Using a SMALP platform to determine a sub-nm single particle cryo-EM membrane protein structure

Biochimica et Biophysica Acta - Biomembranes

Volumn 1860, Issue 2, 2018, Pages 378-383

  Parmar, Mayuriben ^a,b   Rawson, Shaun ^b   Scarff, Charlotte A ^b   Goldman, Adrian ^b,c   Dafforn, Timothy R ^d   Muench, Stephen P ^b   Postis, Vincent L G ^a,b  

^a LEEDS METROPOLITAN UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

AcrB; Electron microscopy; Membrane proteins; SMALP

Indexed keywords

ACRB PROTEIN; AMPHOPHILE; DETERGENT; MEMBRANE PROTEIN; NANODISC; NANOMATERIAL; STYRENE MALEIC ACID LIPOPARTICLE; STYRENE MALEIC ANHYDRIDE COPOLYMER; UNCLASSIFIED DRUG; ACRB PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; MALEIC ACID; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN; POLYSTYRENE DERIVATIVE; PROTEOLIPID; PROTEOLIPOSOMES; STYRENE-MALEIC ACID POLYMER;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LIPID INTERACTION; PROTEIN POLYMERIZATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STRUCTURE ANALYSIS; CHEMISTRY; LIPID BILAYER; METABOLISM; MOLECULAR MODEL; PROCEDURES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIPID BILAYERS; MALEATES; MEMBRANE PROTEINS; MODELS, MOLECULAR; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; POLYSTYRENES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEOLIPIDS;

EID: 85034763479     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2017.10.005     Document Type: Article

References (43)

