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.
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.
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.
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.
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: Physicalchemical and biochemical characterization. Langmuir 22:8881–8890.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Liebau, J., Ye, W., Mäler, L. (2016) Characterization of fast-tumbling isotropic bicelles by PFG diffusion NMR. Magn.
Reson. Chem. 55:395–404.
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.
Loll, P.J. (2014) Membrane proteins, detergents and crystals: what is the state of the art? Acta Crystallogr. F
70:1576–1583.
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.
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.
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.
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.
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.
Mäler, L., Gräslund, A. (2009) Artificial membrane models for the study of macromolecular delivery. Meth. Mol. Biol.
480:129–139.
142
3 Alternatives to Detergents for Handling Membrane Proteins in Aqueous Solutions
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.
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.
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.
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.
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: Physicalchemical and biochemical characterization. Langmuir 22:8881–8890.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Liebau, J., Ye, W., Mäler, L. (2016) Characterization of fast-tumbling isotropic bicelles by PFG diffusion NMR. Magn.
Reson. Chem. 55:395–404.
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.
Loll, P.J. (2014) Membrane proteins, detergents and crystals: what is the state of the art? Acta Crystallogr. F
70:1576–1583.
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.
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.
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.
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.
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.
Mäler, L., Gräslund, A. (2009) Artificial membrane models for the study of macromolecular delivery. Meth. Mol. Biol.
480:129–139.
142
3 Alternatives to Detergents for Handling Membrane Proteins in Aqueous Solutions