Hostname: page-component-7c8c6479df-24hb2 Total loading time: 0 Render date: 2024-03-28T02:32:13.329Z Has data issue: false hasContentIssue false

Amphipathic environments for determining the structure of membrane proteins by single-particle electron cryo-microscopy

Published online by Cambridge University Press:  31 March 2021

Christel Le Bon
Affiliation:
Laboratoire de Biologie Physico-Chimique des Protéines Membranaires, Université de Paris, CNRS, UMR 7099, F-75005, Paris, France Institut de Biologie Physico-Chimique, Fondation Edmond de Rothschild pour le développement de la recherche Scientifique, F-75005, Paris, France
Baptiste Michon
Affiliation:
Laboratoire de Biologie Physico-Chimique des Protéines Membranaires, Université de Paris, CNRS, UMR 7099, F-75005, Paris, France Institut de Biologie Physico-Chimique, Fondation Edmond de Rothschild pour le développement de la recherche Scientifique, F-75005, Paris, France
Jean-Luc Popot
Affiliation:
Laboratoire de Biologie Physico-Chimique des Protéines Membranaires, Université de Paris, CNRS, UMR 7099, F-75005, Paris, France Institut de Biologie Physico-Chimique, Fondation Edmond de Rothschild pour le développement de la recherche Scientifique, F-75005, Paris, France
Manuela Zoonens*
Affiliation:
Laboratoire de Biologie Physico-Chimique des Protéines Membranaires, Université de Paris, CNRS, UMR 7099, F-75005, Paris, France Institut de Biologie Physico-Chimique, Fondation Edmond de Rothschild pour le développement de la recherche Scientifique, F-75005, Paris, France
*
Author for correspondence: Manuela Zoonens, E-mail: manuela.zoonens@ibpc.fr

Abstract

Over the past decade, the structural biology of membrane proteins (MPs) has taken a new turn thanks to epoch-making technical progress in single-particle electron cryo-microscopy (cryo-EM) as well as to improvements in sample preparation. The present analysis provides an overview of the extent and modes of usage of the various types of surfactants for cryo-EM studies. Digitonin, dodecylmaltoside, protein-based nanodiscs, lauryl maltoside-neopentyl glycol, glyco-diosgenin, and amphipols (APols) are the most popular surfactants at the vitrification step. Surfactant exchange is frequently used between MP purification and grid preparation, requiring extensive optimization each time the study of a new MP is undertaken. The variety of both the surfactants and experimental approaches used over the past few years bears witness to the need to continue developing innovative surfactants and optimizing conditions for sample preparation. The possibilities offered by novel APols for EM applications are discussed.

Type
Review
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abeyrathne, PD, Arheit, M, Kebbel, F, Castano-Diez, D, Goldie, KN, Chami, M, Stahlberg, H, Renault, L and Kühlbrandt, W (2012) Analysis of 2-D crystals of membrane proteins by electron microscopy. Comprehensive Biophysics 1, 277310.CrossRefGoogle Scholar
Alam, A, Küng, R, Kowal, J, McLeod, RA, Tremp, N, Broude, EV, Roninson, IB, Stahlberg, H and Locher, KP (2018) Structure of a zosuquidar and UIC2-bound human-mouse chimeric ABCB1. Proceedings of the National Academy of Sciences 115, e1973e1982.CrossRefGoogle ScholarPubMed
Alnabati, E and Kihara, D (2019) Advances in structure modeling methods for cryo-electron microscopy maps. Molecules 25, 82.CrossRefGoogle ScholarPubMed
Althoff, T, Mills, DJ, Popot, J-L and Kühlbrandt, W (2011) Arrangement of electron transport chain components in bovine mitochondrial supercomplex I1III2IV1. The EMBO journal 30, 46524664.CrossRefGoogle ScholarPubMed
Alvadia, C, Lim, NK, Clerico Mosina, V, Oostergetel, GT, Dutzler, R and Paulino, C (2019) Cryo-EM structures and functional characterization of the murine lipid scramblase TMEM16F. eLife 8, e44365.CrossRefGoogle ScholarPubMed
Andréll, J and Tate, CG (2013) Overexpression of membrane proteins in mammalian cells for structural studies. Molecular Membrane Biology 30, 5263.CrossRefGoogle ScholarPubMed
Arkhipova, V, Guskov, A and Slotboom, DJ (2020) Structural ensemble of a glutamate transporter homologue in lipid nanodisc environment. Nature Communications 11, 19.CrossRefGoogle ScholarPubMed
Armstrong, M, Han, B-G, Gomez, S, Turner, J, Fletcher, DA and Glaeser, RM (2020) Microscale fluid behavior during cryo-EM sample blotting. Biophysical Journal 118, 708719.CrossRefGoogle ScholarPubMed
Arnold, SA, Albiez, S, Bieri, A, Syntychaki, A, Adaixo, R, McLeod, RA, Goldie, KN, Stahlberg, H and Braun, T (2017) Blotting-free and lossless cryo-electron microscopy grid preparation from nanoliter-sized protein samples and single-cell extracts. Journal of Structural Biology 197, 220226.CrossRefGoogle ScholarPubMed
Ashtiani, D, Venugopal, H, Belousoff, M, Spicer, B, Mak, J, Neild, A and de Marco, A (2018) Delivery of femtolitre droplets using surface acoustic wave based atomisation for cryo-EM grid preparation. Journal of Structural Biology 203, 94101.CrossRefGoogle ScholarPubMed
Autzen, HE, Julius, D and Cheng, Y (2019) Membrane mimetic systems in CryoEM: keeping membrane proteins in their native environment. Current Opinion in Structural Biology 58, 259268.CrossRefGoogle ScholarPubMed
Baker, MR, Fan, G and Serysheva, II (2015) Single-particle cryo-EM of the ryanodine receptor channel in an aqueous environment. European Journal of Translational Myology 25, 4803.CrossRefGoogle Scholar
Basak, S, Gicheru, Y, Kapoor, A, Mayer, ML, Filizola, M and Chakrapani, S (2019) Molecular mechanism of setron-mediated inhibition of full-length 5-HT3A receptor. Nature Communications 10, 3225.CrossRefGoogle ScholarPubMed
Bausewein, T, Mills, DJ, Langer, JD, Nitschke, B, Nussberger, S and Kühlbrandt, W (2017) Cryo-EM structure of the TOM core complex from Neurospora crassa. Cell 170, 693700.e7.CrossRefGoogle ScholarPubMed
Bazzacco, P, Billon-Denis, E, Sharma, KS, Catoire, LJ, Mary, S, Le Bon, C, Point, E, Banères, J-L, Durand, G, Zito, F, Pucci, B and Popot, J-L (2012) Nonionic homopolymeric amphipols: application to membrane protein folding, cell-free synthesis, and solution nuclear magnetic resonance. Biochemistry 51, 14161430.CrossRefGoogle ScholarPubMed
Benton, DJ, Nans, A, Calder, LJ, Turner, J, Neu, U, Lin, YP, Ketelaars, E, Kallewaard, NL, Corti, D, Lanzavecchia, A, Gamblin, SJ, Rosenthal, PB and Skehel, JJ (2018) Influenza hemagglutinin membrane anchor. Proceedings of the National Academy of Sciences of the USA 115, 1011210117.CrossRefGoogle ScholarPubMed
Benton, DJ, Gamblin, SJ, Rosenthal, PB and Skehel, JJ (2020) Structural transitions in influenza haemagglutinin at membrane fusion pH. Nature 583, 150153.CrossRefGoogle ScholarPubMed
Bhairi, SM and Mohan, C (2007) Detergents. A guide to the properties and uses of detergents in biology and biochemistry (Calbiochem booklet), Darmstadt: EMD Biosciences, an affiliate of Merck KGaA.Google Scholar
Bill, RM, Henderson, PJF, Iwata, S, Kunji, ERS, Michel, H, Neutze, R, Newstead, S, Poolman, B, Tate, CG and Vogel, H (2011) Overcoming barriers to membrane protein structure determination. Nature Biotechnology 29, 335340.CrossRefGoogle ScholarPubMed
Blaza, JN, Vinothkumar, KR and Hirst, J (2018) Structure of the deactive state of mammalian respiratory complex I. Structure 26, 312319.e3.CrossRefGoogle ScholarPubMed
Bloch, JS, Pesciullesi, G, Boilevin, J, Nosol, K, Irobalieva, RN, Darbre, T, Aebi, M, Kossiakoff, AA, Reymond, J-L and Locher, KP (2020) Structure and mechanism of the ER-based glucosyltransferase ALG6. Nature 579, 443447.CrossRefGoogle ScholarPubMed
Brilot, AF, Chen, JZ, Cheng, A, Pan, J, Harrison, SC, Potter, CS, Carragher, B, Henderson, R and Grigorieff, N (2012) Beam-induced motion of vitrified specimen on holey carbon film. Journal of Structural Biology 177, 630637.CrossRefGoogle ScholarPubMed
