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.
Grisshammer, R., Tate, C.G. (1995) Overexpression of integral membrane proteins for structural studies. Quart. Rev.
Biophys. 28:315–422.
Harris, N.J., Booth, P.J. (2012) Folding and stability of membrane transport proteins in vitro. Biochim. Biophys. Acta
1818:1055–1066.
Huang, K.-S., Bayley, H., Liao, M.-J., London, E., Khorana, H.G. (1981) Refolding of an integral membrane protein.
Denaturation, renaturation, and reconstitution of intact bacteriorhodopsin and two proteolytic fragments. J. Biol.
Chem. 256:3802–3809.
Ishchenko, A., Abola, E., Cherezov, V. (2014) Lipidic cubic phase technologies for structural studies of membrane
proteins, in: Mus-Veteau, I. (Ed.), Membrane Proteins Production for Structural Analysis. Springer, New York,
pp. 289–314.
Kahn, T.W., Sturtevant, J.M., Engelman, D.M. (1992) Thermodynamic measurements of the contributions of helixconnecting loops and of retinal to the stability of bacteriorhodopsin. Biochemistry 31:8829–8839.
Kiefer, H. (2003) In vitro folding of α-helical membrane proteins. Biochim. Biophys. Acta 1610:57–62.
Kleinschmidt, J.H. (2015) Folding of β-barrel membrane proteins in lipid bilayers – Unassisted and assisted folding and
insertion. Biochim. Biophys. Acta 1848:1927–1943.
Kleinschmidt, J.H., Popot, J.-L. (2014) Folding and stability of integral membrane proteins in amphipols. Arch. Biochem.
Biophys. 564:327–343.
Kleinschmidt, J.H., Tamm, L.K. (1996) Folding intermediates of a β-barrel membrane protein. Kinetic evidence for a
multi-step membrane insertion mechanism. Biochemistry 35:12993–13000.
Kraft, T.E., Hresko, R.C., Hruz, P.W. (2015) Expression, purification, and functional characterization of the insulinresponsive facilitative glucose transporter GLUT4. Protein Sci. 24:2008–2019.
Le Bon, C., Marconnet, A., Masscheleyn, S., Popot, J.-L., Zoonens, M. (2018) Folding and stabilizing membrane
proteins in amphipol A8-35. Methods, in the press.
Lee, A.G. (2003) Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta
1612:1–40.
Lee, A.G. (2011) How to understand lipid-protein interactions in biological membranes, in: Yeagle, P. (Ed.), Structure of
Biological Membranes. 3rd edition, Taylor and Francis, Boca Raton, Florida, USA, pp. 273–313.
Leney, A.C., McMorran, L.M., Radford, S.E., Ashcroft, A.E. (2012) Amphipathic polymers enable the study of
functional membrane proteins in the gas phase. Anal. Chem. 84:9841–9847.
Leyris, J.-P., Roux, T., Trinquet, E., Verdié, P., Fehrentz, J.A., Oueslati, N., Douzon, S., Bourrier, E., Lamarque, L.,
Gagne, D., Galleyrand, J.-C., M’kadmi, C., Martinez, J., Mary, S., Banères, J.-L., Marie, J. (2011) Homogeneous
time-resolved fluorescence-based assay to screen for ligands targeting the growth hormone secretagogue receptor
type 1a. Anal. Biochem. 408:253–262.
Ma, D., Martin, N., Herbet, A., Boquet, D., Tribet, C., Winnik, F.M. (2012) The thermally induced aggregation of
immunoglobulin G in solution is prevented by amphipols. Chem. Lett. 41:1380–1382.
Maeda, S., Schertler, G.F.X. (2013) Production of GPCR and GPCR complexes for structure determination. Curr. Opin.
Struct. Biol. 23:381–392.
Marie, E., Sagan, S., Cribier, S., Tribet, C. (2014) Amphiphilic macromolecules on cell membranes: from protective
layers to controlled permeabilization. J. Membr. Biol. 247:861–881.
