the structure and dynamics of
proteins. Annu. Rev. Biophys. Biomol. Struct. 27:357–406.
Gautier, A., Mott, H.R., Bostock, M.J., Kirkpatrick, J.P., Nietlispach, D. (2010) Structure determination of the sevenhelix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat. Struct. Mol. Biol.
17:768–774.
Giusti, F., Kessler, P., Westh Hansen, R., Della Pia, E.A., Le Bon, C., Mourier, G., Popot, J.-L., Martinez, K.L., Zoonens,
M. (2015) Synthesis of a polyhistidine-bearing amphipol and its use for immobilizing membrane proteins. Biomacromolecules 16:3751–3761.
Giusti, F., Rieger, J., Catoire, L., Qian, S., Calabrese, A.N., Watkinson, T.G., Casiraghi, M., Radford, S.E., Ashcroft, A.
E., Popot, J.-L. (2014) Synthesis, characterization and applications of a perdeuterated amphipol. J. Membr. Biol.
247:909–924.
Glück, J.M., Wittlich, M., Feuerstein, S., Hoffmann, S., Willbold, D., Koenig, B.W. (2009) Integral membrane proteins
in nanodiscs can be studied by solution NMR spectroscopy. J. Am. Chem. Soc. 131:12060–12061.
Gohon, Y., Dahmane, T., Ruigrok, R., Schuck, P., Charvolin, D., Rappaport, F., Timmins, P., Engelman, D.M., Tribet,
C., Popot, J.-L., Ebel, C. (2008) Bacteriorhodopsin/amphipol complexes: structural and functional properties.
Biophys. J. 94:3523–3537.
Gohon, Y., Giusti, F., Prata, C., Charvolin, D., Timmins, P., Ebel, C., Tribet, C., Popot, J.-L. (2006) Well-defined
nanoparticles formed by hydrophobic assembly of a short and polydisperse random terpolymer, amphipol A8-35.
Langmuir 22:1281–1290.
Gohon, Y., Pavlov, G., Timmins, P., Tribet, C., Popot, J.-L., Ebel, C. (2004) Partial specific volume and solvent
interactions of amphipol A8-35. Anal. Biochem. 334:318–334.
Griesinger, C., Bennati, M., Vieth, H.M., Luchinat, C., Parigi, G., Höfer, P., Engelke, F., Glaser, S.J., Denysenkov, V.,
Prisner, T.F. (2012) Dynamic nuclear polarization at high magnetic fields in liquids. Prog. Nucl. Magn. Reson.
Spectrosc. 64:4–28.
Hagn, F., Etzkorn, M., Raschle, T., Wagner, G. (2013) Optimized phospholipid bilayer nanodiscs facilitate highresolution structure determination of membrane proteins. J. Am. Chem. Soc. 135:1919–1925.
Hiller, S., Garces, R.G., Malia, T.J., Orekhov, V.Y., Colombini, M., Wagner, G. (2008) Solution structure of the integral
human membrane protein VDAC-1 in detergent micelles. Science 321:1206–1210.
Hilty, C., Wider, G., Fernández, C., Wüthrich, K. (2004) Membrane protein-lipid interactions in mixed micelles studied
by NMR spectroscopy with the use of paramagnetic reagents. ChemBioChem 5:467–473.
Hiruma-Shimizu, K., Shimizu, H., Thompson, G.S., Kalverda, A.P., Patching, S.G. (2015) Deuterated detergents for
structural and functional studies of membrane proteins: Properties, chemical synthesis and applications. Mol. Membr.
Biol. 32:139–155.
Hong, H., Szabo, G., Tamm, L.K. (2006) Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for
pore opening. Nat. Chem. Biol. 2:627–635.
492
10 Nuclear Magnetic Resonance Studies of Amphipol-Trapped Membrane Proteins