Burendei, B, Shinozaki, R, Watanabe, M, Terada, T, Tani, K, Fujiyoshi, Y and Oshima, A (2020) Cryo-EM structures of undocked innexin-6 hemichannels in phospholipids. Science Advances 6, eaax3157.CrossRefGoogle ScholarPubMed
Cao, E, Liao, M, Cheng, Y and Julius, D (2013) TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504, 113118.CrossRefGoogle ScholarPubMed
Carlson, ML, Young, JW, Zhao, Z, Fabre, L, Jun, D, Li, J, Li, J, Dhupar, HS, Wason, I, Mills, AT, Beatty, JT, Klassen, JS, Rouiller, I and Duong, F (2018) The Peptidisc, a simple method for stabilizing membrane proteins in detergent-free solution V. Dötsch & R. Aldrich, eds. eLife 7, e34085.CrossRefGoogle Scholar
Chae, PS, Rasmussen, SGF, Rana, RR, Gotfryd, K, Chandra, R, Goren, MA, Kruse, AC, Nurva, S, Loland, CJ, Pierre, Y, Drew, D, Popot, J-L, Picot, D, Fox, BG, Guan, L, Gether, U, Byrne, B, Kobilka, B and Gellman, SH (2010) Maltose-neopentyl glycol (MNG) amphiphiles for solubilization, stabilization and crystallization of membrane proteins. Nature Methods 7, 10031008.CrossRefGoogle ScholarPubMed
Chae, PS, Rasmussen, SGF, Rana, RR, Gotfryd, K, Kruse, AC, Manglik, A, Cho, KH, Nurva, S, Gether, U, Guan, L, Loland, CJ, Byrne, B, Kobilka, BK and Gellman, SH (2012) A new class of amphiphiles bearing rigid hydrophobic groups for solubilization and stabilization of membrane proteins. Chemistry (Weinheim an Der Bergstrasse, Germany) 18, 94859490.Google ScholarPubMed
Charvolin, D, Perez, J-B, Rouvière, F, Giusti, F, Bazzacco, P, Abdine, A, Rappaport, F, Martinez, KL and Popot, J-L (2009) The use of amphipols as universal molecular adapters to immobilize membrane proteins onto solid supports. Proceedings of the National Academy of Sciences of the USA 106, 405410.CrossRefGoogle ScholarPubMed
Charvolin, D, Picard, M, Huang, L-S, Berry, EA and Popot, J-L (2014) Solution behavior and crystallization of cytochrome bc₁ in the presence of amphipols. The Journal of Membrane Biology 247, 981996.CrossRefGoogle ScholarPubMed
Chen, J, Noble, AJ, Kang, JY and Darst, SA (2019) Eliminating effects of particle adsorption to the air/water interface in single-particle cryo-electron microscopy: bacterial RNA polymerase and CHAPSO. Journal of Structural Biology X 1, 100005.CrossRefGoogle ScholarPubMed
Cheng, Y (2015) Single-particle cryo-EM at crystallographic resolution. Cell 161, 450457.CrossRefGoogle ScholarPubMed
Cheng, Y (2018) Single-particle cryo-EM – How did it get here and where will it go. Science 361, 876880.CrossRefGoogle Scholar
Chipot, C, Dehez, F, Schnell, JR, Zitzmann, N, Pebay-Peyroula, E, Catoire, LJ, Miroux, B, Kunji, ERS, Veglia, G, Cross, TA and Schanda, P (2018) Perturbations of native membrane protein structure in alkyl phosphocholine detergents: a critical assessment of NMR and biophysical studies. Chemical Reviews 118, 35593607.CrossRefGoogle ScholarPubMed
Chowdhury, S, Ketcham, SA, Schroer, TA and Lander, GC (2015) Structural organization of the dynein-dynactin complex bound to microtubules. Nature Structural & Molecular Biology 22, 345347.CrossRefGoogle ScholarPubMed
Choy, BC, Cater, RJ, Mancia, F and Pryor, EE (2021) A 10-year meta-analysis of membrane protein structural biology: detergents, membrane mimetics, and structure determination techniques. Biochimica et Biophysica Acta (BBA) – Biomembranes 1863, 183533.CrossRefGoogle ScholarPubMed
Coleman, JA, Navratna, V, Antermite, D, Yang, D, Bull, JA and Gouaux, E (2020) Chemical and structural investigation of the paroxetine-human serotonin transporter complex. eLife 9, e56427.CrossRefGoogle ScholarPubMed
Contreras-Gómez, A, Sánchez-Mirón, A, García-Camacho, F, Molina-Grima, E and Chisti, Y (2014) Protein production using the baculovirus-insect cell expression system. Biotechnology Progress 30, 118.CrossRefGoogle ScholarPubMed
Cooper, RS and Heldwein, EE (2020) Expression, purification, and crystallization of full-length HSV-1 gB for structure determination. Methods in Molecular Biology (Clifton, N.J.) 2060, 395407.CrossRefGoogle ScholarPubMed
Cooper, RS, Georgieva, ER, Borbat, PP, Freed, JH and Heldwein, EE (2018) Structural basis for membrane anchoring and fusion regulation of the herpes simplex virus fusogen gB. Nature Structural & Molecular Biology 25, 416424.CrossRefGoogle ScholarPubMed
Cross, TA, Sharma, M, Yi, M and Zhou, H-X (2011) Influence of solubilizing environments on membrane protein structures. Trends in Biochemical Sciences 36, 117125.CrossRefGoogle ScholarPubMed
Dang, S, Feng, S, Tien, J, Peters, CJ, Bulkley, D, Lolicato, M, Zhao, J, Zuberbühler, K, Ye, W, Qi, L, Chen, T, Craik, CS, Jan, YN, Minor, DL, Cheng, Y and Jan, LY (2017) Cryo-EM structures of the TMEM16A calcium-activated chloride channel. Nature 552, 426429.CrossRefGoogle ScholarPubMed
Deisenhofer, J, Epp, O, Miki, K, Huber, R and Michel, H (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318, 618624.CrossRefGoogle Scholar
Della Pia, EA, Hansen, RW, Zoonens, M and Martinez, KL (2014 a) Functionalized amphipols: a versatile toolbox suitable for applications of membrane proteins in synthetic biology. The Journal of Membrane Biology 247, 815826.CrossRefGoogle ScholarPubMed
Della Pia, EA, Holm, JV, Lloret, N, Le Bon, C, Popot, J-L, Zoonens, M, Nygård, J and Martinez, KL (2014 b) A step closer to membrane protein multiplexed nanoarrays using biotin-doped polypyrrole. ACS Nano 8, 18441853.CrossRefGoogle ScholarPubMed
Deme, JC, Johnson, S, Vickery, O, Aron, A, Monkhouse, H, Griffiths, T, James, RH, Berks, BC, Coulton, JW, Stansfeld, PJ and Lea, SM (2020) Structures of the stator complex that drives rotation of the bacterial flagellum. Nature Microbiology 5, 15531564.CrossRefGoogle ScholarPubMed
Deng, Z, Maksaev, G, Schlegel, AM, Zhang, J, Rau, M, Fitzpatrick, JAJ, Haswell, ES and Yuan, P (2020) Structural mechanism for gating of a eukaryotic mechanosensitive channel of small conductance. Nature Communications 11, 3690.CrossRefGoogle ScholarPubMed
Denisov, IG and Sligar, SG (2017) Nanodiscs in membrane biochemistry and biophysics. Chemical Reviews 117, 46694713.CrossRefGoogle ScholarPubMed
Denisov, IG, Grinkova, YV, Lazarides, AA and Sligar, SG (2004) Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. Journal of the American Chemical Society 126, 34773487.CrossRefGoogle ScholarPubMed
Denisov, IG, Schuler, MA and Sligar, SG (2019) Nanodiscs as a new tool to examine lipid-protein interactions. Methods in Molecular Biology 2003, 645671.CrossRefGoogle ScholarPubMed
De Zorzi, R, Mi, W, Liao, M and Walz, T (2016) Single-particle electron microscopy in the study of membrane protein structure. Microscopy 65, 8196.CrossRefGoogle Scholar
Diederichs, KA, Ni, X, Rollauer, SE, Botos, I, Tan, X, King, MS, Kunji, ERS, Jiang, J and Buchanan, SK (2020) Structural insight into mitochondrial β-barrel outer membrane protein biogenesis. Nature Communications 11, 3290.CrossRefGoogle ScholarPubMed
Dilworth, MV, Piel, MS, Bettaney, KE, Ma, P, Luo, J, Sharples, D, Poyner, DR, Gross, SR, Moncoq, K, Henderson, PJF, Miroux, B and Bill, RM (2018) Microbial expression systems for membrane proteins. Methods 147, 339.CrossRefGoogle ScholarPubMed
D'Imprima, E, Floris, D, Joppe, M, Sánchez, R, Grininger, M and Kühlbrandt, W (2019) Protein denaturation at the air-water interface and how to prevent it. eLife 8, e42747.CrossRefGoogle Scholar
Dobro, MJ, Melanson, LA, Jensen, GJ and McDowall, AW (2010) Plunge freezing for electron cryomicroscopy. Methods in Enzymology 481, 6382.CrossRefGoogle ScholarPubMed
Draper-Joyce, CJ, Khoshouei, M, Thal, DM, Liang, Y-L, Nguyen, ATN, Furness, SGB, Venugopal, H, Baltos, J-A, Plitzko, JM, Danev, R, Baumeister, W, May, LT, Wootten, D, Sexton, PM, Glukhova, A and Christopoulos, A (2018) Structure of the adenosine-bound human adenosine A 1 receptor–G i complex. Nature 558, 559563.CrossRefGoogle Scholar