Martin, N., Ma, D., Herbet, A., Boquet, D., Winnik, F.M., Tribet, C. (2014) Prevention of thermally induced aggregation
of IgG antibodies by noncovalent interaction with poly(acrylate) derivatives. Biomacromolecules 15:2952–2962.
Martin, N., Ruchmann, J., Tribet, C. (2015) Prevention of aggregation during refolding of carbonic anhydrase via
Coulomb and hydrophobic complexation with octadecyl-modified or azobenzene-modified poly(acrylate)
derivatives. Langmuir 31:338–349.
Mesnier, D., Banères, J.-L. (2004) Cooperative conformational changes in a G-protein coupled receptor dimer, the
leukotriene B 4 receptor BLT1. J. Biol. Chem. 279:49664–49670.
Michalke, K., Huyghe, C., Lichière, J., Gravière, M.E., Siponen, M., Sciara, G., Lepaul, I., Wagner, R., Magg, C.,
Rudolph, R., Cambillau, C., Desmyter, A. (2010) Mammalian G protein-coupled receptor expression in Escherichia
coli: II. Refolding and biophysical characterization of mouse cannabinoid receptor 1 and human parathyroid hormone
receptor 1. Anal. Biochem. 401:74–80.
Michaux, C., Pomroy, N.C., Privé, G.G. (2008) Refolding SDS-denatured proteins by the addition of amphipathic
cosolvents. J. Mol. Biol. 375:1477–1488.
Milić, D., Veprintsev, D.B. (2015) Large-scale production and protein engineering of G protein-coupled receptors for
structural studies. Frontiers Pharmacol. 6: article 66.
Moosavi-Movahedi, A.A., Chamanil, J., Goto, Y., Hakimelahi, G.H. (2003) Formation of the molten globule-like state of
cytochrome c induced by n-alkyl sulfates at low concentrations. J. Biochem. 133:93–102.
358
6 Amphipol-Assisted Folding of Membrane Proteins
C., Popot, J.-L., Ebel, C. (2008) Bacteriorhodopsin/amphipol complexes: structural and functional properties.
Biophys. J. 94:3523–3537.
Grisshammer, R., Tate, C.G. (1995) Overexpression of integral membrane proteins for structural studies. Quart. Rev.
Biophys. 28:315–422.
Harris, N.J., Booth, P.J. (2012) Folding and stability of membrane transport proteins in vitro. Biochim. Biophys. Acta
1818:1055–1066.
Huang, K.-S., Bayley, H., Liao, M.-J., London, E., Khorana, H.G. (1981) Refolding of an integral membrane protein.
Denaturation, renaturation, and reconstitution of intact bacteriorhodopsin and two proteolytic fragments. J. Biol.
Chem. 256:3802–3809.
Ishchenko, A., Abola, E., Cherezov, V. (2014) Lipidic cubic phase technologies for structural studies of membrane
proteins, in: Mus-Veteau, I. (Ed.), Membrane Proteins Production for Structural Analysis. Springer, New York,
pp. 289–314.
Kahn, T.W., Sturtevant, J.M., Engelman, D.M. (1992) Thermodynamic measurements of the contributions of helixconnecting loops and of retinal to the stability of bacteriorhodopsin. Biochemistry 31:8829–8839.
Kiefer, H. (2003) In vitro folding of α-helical membrane proteins. Biochim. Biophys. Acta 1610:57–62.
Kleinschmidt, J.H. (2015) Folding of β-barrel membrane proteins in lipid bilayers – Unassisted and assisted folding and
insertion. Biochim. Biophys. Acta 1848:1927–1943.
Kleinschmidt, J.H., Popot, J.-L. (2014) Folding and stability of integral membrane proteins in amphipols. Arch. Biochem.
Biophys. 564:327–343.
Kleinschmidt, J.H., Tamm, L.K. (1996) Folding intermediates of a β-barrel membrane protein. Kinetic evidence for a
multi-step membrane insertion mechanism. Biochemistry 35:12993–13000.
