Orlova, E.V., Saibil, H.R. (2011) Structural analysis of macromolecular assemblies by electron microscopy. Chem. Rev.
111:7710–7748.
Paulsen, C.E., Armache, J.-P., Gao, Y., Cheng, Y., Julius, D. (2015) Structure of the TRPA1 ion channel suggests
regulatory mechanisms. Nature 520:511–517.
Perlmutter, J.D., Popot, J.-L., Sachs, J.N. (2014) Molecular dynamics simulations of a membrane protein/amphipol
complex. J. Membr. Biol. 247:883–895.
Perry, T., Souabni, H., Rapisarda, C., Fronzes, R., Giusti, F., Popot, J.-L., Zoonens, M., Gubellini, F. (2018) Visualizing
transmembrane regions of protein complexes by electron microscopy using biotinylated amphipols, submitted for
publication.
Picard, M., Dahmane, T., Garrigos, M., Gauron, C., Giusti, F., le Maire, M., Popot, J.-L., Champeil, P. (2006) Protective
and inhibitory effects of various types of amphipols on the Ca
2+ -ATPase from sarcoplasmic reticulum: a comparative
study. Biochemistry 45:1861–1869.
Popot, J.-L., Berry, E.A., Charvolin, D., Creuzenet, C., Ebel, C., Engelman, D.M., Flötenmeyer, M., Giusti, F., Gohon,
Y., Hervé, P., Hong, Q., Lakey, J.H., Leonard, K., Shuman, H.A., Timmins, P., Warschawski, D.E., Zito, F.,
Zoonens, M., Pucci, B., Tribet, C. (2003) Amphipols: polymeric surfactants for membrane biology research. Cell.
Mol. Life Sci. 60:1559–1574.
Postis, V., Rawson, S., Mitchell, J.K., Lee, S.C., Parslowc, R.A., Dafforn, T.R., Baldwin, S.A., 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.
Punjani, A., Rubinstein, J.L., Fleet, D.J., Brubaker, M.A. (2017) cryoSPARC: algorithms for rapid unsupervised cryoEM structure determination. Nat. Meth. 14:290–296.
Radermacher, M., Wagenknecht, T., Verschoor, A., Frank, J. (1987) Three-dimensional reconstruction from a singleexposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli. J. Microsc.
146:113–136.
Rahmeh, R., Damian, M., Cottet, M., Orcel, H., Mendre, C., Durroux, T., Sharma, K.S., Durand, G., Pucci, B., Trinquet,
E., Zwier, J.M., Deupi, X., Bron, P., J.-L B, Mouillac, B., Granier, S. (2012) Structural insights into biased G proteincoupled receptor signaling revealed by fluorescence spectroscopy. Proc. Natl. Acad. Sci. USA 109:6733–6738.
Raunser, S., Walz, T. (2009) Electron crystallography as a technique to study the structure on membrane proteins in a
lipidic environment. Annu. Rev. Biophys. 38:89–105.
Rosenthal, P.B., Henderson, R. (2003) Optimal determination of particle orientation, absolute hand, and contrast loss in
single-particle electron cryomicroscopy. J. Mol. Biol. 333:721–745.
Rubinstein, J.L. (2007) Structural analysis of membrane protein complexes by single-particle electron microscopy.
Methods 41:409–416.
Saxton, W.O., Baumeister, W. (1982) The correlation averaging of a regularly arranged bacterial cell envelope protein.
J. Microsc. 127:127–138.
Schabert, F.A., Engel, A. (1994) Reproducible acquisition of Escherichia coli porin surface topographs by atomic-force
microscopy. Biophys. J. 67:2394–2403.
Schäfer, E., Seelert, H., Reifschneider, N.H., Krause, F., Dencher, N.A., Vonck, J. (2006) Architecture of active
mammalian respiratory chain supercomplexes. J. Biol. Chem. 281:15370–15375.
Scheres, S.H.W., Chen, S. (2012) Prevention of overfitting in cryo-EM structure determination. Nat. Meth. 9:853–854.