Drulyte, I, Johnson, RM, Hesketh, EL, Hurdiss, DL, Scarff, CA, Porav, SA, Ranson, NA, Muench, SP and Thompson, RF (2018) Approaches to altering particle distributions in cryo-electron microscopy sample preparation. Acta Crystallographica. Section D, Structural Biology 74, 560571.CrossRefGoogle ScholarPubMed
Falzone, ME, Rheinberger, J, Lee, B-C, Peyear, T, Sasset, L, Raczkowski, AM, Eng, ET, Di Lorenzo, A, Andersen, OS, Nimigean, CM and Accardi, A (2019) Structural basis of Ca2+-dependent activation and lipid transport by a TMEM16 scramblase. eLife 8, e43229.CrossRefGoogle ScholarPubMed
Fan, C, Sukomon, N, Flood, E, Rheinberger, J, Allen, TW and Nimigean, CM (2020) Ball-and-chain inactivation in a calcium-gated potassium channel. Nature 580, 288293.CrossRefGoogle Scholar
Feng, X, Fu, Z, Kaledhonkar, S, Jia, Y, Shah, B, Jin, A, Liu, Z, Sun, M, Chen, B, Grassucci, RA, Ren, Y, Jiang, H, Frank, J and Lin, Q (2017) A fast and effective microfluidic spraying-plunging method for high-resolution single-particle cryo-EM. Structure 25, 663670.e3.CrossRefGoogle ScholarPubMed
Feng, S, Dang, S, Han, TW, Ye, W, Jin, P, Cheng, T, Li, J, Jan, YN, Jan, LY and Cheng, Y (2019) Cryo-EM studies of TMEM16F calcium-activated Ion channel suggest features important for lipid scrambling. Cell Reports 28, 567579.e4.CrossRefGoogle ScholarPubMed
Flores, JA, Haddad, BG, Dolan, KA, Myers, JB, Yoshioka, CC, Copperman, J, Zuckerman, DM and Reichow, SL (2020) Connexin-46/50 in a dynamic lipid environment resolved by CryoEM at 1.9Å. Nature Communications 11, 4331.CrossRefGoogle Scholar
Flötenmeyer, M, Weiss, H, Tribet, C, Popot, J-L and Leonard, K (2007) The use of amphipathic polymers for cryo-electron microscopy of NADH:ubiquinone oxidoreductase (Complex I). Journal of Microscopy 227, 229235.CrossRefGoogle Scholar
Frauenfeld, J, Gumbart, J, van der Sluis, EO, Funes, S, Gartmann, M, Beatrix, B, Mielke, T, Berninghausen, O, Becker, T, Schulten, K and Beckmann, R (2011) Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nature Structural & Molecular Biology 18, 614621.CrossRefGoogle ScholarPubMed
Frauenfeld, J, Löving, R, Armache, J-P, Sonnen, AF-P, Guettou, F, Moberg, P, Zhu, L, Jegerschöld, C, Flayhan, A, Briggs, JAG, Garoff, H, Löw, C, Cheng, Y and Nordlund, P (2016) A saposin-lipoprotein nanoparticle system for membrane proteins. Nature Methods 13, 345351.CrossRefGoogle ScholarPubMed
Fukunaga, K, Szabo, L, Fales, HM and Pitha, J (1988) 2-Hydroxypropyldigitonin: synthesis and properties of preparations differing in degree of substitution. Journal of Pharmaceutical Sciences 77, 640642.CrossRefGoogle ScholarPubMed
Gao, Y, Hu, H, Ramachandran, S, Erickson, JW, Cerione, RA and Skiniotis, G (2019) Structures of the rhodopsin-transducin complex: insights into G-protein activation. Molecular Cell 75, 781790.e3.CrossRefGoogle ScholarPubMed
Gao, S, Valinsky, WC, On, NC, Houlihan, PR, Qu, Q, Liu, L, Pan, X, Clapham, DE and Yan, N (2020 a) Employing NaChBac for cryo-EM analysis of toxin action on voltage-gated Na+ channels in nanodisc. Proceedings of the National Academy of Sciences of the USA 117, 1418714193.CrossRefGoogle ScholarPubMed
Gao, Y, Eskici, G, Ramachandran, S, Poitevin, F, Seven, AB, Panova, O, Skiniotis, G and Cerione, RA (2020 b) Structure of the visual signaling complex between transducin and phosphodiesterase 6. Molecular Cell 80, 237245.e4.CrossRefGoogle ScholarPubMed
Garavito, RM and Ferguson-Miller, S (2001) Detergents as tools in membrane biochemistry. The Journal of Biological Chemistry 276, 3240332406.CrossRefGoogle ScholarPubMed
Gatsogiannis, C, Merino, F, Prumbaum, D, Roderer, D, Leidreiter, F, Meusch, D and Raunser, S (2016) Membrane insertion of a Tc toxin in near-atomic detail. Nature Structural & Molecular Biology 23, 884890.CrossRefGoogle ScholarPubMed
Gharpure, A, Teng, J, Zhuang, Y, Noviello, CM, Walsh, RM, Cabuco, R, Howard, RJ, Zaveri, NT, Lindahl, E and Hibbs, RE (2019) Agonist selectivity and ion permeation in the α3β4 ganglionic nicotinic receptor. Neuron 104, 501511.e6.CrossRefGoogle ScholarPubMed
Giusti, F, Popot, J-L and Tribet, C (2012) Well-defined critical association concentration and rapid adsorption at the air/water interface of a short amphiphilic polymer, amphipol A8-35: a study by Förster resonance energy transfer and dynamic surface tension measurements. Langmuir 28, 1037210380.CrossRefGoogle Scholar
Giusti, F, Kessler, P, Hansen, RW, Della Pia, EA, Le Bon, C, Mourier, G, Popot, J-L, Martinez, KL and Zoonens, M (2015) Synthesis of a polyhistidine-bearing amphipol and its use for immobilizing membrane proteins. Biomacromolecules 16, 37513761.CrossRefGoogle ScholarPubMed
Glaeser, RM and Han, B-G (2017) Opinion: hazards faced by macromolecules when confined to thin aqueous films. Biophysics Reports 3, 17.CrossRefGoogle ScholarPubMed
Glaeser, RM, Han, B-G, Csencsits, R, Killilea, A, Pulk, A and Cate, JHD (2016) Factors that influence the formation and stability of thin, cryo-EM specimens. Biophysical Journal 110, 749755.CrossRefGoogle ScholarPubMed
Glavier, M, Puvanendran, D, Salvador, D, Decossas, M, Phan, G, Garnier, C, Frezza, E, Cece, Q, Schoehn, G, Picard, M, Taveau, J-C, Daury, L, Broutin, I and Lambert, O (2020) Antibiotic export by MexB multidrug efflux transporter is allosterically controlled by a MexA-OprM chaperone-like complex. Nature Communications 11, 4948.CrossRefGoogle ScholarPubMed
Gong, D, Chi, X, Wei, J, Zhou, G, Huang, G, Zhang, L, Wang, R, Lei, J, Chen, SRW and Yan, N (2019) Modulation of cardiac ryanodine receptor 2 by calmodulin. Nature 572, 347351.CrossRefGoogle ScholarPubMed
Gopalasingam, CC, Johnson, RM, Chiduza, GN, Tosha, T, Yamamoto, M, Shiro, Y, Antonyuk, SV, Muench, SP and Hasnain, SS (2019) Dimeric structures of quinol-dependent nitric oxide reductases (qNORs) revealed by cryo-electron microscopy. Science Advances 5, eaax1803.CrossRefGoogle ScholarPubMed
Grinkova, YV, Denisov, IG and Sligar, SG (2010) Engineering extended membrane scaffold proteins for self-assembly of soluble nanoscale lipid bilayers. Protein Engineering, Design & Selection 23, 843848.CrossRefGoogle ScholarPubMed
Gu, J, Wu, M, Guo, R, Yan, K, Lei, J, Gao, N and Yang, M (2016) The architecture of the mammalian respirasome. Nature 537, 639643.CrossRefGoogle ScholarPubMed
Guan, C, Niu, Y, Chen, S-C, Kang, Y, Wu, J-X, Nishi, K, Chang, CCY, Chang, T-Y, Luo, T and Chen, L (2020) Structural insights into the inhibition mechanism of human sterol O-acyltransferase 1 by a competitive inhibitor. Nature Communications 11, 2478.CrossRefGoogle ScholarPubMed
Guo, YR and MacKinnon, R (2017) Structure-based membrane dome mechanism for piezo mechanosensitivity. eLife 6, e33660.CrossRefGoogle ScholarPubMed
Hauer, F, Gerle, C, Fischer, N, Oshima, A, Shinzawa-Itoh, K, Shimada, S, Yokoyama, K, Fujiyoshi, Y and Stark, H (2015) GraDeR: membrane protein complex preparation for single-particle cryo-EM. Structure 23, 17691775.CrossRefGoogle ScholarPubMed
Hays, FA, Roe-Zurz, Z and Stroud, RM (2010) Overexpression and purification of integral membrane proteins in yeast. Methods in Enzymology 470, 695707.CrossRefGoogle ScholarPubMed
Henderson, R (1995) The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. Quarterly Reviews of Biophysics 28, 171193.CrossRefGoogle ScholarPubMed
Henderson, R and Unwin, PNT (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257, 2832.CrossRefGoogle ScholarPubMed
Henderson, R, Baldwin, JM, Ceska, TA, Zemlin, F, Beckmann, E and Downing, KH (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. Journal of Molecular Biology 213, 899929.CrossRefGoogle ScholarPubMed