1. Seddon, A.M., Curnow, P., Booth, P.J., Membrane proteins, lipids and detergents: not just a soap opera. Biochim. Biophys. Acta, Biomembr. 1666:1–2 (2004), 105–117.
2. Schulz, G.E., Validation of the detergent micelle classification for membrane protein crystals and explanation of the Matthews graph for soluble proteins. Protein Sci. 20:10 (2011), 1765–1770.
3. Rawson, S., Davies, S., Lippiat, J.D., Muench, S.P., The changing landscape of membrane protein structural biology through developments in electron microscopy. Mol. Membr. Biol. 33:1–2 (2016), 12–22.
4. Vinothkumar, K.R., Membrane protein structures without crystals by single particle electron microscopy. Curr. Opin. Struct. Biol. 33 (2015), 103–114.
5. Brown, A., Shao, S., Murray, J., Hedge, R.S., Ramakrishnan, V., Structural basis for stop codon recognition in eukaryotes. Nature 524 (2015), 493–496.
6. + channel. Cell 168:3 (2016), 390–399.
7. Moraes, I., Evans, G., Sanchez-Weatherby, J., Newstead, S., Stewart, P.D., Membrane protein structure determination - the next generation. Biochim. Biophys. Acta 1838 (2014), 78–87.
8. Andersen, O.S., Koeppe, R.E., Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36 (2007), 107–130.
9. Marsh, D., Protein modulation of lipids, and vice-versa, in membranes. Biochim. Biophys. Acta 1778:7–8 (2008), 1545–1575.
10. Phillips, R., Ursell, T., Wiggins, P., Sens, P., Emerging roles for lipids in shaping membrane-protein function. Nature 459 (2009), 379–385.
11. Gupta, K., Donlan, J.A., Hopper, J.T., Uzdavinys, P., Landreh, M., Struwe, W.B., Drew, D., Baldwin, A.J., Stansfeld, P.J., Robinson, C.V., The role of interfacial lipids in stabilizing membrane protein oligomers. Nature 541 (2017), 421–424.
12. Gutmann, D.A., Mizohata, E., Newstead, S., Ferrandon, S., Postis, V., Xia, X., Henderson, P.J., van Veen, H.W., Byrne, B., A high-throughput method for membrane protein solubility screening: the ultracentrifugation dispersity sedimentation assay. Protein Sci. 16:7 (2007), 1422–1428.
13. Postis, V.L., Deacon, S.E., Roach, P.C., Wright, G.S., Xia, X., Ingram, J.C., Hadden, J.M., Henderson, P.J., Phillips, S.E., McPherson, M.J., Baldwin, S.A., A high-throughput assay of membrane protein stability. Mol. Membr. Biol. 25:8 (2008), 617–624.
14. Huynh, K.W., Cohen, M.R., Moiseenkova-Bell, V.Y., Application of amphipols for structure-functional analysis of TRP channels. J. Membr. Biol. 247:9–10 (2014), 843–851.
15. Baker, M.R., Fan, G., Serysheva, I.I., Single-particle cryo-EM of the ryanodine receptor channel in an aqueous environment. Eur. J. Transl. Myol. 25:1 (2015), 35–48.
16. Gao, Y., Cao, E., Julius, D., Cheng, Y., TRPV1 structure in nanodiscs reveal mechanisms of ligand and lipid action. Nature 534 (2016), 347–351.
17. Bayburt, T.H., Sligar, S.G., Membrane protein assembly into nanodisks. FEBS Lett. 584:9 (2010), 1721–1727.
18. Knowles, T.J., Finka, R., Smith, C., Lin, Y.P., Dafforn, T., Overduin, M., Membrane proteins solubilized intact in lipid containing nanoparticles bounded by styrene maleic acid copolymer. J. Am. Chem. Soc. 131:22 (2009), 7484–7485.
19. Dörr, J.M., Scheidelaar, S., Koorengevel, M.C., Dominguez, J.J., Schäfer, M., van Walree, C.A., Killian, J.A., The styrene-maleic acid co-polymer: a versatile tool in membrane research. Eur. Biophys. J. 45:1 (2016), 3–21.
20. + channel: the power of native nanodiscs. Proc. Natl. Acad. Sci. U. S. A. 111:52 (2014), 18607–18612.
21. Gulati, S., Jamshad, M., Knowles, T.J., Morrison, K.A., Downing, R., Cant, N., Collins, R., Koenderink, J.B., Ford, R.C., Overduin, M., Kerr, I.D., Dafforn, T.R., Rothnie, A.J., Detergent-free purification of ABC (ATP-binding-cassette) transporters. Biochem. J. 461:2 (2014), 269–278.
22. Postis, V., Rawson, S., Mitchell, J.K., Lee, S.C., Parslow, R.A., Dafforn, T.R., Baldwin, S.A., Muench, S.P., The use of SMALPs as a novel membrane protein scaffold for structure study by negative stain electron microscopy. Biochim. Biophys. Acta 1848:2 (2015), 496–501.
23. Broecker, J., Eger, B.T., Ernst, O.P., Crystallogenesis of membrane proteins mediated by polymer bounded lipid nanodiscs. Structure 25:2 (2017), 384–392.
24. Jamshad, M. et al., Structural analysis of a nanoparticle containing a lipid bilayer used for detergent-free extraction of membrane proteins. Nano Res. 8:3 (2014), 774–789.
25. Glover, C.A., Postis, V.L., Charalambous, K., Tzokov, S.B., Booth, W.I., Deacon, S.E., Wallace, B.A., Baldwin, S.A., Bullough, P.A., AcrB contamination in 2-D crystallization of membrane proteins: lessons from a sodium channel and a putative monovalent cation/proton antiporter. J. Struct. Biol. 176:3 (2011), 419–424.
26. Lee, S.C., Postis, V.L., Knowles, T.J., Jamshad, M., Parslow, R.A., Lin, Y., Goldman, A., Sridhar, P., Overduin, M., Muench, S.P., Dafforn, T.R., Detergent-free method of membrane protein isolation for biophysical methods. Nat. Protoc. 11:7 (2016), 1149–1162.
27. Tang, G., Peng, L., Baldwin, P.R., Mann, D.S., Jiang, W., Rees, I., Ludtke, S.J., EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157:1 (2007), 38–46.
28. Zheng, S.Q., Palovcak, E., Armache, J.P., Verba, K.A., Cheng, Y., Agard, D.A., MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14:4 (2017), 331–332.
29. Zhang, K., Gctf: real-time CTF determination and correction. J. Struct. Biol. 193:1 (2016), 1–12.
30. Scheres, S.H., RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180:3 (2012), 519–530.
31. Punjani, A., Rubinstein, J.L., Fleet, D.J., Brubaker, M.A., cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14:3 (2017), 290–296.
32. Daury, L., Orange, F., Taveau, J.C., Verchère, A., Monlezun, L., Gounou, C., Marreddy, R.K., Picard, M., Broutin, I., Pos, K.M., Lambert, O., Tripartite assembly of RND multidrug efflux pumps. Nat. Commun., 7, 2016, 10731, 10.1038/ncomms10731.
33. Murakami, S., Nakashima, R., Yamashita, E., Yamaguchi, A., Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419 (2002), 587–593.
34. Wang, Z., Fan, G., Hryc, C.F., Blaza, J.N., Serysheva, I.I., Schmid, M.F., Chiu, W., Luisi, B.F., Du, D., An allosteric transport mechanism for the AcrB-TolC multidrug efflux pump. elife, 6, 2017, 10.7554/eLife.24905.
35. Jeong, H., Kim, J.S., Song, S., Shigematsu, H., Yokoyama, T., Hyun, J., Ha, N.C., Pseudoatomic structure of the tripartite multidrug efflux pump AcrAB-TolC reveals the intermeshing cogwheel-like interaction between AcrA and TolC. Structure 24:2 (2016), 272–276.
36. Kim, J.S., Jeong, H., Song, S., Kim, H.Y., Lee, K., Hyun, J., Ha, N.C., Structure of the tripartite multidrug efflux pump AcrAB-TolC suggests an alternative assembly mode. Mol. Cell 38:2 (2015), 180–186.
37. Walker, M., White, H., Belknap, B., Trinick, J., Electron cryomicroscopy of acto-myosin-S1 during steady state ATP hydrolysis. Biophys. J. 66:5 (1994), 1563–1572.
38. Bai, X.C., Yan, C., Yang, G., Lu, P., Ma, D., Sun, L., Zhou, R., Scheres, S.H.W., Shi, Y., An atomic structure of human γ-secretase. Nature 525:7568 (2015), 212–217.
39. Frauenfeld, J. et al., A saposin-lipoprotein nanoparticle system for membrane proteins. Nat. Methods 13:4 (2016), 345–351.
40. Taylor, K.A., Glaeser, R.M., Retrospective on the early development of cryoelectron microscopy of macromolecules and a prospective on opportunities for the future. J. Struct. Biol. 163:3 (2008), 214–223.
41. Frey, L., Lakomek, N.A., Riek, R., Bibow, S., Micelles, bicelles, and nanodiscs: comparing the impact of membrane mimetics on membrane protein backbone dynamics. Agnew Chem. Int. Ed. Ingl. 56:1 (2017), 380–383.
42. Hazell, G., Arnold, T., Barker, R.D., Clifton, L.A., Steinke, N.J., Tognoloni, C., Edler, K.J., Evidence of lipid exchange in styrene maleic acid lipid particle (SMALP) nanodisc systems. Langmuir 32:45 (2016), 11845–11853.
43. Cuevas Arenas, R., Danielczak, B., Martel, A., Porcar, L., Breyton, C., Ebel, C., Keller, S., Fast collisional lipid transfer among polymer-bounded nanodiscs. Sci Rep, 7, 2017, 45875, 10.1038/srep45875.