Schneck, E., Schubert, T., Konovalov, O.V., Quinn, B.E., Gutsmann, T., Brandenburg, K., Oliveira, R.G., Pink, D.A.,
Tanaka, M. (2010) Quantitative determination of ion distributions in bacterial lipopolysaccharide membranes by
grazing-incidence X-ray fluorescence. Proc. Natl. Acad. Sci. USA 107:9147–9151.
Schoebel, S., Mi, W., Stein, A., Ovchinnikov, S., Pavlovicz, R., DiMaio, F., Baker, D., Chambers, M.G., Su, H., Li, D.,
Rapoport, T.A., Liao, M. (2017) Cryo-EM structure of the protein-conducting ERAD channel Hrd1 in complex with
Hrd3. Nature 548:352–355.
Schröder, R.S. (2015) Advances in electron microscopy: A qualitative view of instrumentation development for
macromolecular imaging and tomography. Arch. Biochem. Biophys. 581:25–38.
Schulz, S., Wilkes, M., Mills, D.J., Kühlbrandt, W., Meier, T. (2017) Molecular architecture of the N-type ATPase rotor
ring from Burkholderia pseudomallei. EMBO Rep. 18:526–535.
Selmi, D.N., Adamson, R.J., Attrill, H., Goddard, A.D., Gilbert, R.J.C., Watts, A., Turberfield, A.J. (2011)
DNA-templated protein arrays for single-molecule imaging. Nano Lett. 11:657–660.
Serysheva, I.I., Orlova, E.V., Chiu, W., Sherman, M.B., Hamilton, S.L., van Heel, M. (1995) Electron cryomicroscopy
and angular reconstitution used to visualize the skeletal muscle calcium release channel. Nat. Struct. Biol. 2:18–24.
Shao, J., Fu, Z., Ji, Y., Guan, X., Guo, S., Ding, Z., Yang, X., Cong, Y., Shen, Y. (2016) Leucine zipper-EF-hand
containing transmembrane protein 1 (LETM1) forms a Ca
2+ /H
+ antiporter. Sci. Rep. 6:34174.
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.e711.
588
12 The Use of Amphipols for Electron Microscopy
111:7710–7748.
Paulsen, C.E., Armache, J.-P., Gao, Y., Cheng, Y., Julius, D. (2015) Structure of the TRPA1 ion channel suggests
regulatory mechanisms. Nature 520:511–517.
Perlmutter, J.D., Popot, J.-L., Sachs, J.N. (2014) Molecular dynamics simulations of a membrane protein/amphipol
complex. J. Membr. Biol. 247:883–895.
Perry, T., Souabni, H., Rapisarda, C., Fronzes, R., Giusti, F., Popot, J.-L., Zoonens, M., Gubellini, F. (2018) Visualizing
transmembrane regions of protein complexes by electron microscopy using biotinylated amphipols, submitted for
publication.
Picard, M., Dahmane, T., Garrigos, M., Gauron, C., Giusti, F., le Maire, M., Popot, J.-L., Champeil, P. (2006) Protective
and inhibitory effects of various types of amphipols on the Ca
2+ -ATPase from sarcoplasmic reticulum: a comparative
study. Biochemistry 45:1861–1869.
Popot, J.-L., Berry, E.A., Charvolin, D., Creuzenet, C., Ebel, C., Engelman, D.M., Flötenmeyer, M., Giusti, F., Gohon,
Y., Hervé, P., Hong, Q., Lakey, J.H., Leonard, K., Shuman, H.A., Timmins, P., Warschawski, D.E., Zito, F.,
Zoonens, M., Pucci, B., Tribet, C. (2003) Amphipols: polymeric surfactants for membrane biology research. Cell.
Mol. Life Sci. 60:1559–1574.
Postis, V., Rawson, S., Mitchell, J.K., Lee, S.C., Parslowc, R.A., Dafforn, T.R., Baldwin, S.A., 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.
Punjani, A., Rubinstein, J.L., Fleet, D.J., Brubaker, M.A. (2017) cryoSPARC: algorithms for rapid unsupervised cryoEM structure determination. Nat. Meth. 14:290–296.