Higgins, AJ, Flynn, AJ, Marconnet, A, Musgrove, LJ, Postis, VLG, Lippiat, JD, Chung, C, Ceska, T, Zoonens, M, Sobott, F and Muench, SP Cycloalkane-modified amphiphilic polymers provide direct extraction of membrane proteins for CryoEM analysis. Submitted for publication. doi:10.21203/rs.3.rs-131488/v1CrossRefGoogle Scholar
Hovers, J, Potschies, M, Polidori, A, Pucci, B, Raynal, S, Bonneté, F, Serrano-Vega, M, Tate, C, Picot, D, Pierre, Y, Popot, J-L, Nehmé, R, Bidet, M, Mus-Veteau, I, Bußkamp, H, Jung, K-H, Marx, A, Timmins, PA and Welte, W (2011) A class of mild surfactants that keep integral membrane proteins water-soluble for functional studies and crystallization. Molecular Membrane Biology 28, 171181. https://blanco.biomol.uci.edu/mpstruc/.CrossRefGoogle ScholarPubMed
Hua, T, Li, X, Wu, L, Iliopoulos-Tsoutsouvas, C, Wang, Y, Wu, M, Shen, L, Johnston, CA, Nikas, SP, Song, F, Song, X, Yuan, S, Sun, Q, Wu, Y, Jiang, S, Grim, TW, Benchama, O, Stahl, EL, Zvonok, N, Zhao, S, Bohn, LM, Makriyannis, A and Liu, Z-J (2020) Activation and signaling mechanism revealed by cannabinoid receptor-Gi complex structures. Cell 180, 655665.e18.CrossRefGoogle ScholarPubMed
Huang, W, Masureel, M, Qu, Q, Janetzko, J, Inoue, A, Kato, HE, Robertson, MJ, Nguyen, KC, Glenn, JS, Skiniotis, G and Kobilka, BK (2020 a) Structure of the neurotensin receptor 1 in complex with β-arrestin 1. Nature 579, 303308.CrossRefGoogle ScholarPubMed
Huang, Y, Wang, X, Lv, G, Razavi, AM, Huysmans, GHM, Weinstein, H, Bracken, C, Eliezer, D and Boudker, O (2020 b) Use of paramagnetic 19F NMR to monitor domain movement in a glutamate transporter homolog. Nature Chemical Biology 16, 10061012.CrossRefGoogle Scholar
Ishchenko, A, Abola, EE and Cherezov, V (2017) Crystallization of membrane proteins: an overview. Methods in Molecular Biology 1607, 117141.CrossRefGoogle ScholarPubMed
Itskanov, S and Park, E (2019) Structure of the posttranslational Sec protein-translocation channel complex from yeast. Science 363, 8487.CrossRefGoogle ScholarPubMed
Jin, Q, Zhang, B, Zheng, X, Li, N, Xu, L, Xie, Y, Song, F, Bhat, EA, Chen, Y, Gao, N, Guo, J, Zhang, X and Ye, S (2020) Cryo-EM structures of human pannexin 1 channel. Cell Research 30, 449451.CrossRefGoogle ScholarPubMed
Johnson, ZL and Chen, J (2018) ATP binding enables substrate release from multidrug resistance protein 1. Cell 172, 8189.e10.CrossRefGoogle ScholarPubMed
Johnson, S, Fong, YH, Deme, JC, Furlong, EJ, Kuhlen, L and Lea, SM (2020) Symmetry mismatch in the MS-ring of the bacterial flagellar rotor explains the structural coordination of secretion and rotation. Nature Microbiology 5, 966975.CrossRefGoogle ScholarPubMed
Jojoa-Cruz, S, Saotome, K, Murthy, SE, Tsui, CCA, Sansom, MS, Patapoutian, A and Ward, AB (2018) Cryo-EM structure of the mechanically activated ion channel OSCA1⋅2. eLife 7, e41845.CrossRefGoogle Scholar
Kalienkova, V, Clerico Mosina, V, Bryner, L, Oostergetel, GT, Dutzler, R and Paulino, C (2019) Stepwise activation mechanism of the scramblase nhTMEM16 revealed by cryo-EM. eLife 8, e44364.CrossRefGoogle ScholarPubMed
Kampjut, D and Sazanov, LA (2019) Structure and mechanism of mitochondrial proton-translocating transhydrogenase. Nature 573, 291295.CrossRefGoogle ScholarPubMed
Kampjut, D and Sazanov, LA (2020) The coupling mechanism of mammalian respiratory complex I. Science 370, eabc4209.CrossRefGoogle ScholarPubMed
Kater, L, Frieg, B, Berninghausen, O, Gohlke, H, Beckmann, R and Kedrov, A (2019) Partially inserted nascent chain unzips the lateral gate of the Sec translocon. EMBO Reports 20, e48191.CrossRefGoogle ScholarPubMed
Khelashvili, G, Falzone, ME, Cheng, X, Lee, B-C, Accardi, A and Weinstein, H (2019) Dynamic modulation of the lipid translocation groove generates a conductive ion channel in Ca2+-bound nhTMEM16. Nature Communications 10, 115.CrossRefGoogle ScholarPubMed
Kim, JJ, Gharpure, A, Teng, J, Zhuang, Y, Howard, RJ, Zhu, S, Noviello, CM, Walsh, RM, Lindahl, E and Hibbs, RE (2020 a) Shared structural mechanisms of general anaesthetics and benzodiazepines. Nature 585, 303308.CrossRefGoogle ScholarPubMed
Kim, Y, Jeong, E, Jeong, J-H, Kim, Y and Cho, Y (2020 b) Structural basis for activation of the heterodimeric GABAB receptor. Journal of Molecular Biology 432, 59665984.CrossRefGoogle ScholarPubMed
Kishikawa, J-I, Nakanishi, A, Furuta, A, Kato, T, Namba, K, Tamakoshi, M, Mitsuoka, K and Yokoyama, K (2020) Mechanical inhibition of isolated Vo from V/A-ATPase for proton conductance. eLife 9, e56862.CrossRefGoogle ScholarPubMed
Knowles, TJ, 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. Journal of the American Chemical Society 131, 74847485.CrossRefGoogle ScholarPubMed
Koehl, A, Hu, H, Feng, D, Sun, B, Zhang, Y, Robertson, MJ, Chu, M, Kobilka, TS, Laeremans, T, Steyaert, J, Tarrasch, J, Dutta, S, Fonseca, R, Weis, WI, Mathiesen, JM, Skiniotis, G and Kobilka, BK (2019) Structural insights into the activation of metabotropic glutamate receptors. Nature 566, 7984.CrossRefGoogle ScholarPubMed
Kühlbrandt, W (2013) Introduction to electron crystallography. Methods in Molecular Biology 955, 116.CrossRefGoogle ScholarPubMed
Kuhlen, L, Johnson, S, Zeitler, A, Bäurle, S, Deme, JC, Caesar, JJE, Debo, R, Fisher, J, Wagner, S and Lea, SM (2020) The substrate specificity switch FlhB assembles onto the export gate to regulate type three secretion. Nature Communications 11, 1296.CrossRefGoogle ScholarPubMed
Kun, E, Kirsten, E and Piper, WN (1979) Stabilization of mitochondrial functions with digitonin. Methods in Enzymology 55, 115118.CrossRefGoogle ScholarPubMed
Lauber, F, Deme, JC, Lea, SM and Berks, BC (2018) Type 9 secretion system structures reveal a new protein transport mechanism. Nature 564, 7782.CrossRefGoogle ScholarPubMed
Le Bon, C, Della Pia, EA, Giusti, F, Lloret, N, Zoonens, M, Martinez, KL and Popot, J-L (2014) Synthesis of an oligonucleotide-derivatized amphipol and its use to trap and immobilize membrane proteins. Nucleic Acids Research 42, e83.CrossRefGoogle ScholarPubMed
Le Bon, C, Marconnet, A, Masscheleyn, S, Popot, J-L and Zoonens, M (2018) Folding and stabilizing membrane proteins in amphipol A8-35. Methods 147, 95105.CrossRefGoogle ScholarPubMed
Letts, JA, Fiedorczuk, K and Sazanov, LA (2016) The architecture of respiratory supercomplexes. Nature 537, 644648.CrossRefGoogle ScholarPubMed
Letts, JA, Fiedorczuk, K, Degliesposti, G, Skehel, M and Sazanov, LA (2019) Structures of respiratory supercomplex I + III2 reveal functional and conformational crosstalk. Molecular Cell 75, 11311146.e6.CrossRefGoogle ScholarPubMed
Li, J, Richards, MR, Bagal, D, Campuzano, IDG, Kitova, EN, Xiong, ZJ, Privé, GG and Klassen, JS (2016) Characterizing the size and composition of saposin A lipoprotein picodiscs. Analytical Chemistry 88, 95249531.CrossRefGoogle ScholarPubMed
Liang, Y-L, Khoshouei, M, Radjainia, M, Zhang, Y, Glukhova, A, Tarrasch, J, Thal, DM, Furness, SGB, Christopoulos, G, Coudrat, T, Danev, R, Baumeister, W, Miller, LJ, Christopoulos, A, Kobilka, BK, Wootten, D, Skiniotis, G and Sexton, PM (2017) Phase-plate cryo-EM structure of a class B GPCR-G-protein complex. Nature 546, 118123.CrossRefGoogle Scholar
Liao, M, Cao, E, Julius, D and Cheng, Y (2013) Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504, 107112.CrossRefGoogle ScholarPubMed
Linsky, TW, Vergara, R, Codina, N, Nelson, JW, Walker, MJ, Su, W, Barnes, CO, Hsiang, T-Y, Esser-Nobis, K, Yu, K, Reneer, ZB, Hou, YJ, Priya, T, Mitsumoto, M, Pong, A, Lau, UY, Mason, ML, Chen, J, Chen, A, Berrocal, T, Peng, H, Clairmont, NS, Castellanos, J, Lin, Y-R, Josephson-Day, A, Baric, RS, Fuller, DH, Walkey, CD, Ross, TM, Swanson, R, Bjorkman, PJ, Gale, M, Blancas-Mejia, LM, Yen, H-L and Silva, D-A (2020) De novo design of potent and resilient hACE2 decoys to neutralize SARS-CoV-2. Science 370, 12081214.CrossRefGoogle ScholarPubMed