Kraft, T.E., Hresko, R.C., Hruz, P.W. (2015) Expression, purification, and functional characterization of the insulinresponsive facilitative glucose transporter GLUT4. Protein Sci. 24:2008–2019.
Le Bon, C., Marconnet, A., Masscheleyn, S., Popot, J.-L., Zoonens, M. (2018) Folding and stabilizing membrane
proteins in amphipol A8-35. Methods, in the press.
Lee, A.G. (2003) Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta
1612:1–40.
Lee, A.G. (2011) How to understand lipid-protein interactions in biological membranes, in: Yeagle, P. (Ed.), Structure of
Biological Membranes. 3rd edition, Taylor and Francis, Boca Raton, Florida, USA, pp. 273–313.
Leney, A.C., McMorran, L.M., Radford, S.E., Ashcroft, A.E. (2012) Amphipathic polymers enable the study of
functional membrane proteins in the gas phase. Anal. Chem. 84:9841–9847.
Leyris, J.-P., Roux, T., Trinquet, E., Verdié, P., Fehrentz, J.A., Oueslati, N., Douzon, S., Bourrier, E., Lamarque, L.,
Gagne, D., Galleyrand, J.-C., M’kadmi, C., Martinez, J., Mary, S., Banères, J.-L., Marie, J. (2011) Homogeneous
time-resolved fluorescence-based assay to screen for ligands targeting the growth hormone secretagogue receptor
type 1a. Anal. Biochem. 408:253–262.
Ma, D., Martin, N., Herbet, A., Boquet, D., Tribet, C., Winnik, F.M. (2012) The thermally induced aggregation of
immunoglobulin G in solution is prevented by amphipols. Chem. Lett. 41:1380–1382.
Maeda, S., Schertler, G.F.X. (2013) Production of GPCR and GPCR complexes for structure determination. Curr. Opin.
Struct. Biol. 23:381–392.
Marie, E., Sagan, S., Cribier, S., Tribet, C. (2014) Amphiphilic macromolecules on cell membranes: from protective
layers to controlled permeabilization. J. Membr. Biol. 247:861–881.
Martin, N., Ma, D., Herbet, A., Boquet, D., Winnik, F.M., Tribet, C. (2014) Prevention of thermally induced aggregation
of IgG antibodies by noncovalent interaction with poly(acrylate) derivatives. Biomacromolecules 15:2952–2962.
Martin, N., Ruchmann, J., Tribet, C. (2015) Prevention of aggregation during refolding of carbonic anhydrase via
Coulomb and hydrophobic complexation with octadecyl-modified or azobenzene-modified poly(acrylate)
derivatives. Langmuir 31:338–349.
Mesnier, D., Banères, J.-L. (2004) Cooperative conformational changes in a G-protein coupled receptor dimer, the
leukotriene B 4 receptor BLT1. J. Biol. Chem. 279:49664–49670.
Michalke, K., Huyghe, C., Lichière, J., Gravière, M.E., Siponen, M., Sciara, G., Lepaul, I., Wagner, R., Magg, C.,
Rudolph, R., Cambillau, C., Desmyter, A. (2010) Mammalian G protein-coupled receptor expression in Escherichia
coli: II. Refolding and biophysical characterization of mouse cannabinoid receptor 1 and human parathyroid hormone
receptor 1. Anal. Biochem. 401:74–80.
Michaux, C., Pomroy, N.C., Privé, G.G. (2008) Refolding SDS-denatured proteins by the addition of amphipathic
cosolvents. J. Mol. Biol. 375:1477–1488.
Milić, D., Veprintsev, D.B. (2015) Large-scale production and protein engineering of G protein-coupled receptors for
structural studies. Frontiers Pharmacol. 6: article 66.
Moosavi-Movahedi, A.A., Chamanil, J., Goto, Y., Hakimelahi, G.H. (2003) Formation of the molten globule-like state of
cytochrome c induced by n-alkyl sulfates at low concentrations. J. Biochem. 133:93–102.
358
6 Amphipol-Assisted Folding of Membrane Proteins