Radermacher, M., Wagenknecht, T., Verschoor, A., Frank, J. (1987) Three-dimensional reconstruction from a singleexposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli. J. Microsc.
146:113–136.
Rahmeh, R., Damian, M., Cottet, M., Orcel, H., Mendre, C., Durroux, T., Sharma, K.S., Durand, G., Pucci, B., Trinquet,
E., Zwier, J.M., Deupi, X., Bron, P., J.-L B, Mouillac, B., Granier, S. (2012) Structural insights into biased G proteincoupled receptor signaling revealed by fluorescence spectroscopy. Proc. Natl. Acad. Sci. USA 109:6733–6738.
Raunser, S., Walz, T. (2009) Electron crystallography as a technique to study the structure on membrane proteins in a
lipidic environment. Annu. Rev. Biophys. 38:89–105.
Rosenthal, P.B., Henderson, R. (2003) Optimal determination of particle orientation, absolute hand, and contrast loss in
single-particle electron cryomicroscopy. J. Mol. Biol. 333:721–745.
Rubinstein, J.L. (2007) Structural analysis of membrane protein complexes by single-particle electron microscopy.
Methods 41:409–416.
Saxton, W.O., Baumeister, W. (1982) The correlation averaging of a regularly arranged bacterial cell envelope protein.
J. Microsc. 127:127–138.
Schabert, F.A., Engel, A. (1994) Reproducible acquisition of Escherichia coli porin surface topographs by atomic-force
microscopy. Biophys. J. 67:2394–2403.
Schäfer, E., Seelert, H., Reifschneider, N.H., Krause, F., Dencher, N.A., Vonck, J. (2006) Architecture of active
mammalian respiratory chain supercomplexes. J. Biol. Chem. 281:15370–15375.
Scheres, S.H.W., Chen, S. (2012) Prevention of overfitting in cryo-EM structure determination. Nat. Meth. 9:853–854.
Schneck, E., Schubert, T., Konovalov, O.V., Quinn, B.E., Gutsmann, T., Brandenburg, K., Oliveira, R.G., Pink, D.A.,
Tanaka, M. (2010) Quantitative determination of ion distributions in bacterial lipopolysaccharide membranes by
grazing-incidence X-ray fluorescence. Proc. Natl. Acad. Sci. USA 107:9147–9151.
Schoebel, S., Mi, W., Stein, A., Ovchinnikov, S., Pavlovicz, R., DiMaio, F., Baker, D., Chambers, M.G., Su, H., Li, D.,
Rapoport, T.A., Liao, M. (2017) Cryo-EM structure of the protein-conducting ERAD channel Hrd1 in complex with
Hrd3. Nature 548:352–355.
Schröder, R.S. (2015) Advances in electron microscopy: A qualitative view of instrumentation development for
macromolecular imaging and tomography. Arch. Biochem. Biophys. 581:25–38.
Schulz, S., Wilkes, M., Mills, D.J., Kühlbrandt, W., Meier, T. (2017) Molecular architecture of the N-type ATPase rotor
ring from Burkholderia pseudomallei. EMBO Rep. 18:526–535.
Selmi, D.N., Adamson, R.J., Attrill, H., Goddard, A.D., Gilbert, R.J.C., Watts, A., Turberfield, A.J. (2011)
DNA-templated protein arrays for single-molecule imaging. Nano Lett. 11:657–660.
Serysheva, I.I., Orlova, E.V., Chiu, W., Sherman, M.B., Hamilton, S.L., van Heel, M. (1995) Electron cryomicroscopy
and angular reconstitution used to visualize the skeletal muscle calcium release channel. Nat. Struct. Biol. 2:18–24.
Shao, J., Fu, Z., Ji, Y., Guan, X., Guo, S., Ding, Z., Yang, X., Cong, Y., Shen, Y. (2016) Leucine zipper-EF-hand
containing transmembrane protein 1 (LETM1) forms a Ca
2+ /H
+ antiporter. Sci. Rep. 6:34174.
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.e711.
588
12 The Use of Amphipols for Electron Microscopy