Liu, F, Zhang, Z, Csanády, L, Gadsby, DC and Chen, J (2017) Molecular structure of the human CFTR ion channel. Cell 169, 8595.e8.CrossRefGoogle ScholarPubMed
Liu, F, Zhang, Z, Levit, A, Levring, J, Touhara, KK, Shoichet, BK and Chen, J (2019 a) Structural identification of a hotspot on CFTR for potentiation. Science 364, 11841188.CrossRefGoogle ScholarPubMed
Liu, S, Chang, S, Han, B, Xu, L, Zhang, M, Zhao, C, Yang, W, Wang, F, Li, J, Delpire, E, Ye, S, Bai, X-C and Guo, J (2019 b) Cryo-EM structures of the human cation-chloride cotransporter KCC1. Science 366, 505508.CrossRefGoogle ScholarPubMed
Liu, J, Wan, F, Jin, Q, Li, X, Bhat, EA, Guo, J, Lei, M, Guan, F, Wu, J and Ye, S (2020) Cryo-EM structures of human calcium homeostasis modulator 5. Cell Discovery 6, 14.CrossRefGoogle ScholarPubMed
Llaguno, MC, Xu, H, Shi, L, Huang, N, Zhang, H, Liu, Q and Jiang, Q-X (2014) Chemically functionalized carbon films for single molecule imaging. Journal of Structural Biology 185, 405417.CrossRefGoogle ScholarPubMed
Lopez-Redondo, ML, Coudray, N, Zhang, Z, Alexopoulos, J and Stokes, DL (2018) Structural basis for the alternating access mechanism of the cation diffusion facilitator YiiP. Proceedings of the National Academy of Sciences of the USA 115, 30423047.CrossRefGoogle ScholarPubMed
Lu, P, Bai, X-C, Ma, D, Xie, T, Yan, C, Sun, L, Yang, G, Zhao, Y, Zhou, R, Scheres, SHW and Shi, Y (2014) Three-dimensional structure of human γ-secretase. Nature 512, 166170.CrossRefGoogle ScholarPubMed
Ma, S, Shen, Q, Zhao, L-H, Mao, C, Zhou, XE, Shen, D-D, de Waal, PW, Bi, P, Li, C, Jiang, Y, Wang, M-W, Sexton, PM, Wootten, D, Melcher, K, Zhang, Y and Xu, HE (2020) Molecular basis for hormone recognition and activation of corticotropin-releasing factor receptors. Molecular Cell 77, 669680.e4.CrossRefGoogle ScholarPubMed
Maeda, S, Yamamoto, H, Kinch, LN, Garza, CM, Takahashi, S, Otomo, C, Grishin, NV, Forli, S, Mizushima, N and Otomo, T (2020) Structure, lipid scrambling activity and role in autophagosome formation of ATG9A. Nature Structural & Molecular Biology 27, 11941201.CrossRefGoogle ScholarPubMed
Magnani, F, Shibata, Y, Serrano-Vega, MJ and Tate, CG (2008) Co-evolving stability and conformational homogeneity of the human adenosine A2a receptor. Proceedings of the National Academy of Sciences of the USA 105, 1074410749.CrossRefGoogle ScholarPubMed
Maldonado, M, Padavannil, A, Zhou, L, Guo, F and Letts, JA (2020) Atomic structure of a mitochondrial complex I intermediate from vascular plants. eLife 9, e56664.CrossRefGoogle ScholarPubMed
Marconnet, A, Michon, B, Le Bon, C, Giusti, F, Tribet, C and Zoonens, M (2020) Solubilization and stabilization of membrane proteins by cycloalkane-modified amphiphilic polymers. Biomacromolecules 21, 34593467.CrossRefGoogle ScholarPubMed
Martin-Garcia, JM, Conrad, CE, Coe, J, Roy-Chowdhury, S and Fromme, P (2016) Serial femtosecond crystallography: a revolution in structural biology. Archives of Biochemistry and Biophysics 602, 3247.CrossRefGoogle ScholarPubMed
Martin, TG, Bharat, TAM, Joerger, AC, Bai, X-C, Praetorius, F, Fersht, AR, Dietz, H and Scheres, SHW (2016) Design of a molecular support for cryo-EM structure determination. Proceedings of the National Academy of Sciences of the USA 113, e7456e7463.CrossRefGoogle ScholarPubMed
McCullough, J, Clippinger, AK, Talledge, N, Skowyra, ML, Saunders, MG, Naismith, TV, Colf, LA, Afonine, P, Arthur, C, Sundquist, WI, Hanson, PI and Frost, A (2015) Structure and membrane remodeling activity of ESCRT-III helical polymers. Science 350, 15481551.CrossRefGoogle ScholarPubMed
McDowell, MA, Heimes, M, Fiorentino, F, Mehmood, S, Farkas, Á, Coy-Vergara, J, Wu, D, Bolla, JR, Schmid, V, Heinze, R, Wild, K, Flemming, D, Pfeffer, S, Schwappach, B, Robinson, CV and Sinning, I (2020) Structural basis of tail-anchored membrane protein biogenesis by the GET insertase complex. Molecular Cell 80, 7286.e7.CrossRefGoogle ScholarPubMed
McGoldrick, LL, Singh, AK, Saotome, K, Yelshanskaya, MV, Twomey, EC, Grassucci, RA and Sobolevsky, AI (2018) Opening of the human epithelial calcium channel TRPV6. Nature 553, 233237.CrossRefGoogle ScholarPubMed
McGoldrick, LL, Singh, AK, Demirkhanyan, L, Lin, T-Y, Casner, RG, Zakharian, E and Sobolevsky, AI (2019) Structure of the thermo-sensitive TRP channel TRP1 from the alga Chlamydomonas reinhardtii. Nature Communications 10, 4180.CrossRefGoogle ScholarPubMed
Meyerson, JR, Rao, P, Kumar, J, Chittori, S, Banerjee, S, Pierson, J, Mayer, ML and Subramaniam, S (2014) Self-assembled monolayers improve protein distribution on holey carbon cryo-EM supports. Scientific Reports 4, 7084.CrossRefGoogle ScholarPubMed
Mio, K and Sato, C (2018) Lipid environment of membrane proteins in cryo-EM based structural analysis. Biophysical Reviews 10, 307316.CrossRefGoogle ScholarPubMed
Nagy, JK, Kuhn Hoffmann, A, Keyes, MH, Gray, DN, Oxenoid, K and Sanders, CR (2001) Use of amphipathic polymers to deliver a membrane protein to lipid bilayers. FEBS Letters 501, 115120.CrossRefGoogle ScholarPubMed
Nakane, T, Kotecha, A, Sente, A, McMullan, G, Masiulis, S, Brown, PMGE, Grigoras, IT, Malinauskaite, L, Malinauskas, T, Miehling, J, Uchański, T, Yu, L, Karia, D, Pechnikova, EV, de Jong, E, Keizer, J, Bischoff, M, McCormack, J, Tiemeijer, P, Hardwick, SW, Chirgadze, DY, Murshudov, G, Aricescu, AR and Scheres, SHW (2020) Single-particle cryo-EM at atomic resolution. Nature 587, 152156.CrossRefGoogle ScholarPubMed
Nannenga, BL and Gonen, T (2019) The cryo-EM method microcrystal electron diffraction (MicroED). Nature Methods 16, 369379.CrossRefGoogle Scholar
Nasr, ML and Wagner, G (2018) Covalently circularized nanodiscs; challenges and applications. Current Opinion in Structural Biology 51, 129134.CrossRefGoogle ScholarPubMed
Nasr, ML, Baptista, D, Strauss, M, Sun, ZJ, Grigoriu, S, Huser, S, Plückthun, A, Hagn, F, Walz, T, Hogle, JM and Wagner, G (2017) Covalently circularized nanodiscs for studying membrane proteins and viral entry. Nature Methods 14, 4952.CrossRefGoogle ScholarPubMed
Nguyen, C and Gonen, T (2020) Beyond protein structure determination with MicroED. Current Opinion in Structural Biology 64, 5158.CrossRefGoogle ScholarPubMed
Nguyen, NX, Armache, J-P, Lee, C, Yang, Y, Zeng, W, Mootha, VK, Cheng, Y, Bai, X-C and Jiang, Y (2018) Cryo-EM structure of a fungal mitochondrial calcium uniporter. Nature 559, 570574.CrossRefGoogle ScholarPubMed
Nguyen, AH, Thomsen, ARB, Cahill, TJ, Huang, R, Huang, L-Y, Marcink, T, Clarke, OB, Heissel, S, Masoudi, A, Ben-Hail, D, Samaan, F, Dandey, VP, Tan, YZ, Hong, C, Mahoney, JP, Triest, S, Little, J, Chen, X, Sunahara, R, Steyaert, J, Molina, H, Yu, Z, des Georges, A and Lefkowitz, RJ (2019) Structure of an endosomal signaling GPCR-G protein-β-arrestin megacomplex. Nature Structural & Molecular Biology 26, 11231131.CrossRefGoogle ScholarPubMed
Niu, Y, Tao, X, Touhara, KK and MacKinnon, R (2020) Cryo-EM analysis of PIP2 regulation in mammalian GIRK channels. eLife 9, e60552.CrossRefGoogle ScholarPubMed
Noble, AJ, Dandey, VP, Wei, H, Brasch, J, Chase, J, Acharya, P, Tan, YZ, Zhang, Z, Kim, LY, Scapin, G, Rapp, M, Eng, ET, Rice, WJ, Cheng, A, Negro, CJ, Shapiro, L, Kwong, PD, Jeruzalmi, D, des Georges, A, Potter, CS and Carragher, B (2018) Routine single particle CryoEM sample and grid characterization by tomography. eLife 7, e34257.CrossRefGoogle ScholarPubMed
Nogales, E and Scheres, SHW (2015) Cryo-EM: a unique tool for the visualization of macromolecular complexity. Molecular Cell 58, 677689.CrossRefGoogle ScholarPubMed
Nwanochie, E and Uversky, VN (2019) Structure determination by single-particle cryo-electron microscopy: only the sky (and intrinsic disorder) is the limit. International Journal of Molecular Sciences 20, 4186.CrossRefGoogle ScholarPubMed
Nygaard, R, Kim, J and Mancia, F (2020) Cryo-electron microscopy analysis of small membrane proteins. Current Opinion in Structural Biology 64, 2633.CrossRefGoogle ScholarPubMed
Orwick-Rydmark, M, Arnold, T and Linke, D (2016) The use of detergents to purify membrane proteins. Current Protocols in Protein Science 84, 4.8.14.8.35.CrossRefGoogle ScholarPubMed
Otzen, DE (2015) Proteins in a brave new surfactant world. Current Opinion in Colloid & Interface Science 20, 161169.CrossRefGoogle Scholar
Owji, AP, Zhao, Q, Ji, C, Kittredge, A, Hopiavuori, A, Fu, Z, Ward, N, Clarke, OB, Shen, Y, Zhang, Y, Hendrickson, WA and Yang, T (2020) Structural and functional characterization of the bestrophin-2 anion channel. Nature Structural & Molecular Biology 27, 382391.CrossRefGoogle ScholarPubMed
Parey, K, Haapanen, O, Sharma, V, Köfeler, H, Züllig, T, Prinz, S, Siegmund, K, Wittig, I, Mills, DJ, Vonck, J, Kühlbrandt, W and Zickermann, V (2019) High-resolution cryo-EM structures of respiratory complex I: mechanism, assembly, and disease. Science Advances 5, eaax9484.CrossRefGoogle ScholarPubMed
Pérez-Pérez, R, Lobo-Jarne, T, Milenkovic, D, Mourier, A, Bratic, A, García-Bartolomé, A, Fernández-Vizarra, E, Cadenas, S, Delmiro, A, García-Consuegra, I, Arenas, J, Martín, MA, Larsson, N-G and Ugalde, C (2016) COX7A2L is a mitochondrial complex III binding protein that stabilizes the III2 + IV supercomplex without affecting respirasome formation. Cell Reports 16, 23872398.CrossRefGoogle ScholarPubMed
Perlmutter, JD, Popot, J-L and Sachs, JN (2014) Molecular dynamics simulations of a membrane protein/amphipol complex. The Journal of Membrane Biology 247, 883895.CrossRefGoogle ScholarPubMed
Perry, TN, Souabni, H, Rapisarda, C, Fronzes, R, Giusti, F, Popot, J-L, Zoonens, M and Gubellini, F (2019) BAmSA: visualising transmembrane regions in protein complexes using biotinylated amphipols and electron microscopy. Biochimica Et Biophysica Acta. Biomembranes 1861, 466477.CrossRefGoogle ScholarPubMed
Picard, M, Dahmane, T, Garrigos, M, Gauron, C, Giusti, F, le Maire, M, Popot, J-L and Champeil, P (2006) Protective and inhibitory effects of various types of amphipols on the Ca2+-ATPase from sarcoplasmic reticulum: a comparative study. Biochemistry 45, 18611869.CrossRefGoogle ScholarPubMed
Pinke, G, Zhou, L and Sazanov, LA (2020) Cryo-EM structure of the entire mammalian F-type ATP synthase. Nature Structural & Molecular Biology 27, 10771085.CrossRefGoogle ScholarPubMed
Piton, J, Pojer, F, Wakatsuki, S, Gati, C and Cole, ST (2020) High resolution CryoEM structure of the ring-shaped virulence factor EspB from Mycobacterium tuberculosis. Journal of Structural Biology X 4, 100029.CrossRefGoogle ScholarPubMed
Pleiner, T, Tomaleri, GP, Januszyk, K, Inglis, AJ, Hazu, M and Voorhees, RM (2020) Structural basis for membrane insertion by the human ER membrane protein complex. Science 369, 433436.Google ScholarPubMed
Pocanschi, CL, Popot, J-L and Kleinschmidt, JH (2013) Folding and stability of outer membrane protein A (OmpA) from Escherichia coli in an amphipathic polymer, amphipol A8-35. European biophysics journal 42, 103118.CrossRefGoogle Scholar
Popot, J-L (2018) Membrane Proteins in Aqueous Solutions: From Detergents to Amphipols. New York: Springer.CrossRefGoogle Scholar
Popot, J-L, Althoff, T, Bagnard, D, Banères, J-L, Bazzacco, P, Billon-Denis, E, Catoire, LJ, Champeil, P, Charvolin, D, Cocco, MJ, Crémel, G, Dahmane, T, de la Maza, LM, Ebel, C, Gabel, F, Giusti, F, Gohon, Y, Goormaghtigh, E, Guittet, E, Kleinschmidt, JH, Kühlbrandt, W, Le Bon, C, Martinez, KL, Picard, M, Pucci, B, Sachs, JN, Tribet, C, van Heijenoort, C, Wien, F, Zito, F and Zoonens, M (2011) Amphipols from A to Z. Annual Review of Biophysics 40, 379408.CrossRefGoogle ScholarPubMed
Qian, H, Wu, X, Du, X, Yao, X, Zhao, X, Lee, J, Yang, H and Yan, N (2020) Structural basis of low-pH-dependent lysosomal cholesterol egress by NPC1 and NPC2. Cell 182, 98111.e18.CrossRefGoogle ScholarPubMed
Qiao, A, Han, S, Li, X, Li, Z, Zhao, P, Dai, A, Chang, R, Tai, L, Tan, Q, Chu, X, Ma, L, Thorsen, TS, Reedtz-Runge, S, Yang, D, Wang, M-W, Sexton, PM, Wootten, D, Sun, F, Zhao, Q and Wu, B (2020) Structural basis of Gs and Gi recognition by the human glucagon receptor. Science 367, 13461352.CrossRefGoogle ScholarPubMed
Qiu, W, Fu, Z, Xu, GG, Grassucci, RA, Zhang, Y, Frank, J, Hendrickson, WA and Guo, Y (2018) Structure and activity of lipid bilayer within a membrane-protein transporter. Proceedings of the National Academy of Sciences of the USA 115, 1298512990.CrossRefGoogle ScholarPubMed
Rahman, MM, Teng, J, Worrell, BT, Noviello, CM, Lee, M, Karlin, A, Stowell, MHB and Hibbs, RE (2020) Structure of the native muscle-type nicotinic receptor and inhibition by snake venom toxins. Neuron 106, 952962.e5.CrossRefGoogle ScholarPubMed
Ravelli, RBG, Nijpels, FJT, Henderikx, RJM, Weissenberger, G, Thewessem, S, Gijsbers, A, Beulen, BWAMM, López-Iglesias, C and Peters, PJ (2020) Cryo-EM structures from sub-nl volumes using pin-printing and jet vitrification. Nature Communications 11, 2563.CrossRefGoogle ScholarPubMed
Razinkov, I, Dandey, V, Wei, H, Zhang, Z, Melnekoff, D, Rice, WJ, Wigge, C, Potter, CS and Carragher, B (2016) A new method for vitrifying samples for cryoEM. Journal of Structural Biology 195, 190198.CrossRefGoogle ScholarPubMed
Reddy, B, Bavi, N, Lu, A, Park, Y and Perozo, E (2019) Molecular basis of force-from-lipids gating in the mechanosensitive channel MscS. eLife 8, e50486.CrossRefGoogle ScholarPubMed
Righetto, RD, Biyani, N, Kowal, J, Chami, M and Stahlberg, H (2019) Retrieving high-resolution information from disordered 2D crystals by single-particle cryo-EM. Nature Communications 10, 1722.CrossRefGoogle ScholarPubMed
Roh, S-H, Stam, NJ, Hryc, CF, Couoh-Cardel, S, Pintilie, G, Chiu, W and Wilkens, S (2018) The 3.5-Å CryoEM structure of nanodisc-reconstituted yeast vacuolar ATPase Vo proton channel. Molecular Cell 69, 9931004.e3.CrossRefGoogle ScholarPubMed
Roh, S-H, Shekhar, M, Pintilie, G, Chipot, C, Wilkens, S, Singharoy, A and Chiu, W (2020) Cryo-EM and MD infer water-mediated proton transport and autoinhibition mechanisms of Vo complex. Science Advances 6, eabb9605.CrossRefGoogle ScholarPubMed
Rosevear, P, VanAken, T, Baxter, J and Ferguson-Miller, S (1980) Alkyl glycoside detergents: a simpler synthesis and their effects on kinetic and physical properties of cytochrome c oxidase. Biochemistry 19, 41084115.CrossRefGoogle ScholarPubMed
Ruan, Z, Orozco, IJ, Du, J and , W (2020 a) Structures of human pannexin 1 reveal ion pathways and mechanism of gating. Nature 584, 646651.CrossRefGoogle ScholarPubMed
Ruan, Z, Osei-Owusu, J, Du, J, Qiu, Z and , W (2020 b) Structures and pH-sensing mechanism of the proton-activated chloride channel. Nature 588, 350354.CrossRefGoogle ScholarPubMed
Russo, CJ and Passmore, LA (2014) Ultrastable gold substrates for electron cryomicroscopy. Science 346, 13771380.CrossRefGoogle ScholarPubMed
Sadaf, A, Cho, KH, Byrne, B and Chae, PS (2015) Amphipathic agents for membrane protein study. Methods in Enzymology 557, 5794.CrossRefGoogle ScholarPubMed
Sauer, DB, Trebesch, N, Marden, JJ, Cocco, N, Song, J, Koide, A, Koide, S, Tajkhorshid, E and Wang, D-N (2020) Structural basis for the reaction cycle of DASS dicarboxylate transporters. eLife 9, e61350.CrossRefGoogle ScholarPubMed
Schmidli, C, Albiez, S, Rima, L, Righetto, R, Mohammed, I, Oliva, P, Kovacik, L, Stahlberg, H and Braun, T (2019) Microfluidic protein isolation and sample preparation for high-resolution cryo-EM. Proceedings of the National Academy of Sciences of the USA 116, 1500715012.CrossRefGoogle ScholarPubMed
Sgro, GG and Costa, TRD (2018) Cryo-EM grid preparation of membrane protein samples for single particle analysis. Frontiers in Molecular Biosciences 5, 74.CrossRefGoogle ScholarPubMed
Shen, PS, Yang, X, DeCaen, PG, Liu, X, Bulkley, D, Clapham, DE and Cao, E (2016) The structure of the polycystic kidney disease channel PKD2 in lipid nanodiscs. Cell 167, 763773.e11.CrossRefGoogle ScholarPubMed
Shen, H, Li, Z, Jiang, Y, Pan, X, Wu, J, Cristofori-Armstrong, B, Smith, JJ, Chin, YKY, Lei, J, Zhou, Q, King, GF and Yan, N (2018) Structural basis for the modulation of voltage-gated sodium channels by animal toxins. Science 362, eaau2596.CrossRefGoogle ScholarPubMed
Shih, AY, Denisov, IG, Phillips, JC, Sligar, SG and Schulten, K (2005) Molecular dynamics simulations of discoidal bilayers assembled from truncated human lipoproteins. Biophysical Journal 88, 548556.CrossRefGoogle ScholarPubMed
Singh, AK, McGoldrick, LL and Sobolevsky, AI (2018) Structure and gating mechanism of the transient receptor potential channel TRPV3. Nature Structural & Molecular Biology 25, 805813.CrossRefGoogle ScholarPubMed
Sligar, SG and Denisov, IG (2020) Nanodiscs: a toolkit for membrane protein science. Protein Science 30, 297315.CrossRefGoogle ScholarPubMed
Sousa, JS, Mills, DJ, Vonck, J and Kühlbrandt, W (2016) Functional asymmetry and electron flow in the bovine respirasome. eLIFE 5, e21290.CrossRefGoogle ScholarPubMed
Srivastava, AP, Luo, M, Zhou, W, Symersky, J, Bai, D, Chambers, MG, Faraldo-Gómez, JD, Liao, M and Mueller, DM (2018) High-resolution cryo-EM analysis of the yeast ATP synthase in a lipid membrane. Science 360, eaas9699.CrossRefGoogle Scholar
Stetsenko, A and Guskov, A (2017) An overview of the top ten detergents used for membrane protein crystallization. Crystals 7, 197.CrossRefGoogle Scholar
Stroud, Z, Hall, SCL and Dafforn, TR (2018) Purification of membrane proteins free from conventional detergents: SMA, new polymers, new opportunities and new insights. Methods 147, 106117.CrossRefGoogle ScholarPubMed
Sui, X, Arlt, H, Brock, KP, Lai, ZW, DiMaio, F, Marks, DS, Liao, M, Farese, RV and Walther, TC (2018) Cryo-electron microscopy structure of the lipid droplet-formation protein seipin. The Journal of Cell Biology 217, 40804091.CrossRefGoogle ScholarPubMed
Sun, J and MacKinnon, R (2020) Structural basis of human KCNQ1 modulation and gating. Cell 180, 340347.e9.CrossRefGoogle ScholarPubMed
Sun, C, Benlekbir, S, Venkatakrishnan, P, Wang, Y, Hong, S, Hosler, J, Tajkhorshid, E, Rubinstein, JL and Gennis, RB (2018) Structure of the alternative complex III in a supercomplex with cytochrome oxidase. Nature 557, 123126.CrossRefGoogle Scholar
Sverzhinsky, A, Qian, S, Yang, L, Allaire, M, Moraes, I, Ma, D, Chung, JW, Zoonens, M, Popot, J-L and Coulton, JW (2014) Amphipol-trapped ExbB-ExbD membrane protein complex from Escherichia coli: a biochemical and structural case study. The Journal of Membrane Biology 247, 10051018.CrossRefGoogle ScholarPubMed
Tao, X and MacKinnon, R (2019) Molecular structures of the human Slo1 K+ channel in complex with β4. eLife 8, e51409.CrossRefGoogle ScholarPubMed
Tascón, I, Sousa, JS, Corey, RA, Mills, DJ, Griwatz, D, Aumüller, N, Mikusevic, V, Stansfeld, PJ, Vonck, J and Hänelt, I (2020) Structural basis of proton-coupled potassium transport in the KUP family. Nature Communications 11, 626.CrossRefGoogle ScholarPubMed
Tate, CG (2010) Practical considerations of membrane protein instability during purification and crystallisation. Heterologous expression of membrane proteins: methods and protocols. In Mus-Veteau, I (ed.), Methods in Molecular Biology. Totowa, NJ: Humana Press, pp. 187203.Google Scholar
Thompson, AA, Liu, JJ, Chun, E, Wacker, D, Wu, H, Cherezov, V and Stevens, RC (2011) GPCR stabilization using the bicelle-like architecture of mixed sterol-detergent micelles. Methods 55, 310317.CrossRefGoogle ScholarPubMed
Tonggu, L and Wang, L (2018) Broken Symmetry in the Human BK Channel, bioRxiv.CrossRefGoogle Scholar
Tonggu, L and Wang, L (2020) Cryo-EM sample preparation method for extremely low concentration liposomes. Ultramicroscopy 208, 112849.CrossRefGoogle ScholarPubMed
Tribet, C, Audebert, R and Popot, J-L (1996) Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proceedings of the National Academy of Sciences 93, 1504715050.CrossRefGoogle ScholarPubMed
Tsai, C-J, Marino, J, Adaixo, R, Pamula, F, Muehle, J, Maeda, S, Flock, T, Taylor, NM, Mohammed, I, Matile, H, Dawson, RJ, Deupi, X, Stahlberg, H and Schertler, G (2019) Cryo-EM structure of the rhodopsin-Gαi-βγ complex reveals binding of the rhodopsin C-terminal tail to the gβ subunit. eLife 8, e46041.CrossRefGoogle ScholarPubMed
Tsutsumi, N, Mukherjee, S, Waghray, D, Janda, CY, Jude, KM, Miao, Y, Burg, JS, Aduri, NG, Kossiakoff, AA, Gati, C and Garcia, KC (2020) Structure of human Frizzled5 by fiducial-assisted cryo-EM supports a heterodimeric mechanism of canonical Wnt signaling. eLife 9, e58464.CrossRefGoogle ScholarPubMed
Tucker, K and Park, E (2019) Cryo-EM structure of the mitochondrial protein-import channel TOM complex at near-atomic resolution. Nature Structural & Molecular Biology 26, 11581166.CrossRefGoogle ScholarPubMed
Uchański, T, Masiulis, S, Fischer, B, Kalichuk, V, López-Sánchez, U, Zarkadas, E, Weckener, M, Sente, A, Ward, P, Wohlkönig, A, Zögg, T, Remaut, H, Naismith, JH, Nury, H, Vranken, W, Aricescu, AR, Pardon, E and Steyaert, J (2021) Megabodies expand the nanobody toolkit for protein structure determination by single-particle cryo-EM. Nature Methods 18, 6068.CrossRefGoogle ScholarPubMed
Vinayagam, D, Quentin, D, Yu-Strzelczyk, J, Sitsel, O, Merino, F, Stabrin, M, Hofnagel, O, Yu, M, Ledeboer, MW, Nagel, G, Malojcic, G and Raunser, S (2020) Structural basis of TRPC4 regulation by calmodulin and pharmacological agents. eLife 9, e60603.CrossRefGoogle ScholarPubMed
Vinothkumar, KR and Henderson, R (2016) Single particle electron cryomicroscopy: trends, issues and future perspective. Quarterly Reviews of Biophysics 49, e13.CrossRefGoogle ScholarPubMed
Walter, JD, Sawicka, M and Dutzler, R (2019) Cryo-EM structures and functional characterization of murine Slc26a9 reveal mechanism of uncoupled chloride transport. eLife 8, e46986.CrossRefGoogle ScholarPubMed
Wang, X and Boudker, O (2020) Large domain movements through the lipid bilayer mediate substrate release and inhibition of glutamate transporters. eLife 9, e58417.CrossRefGoogle ScholarPubMed
Wang, L and Sigworth, FJ (2009) Structure of the BK potassium channel in a lipid membrane from electron cryomicroscopy. Nature 461, 292295.CrossRefGoogle Scholar
Wang, L and Sigworth, FJ (2010) Liposomes on a streptavidin crystal: a system to study membrane proteins by cryo-EM. Methods in Enzymology 481, 147164.CrossRefGoogle ScholarPubMed
Wang, K, Preisler, SS, Zhang, L, Cui, Y, Missel, JW, Grønberg, C, Gotfryd, K, Lindahl, E, Andersson, M, Calloe, K, Egea, PF, Klaerke, DA, Pusch, M, Pedersen, PA, Zhou, ZH and Gourdon, P (2019) Structure of the human ClC-1 chloride channel. PLoS Biology 17, e3000218.CrossRefGoogle ScholarPubMed
Wang, L, Johnson, ZL, Wasserman, MR, Levring, J, Chen, J and Liu, S (2020 a) Characterization of the kinetic cycle of an ABC transporter by single-molecule and cryo-EM analyses. eLife 9, e56451.CrossRefGoogle ScholarPubMed
Wang, Z, Hu, W and Zheng, H (2020b) Pathogenic siderophore ABC importer YbtPQ adopts a surprising fold of exporter. Science Advances 6, eaay7997.CrossRefGoogle Scholar
Wasilko, DJ, Johnson, ZL, Ammirati, M, Che, Y, Griffor, MC, Han, S and Wu, H (2020) Structural basis for chemokine receptor CCR6 activation by the endogenous protein ligand CCL20. Nature Communications 11, 3031.CrossRefGoogle ScholarPubMed
Weiss, HM and Grisshammer, R (2002) Purification and characterization of the human adenosine A(2a) receptor functionally expressed in Escherichia coli. European Journal of Biochemistry 269, 8292.CrossRefGoogle ScholarPubMed
Weiss, MS, Wacker, T, Weckesser, J, Weite, W and Schulz, GE (1990) The three-dimensional structure of porin from Rhodobacter capsulatus at 3 Å resolution. FEBS Letters 267, 268272.CrossRefGoogle ScholarPubMed
Willegems, K and Efremov, RG (2018) Influence of lipid mimetics on gating of ryanodine receptor. Structure 26, 13031313.e4.CrossRefGoogle ScholarPubMed
Wu, S, Avila-Sakar, A, Kim, J, Booth, DS, Greenberg, CH, Rossi, A, Liao, M, Li, X, Alian, A, Griner, SL, Juge, N, Yu, Y, Mergel, CM, Chaparro-Riggers, J, Strop, P, Tampé, R, Edwards, RH, Stroud, RM, Craik, CS and Cheng, Y (2012) Fabs enable single particle cryoEM studies of small proteins. Structure 20, 582592.CrossRefGoogle ScholarPubMed
Wu, M, Gu, J, Guo, R, Huang, Y and Yang, M (2016) Structure of mammalian respiratory supercomplex I1III2IV1. Cell 167, 15981609.e10.CrossRefGoogle ScholarPubMed
Wu, X, Cabanos, C and Rapoport, TA (2019) Structure of the post-translational protein translocation machinery of the ER membrane. Nature 566, 136139.CrossRefGoogle ScholarPubMed
Wu, X, Siggel, M, Ovchinnikov, S, Mi, W, Svetlov, V, Nudler, E, Liao, M, Hummer, G and Rapoport, TA (2020) Structural basis of ER-associated protein degradation mediated by the Hrd1 ubiquitin ligase complex. Science 368, eaaz2449.CrossRefGoogle ScholarPubMed
Yan, R, Zhao, X, Lei, J and Zhou, Q (2019) Structure of the human LAT1-4F2hc heteromeric amino acid transporter complex. Nature 568, 127130.CrossRefGoogle ScholarPubMed
Yang, G, Zhou, R, Zhou, Q, Guo, X, Yan, C, Ke, M, Lei, J and Shi, Y (2019) Structural basis of notch recognition by human γ-secretase. Nature 565, 192197.CrossRefGoogle ScholarPubMed
Yao, X, Fan, X and Yan, N (2020) Cryo-EM analysis of a membrane protein embedded in the liposome. Proceedings of the National Academy of Sciences 117, 1849718503.CrossRefGoogle ScholarPubMed
Yin, W, Li, Z, Jin, M, Yin, Y-L, de Waal, PW, Pal, K, Yin, Y, Gao, X, He, Y, Gao, J, Wang, X, Zhang, Y, Zhou, H, Melcher, K, Jiang, Y, Cong, Y, Edward Zhou, X, Yu, X and Eric Xu, H (2019 a) A complex structure of arrestin-2 bound to a G protein-coupled receptor. Cell Research 29, 971983.CrossRefGoogle ScholarPubMed
Yin, Y, Wu, M, Hsu, AL, Borschel, WF, Borgnia, MJ, Lander, GC and Lee, S-Y (2019 b) Visualizing structural transitions of ligand-dependent gating of the TRPM2 channel. Nature Communications 10, 114.CrossRefGoogle ScholarPubMed
Yin, J, Chen, K-YM, Clark, MJ, Hijazi, M, Kumari, P, Bai, X-C, Sunahara, RK, Barth, P and Rosenbaum, DM (2020) Structure of a D2 dopamine receptor-G-protein complex in a lipid membrane. Nature 584, 125129.CrossRefGoogle Scholar
Yoder, N and Gouaux, E (2020) The His-Gly motif of acid-sensing ion channels resides in a reentrant ‘loop’ implicated in gating and ion selectivity. eLife 9, e56527.CrossRefGoogle Scholar
Yoo, J, Wu, M, Yin, Y, Herzik, MA, Lander, GC and Lee, S-Y (2018) Cryo-EM structure of a mitochondrial calcium uniporter. Science 361, 506511.Google ScholarPubMed
Yu, X, Plotnikova, O, Bonin, PD, Subashi, TA, McLellan, TJ, Dumlao, D, Che, Y, Dong, YY, Carpenter, EP, West, GM, Qiu, X, Culp, JS and Han, S (2019) Cryo-EM structures of the human glutamine transporter SLC1A5 (ASCT2) in the outward-facing conformation. eLife 8, e48120.CrossRefGoogle ScholarPubMed
Zhang, Z, Liu, F and Chen, J (2017) Conformational changes of CFTR upon phosphorylation and ATP binding. Cell 170, 483491.e8.CrossRefGoogle ScholarPubMed
Zhang, C, Konermann, S, Brideau, NJ, Lotfy, P, Wu, X, Novick, SJ, Strutzenberg, T, Griffin, PR, Hsu, PD and Lyumkis, D (2018 a) Structural basis for the RNA-guided ribonuclease activity of CRISPR-Cas13d. Cell 175, 212223.e17.CrossRefGoogle ScholarPubMed
Zhang, Z, Liu, F and Chen, J (2018 b) Molecular structure of the ATP-bound, phosphorylated human CFTR. Proceedings of the National Academy of Sciences of the USA 115, 1275712762.CrossRefGoogle ScholarPubMed
Zhang, L, Zhao, Y, Gao, Y, Wu, L, Gao, R, Zhang, Q, Wang, Y, Wu, C, Wu, F, Gurcha, SS, Veerapen, N, Batt, SM, Zhao, W, Qin, L, Yang, X, Wang, M, Zhu, Y, Zhang, B, Bi, L, Zhang, X, Yang, H, Guddat, LW, Xu, W, Wang, Q, Li, J, Besra, GS and Rao, Z (2020) Structures of cell wall arabinosyltransferases with the anti-tuberculosis drug ethambutol. Science 368, 12111219.CrossRefGoogle ScholarPubMed
Zhao, DY, Pöge, M, Morizumi, T, Gulati, S, Van Eps, N, Zhang, J, Miszta, P, Filipek, S, Mahamid, J, Plitzko, JM, Baumeister, W, Ernst, OP and Palczewski, K (2019 a) Cryo-EM structure of the native rhodopsin dimer in nanodiscs. The Journal of Biological Chemistry 294, 1421514230.CrossRefGoogle ScholarPubMed
Zhao, J, Xu, H, Carroni, M, Lebrette, H, Wallden, K, Moe, A, Matsuoka, R, Högbom, M and Zou, X (2019 b) A simple pressure-assisted method for cryo-EM specimen preparation. bioRxiv, 665448.CrossRefGoogle Scholar
Zhao, L-H, Ma, S, Sutkeviciute, I, Shen, D-D, Zhou, XE, de Waal, PW, Li, C-Y, Kang, Y, Clark, LJ, Jean-Alphonse, FG, White, AD, Yang, D, Dai, A, Cai, X, Chen, J, Li, C, Jiang, Y, Watanabe, T, Gardella, TJ, Melcher, K, Wang, M-W, Vilardaga, J-P, Xu, HE and Zhang, Y (2019 c) Structure and dynamics of the active human parathyroid hormone receptor-1. Science 364, 148153.CrossRefGoogle ScholarPubMed
Zhao, Y, Huang, G, Wu, J, Wu, Q, Gao, S, Yan, Z, Lei, J and Yan, N (2019 d) Molecular basis for ligand modulation of a mammalian voltage-gated Ca2+ channel. Cell 177, 14951506.e12.CrossRefGoogle ScholarPubMed
Zhao, J, Lin King, JV, Paulsen, CE, Cheng, Y and Julius, D (2020) Irritant-evoked activation and calcium modulation of the TRPA1 receptor. Nature 585, 141145.CrossRefGoogle ScholarPubMed
Zheng, L, Li, Y, Li, X, Zhong, Q, Li, N, Zhang, K, Zhang, Y, Chu, H, Ma, C, Li, G, Zhao, J and Gao, N (2019) Structural and functional insights into the tetrameric photosystem I from heterocyst-forming cyanobacteria. Nature Plants 5, 10871097.CrossRefGoogle ScholarPubMed
Zhou, X, Li, M, Su, D, Jia, Q, Li, H, Li, X and Yang, J (2017) Cryo-EM structures of the human endolysosomal TRPML3 channel in three distinct states. Nature Structural and Molecular Biology 24, 11461154.CrossRefGoogle ScholarPubMed
Zhou, R, Yang, G, Guo, X, Zhou, Q, Lei, J and Shi, Y (2019) Recognition of the amyloid precursor protein by human γ-secretase. Science 363, eaaw0930.CrossRefGoogle ScholarPubMed
Zoonens, M and Miroux, B (2010) Expression of membrane proteins at the Escherichia coli membrane for structural studies. Methods in Molecular Biology 601, 4966.CrossRefGoogle ScholarPubMed
Zoonens, M and Popot, J-L (2014) Amphipols for each season. The Journal of Membrane Biology 247, 759796.CrossRefGoogle ScholarPubMed
Zoonens, M, Giusti, F, Zito, F and Popot, J-L (2007) Dynamics of membrane protein/amphipol association studied by Förster resonance energy transfer: implications for in vitro studies of amphipol-stabilized membrane proteins. Biochemistry 46, 1039210404.CrossRefGoogle ScholarPubMed
Zubcevic, L, Herzik, MA, Chung, BC, Liu, Z, Lander, GC and Lee, S-Y (2016) Cryo-electron microscopy structure of the TRPV2 ion channel. Nature Structural & Molecular Biology 23, 180186.CrossRefGoogle ScholarPubMed
Zubcevic, L, Herzik, MA, Wu, M, Borschel, WF, Hirschi, M, Song, AS, Lander, GC and Lee, S-Y (2018) Conformational ensemble of the human TRPV3 ion channel. Nature Communications 9, 112.CrossRefGoogle ScholarPubMed
Zubcevic, L, Hsu, AL, Borgnia, MJ and Lee, S-Y (2019) Symmetry transitions during gating of the TRPV2 ion channel in lipid membranes. eLife 8, e45779.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Le Bon et al. supplementary material

Le Bon et al. supplementary material

Download Le Bon et al. supplementary material(PDF)
PDF 341.2 KB