The Use of Amphipols for Solution NMR Studies of Membrane Proteins: Advantages and Constraints as Compared to Other Solubilizing Media

Journal of Membrane Biology

Volumn 247, Issue 9-10, 2014, Pages 827-842

  Planchard, Noelya ^a,b   Point, Élodie ^a   Dahmane, Tassadite ^a,c   Giusti, Fabrice ^a   Renault, Marie ^d   Le Bon, Christel ^a   Durand, Grégory ^e,f   Milon, Alain ^d   Guittet, Éric ^g   Zoonens, Manuela ^a   Popot, Jean Luc ^a   Catoire, Laurent J ^a  

^a PSL Research University   (France)

^b AGROPARISTECH   (France)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^e UNIVERSITY OF AVIGNON   (France)

^f UNIVERSITÉ DE MONTPELLIER   (France)

^g INSTITUT DE CHIMIE DES SUBSTANCES NATURELLES   (France)

Author keywords

Amphipols; Membrane proteins; Solution NMR

Indexed keywords

AMPHIPOL; DETERGENT; LIGAND; MEMBRANE PROTEIN; NANODISC; OMPX PROTEIN; OUTER MEMBRANE PROTEIN; POLYMER; UNCLASSIFIED DRUG; LIPID BILAYER; SOLUTION AND SOLUBILITY; SURFACTANT; WATER;

ARTICLE; CHEMICAL STRUCTURE; CONTROLLED STUDY; ESCHERICHIA COLI; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OUTER MEMBRANE; PARTICLE SIZE; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; SOLUBILIZATION; ANIMAL; ARTIFACT; BIOMEDICAL TECHNOLOGY ASSESSMENT; CELL MEMBRANE; CHEMICAL PHENOMENA; CHEMISTRY; HUMAN; LIPID BILAYER; PROCEDURES; SOLUBILITY; SOLUTION AND SOLUBILITY;

ANIMALS; ARTIFACTS; CELL MEMBRANE; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; POLYMERS; SOLUBILITY; SOLUTIONS; SURFACE-ACTIVE AGENTS; TECHNOLOGY ASSESSMENT, BIOMEDICAL; WATER;

EID: 84910156400     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-014-9654-z     Document Type: Article

References (78)

1. 1. EMBO J 30:4652–4664
2. Arnold T, Poynor M, Nussberger S, Lupas AN, Linke D (2007) Gene duplication of the eight-stranded β-barrel OmpX produces a functional pore: a scenario for the evolution of transmembrane β-barrel. J Mol Biol 366:1174–1184
3. Arora A, Abildgaard F, Bushweller JH, Tamm LK (2001) Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat Struct Biol 8:334–338
4. 4 binding to recombinant BLT1. J Mol Biol 329:801–814
5. Banères JL, Popot JL, Mouillac B (2011) New advances in production and functional folding of G-protein-coupled receptors. Trends Biotechnol 29:314–322
6. Bayburt TH, Grinkova YV, Sligar SG (2002) Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett 2:853–856
7. Bazzacco P, Billon-Denis E, Sharma KS, Catoire LJ, Mary S, Le Bon C, Point E, Banères JL, Durand G, Zito F, Pucci B, Popot JL (2012) Nonionic homopolymeric amphipols: application to membrane protein folding, cell-free synthesis, and solution nuclear magnetic resonance. Biochemistry 51:1416–1430
8. Catoire LJ, Zoonens M, van Heijenoort C, Giusti F, Popot JL, Guittet E (2009) Inter- and intramolecular contacts in a membrane protein/surfactant complex observed by heteronuclear dipole-to-dipole cross-relaxation. J Magn Reson 197:91–95
9. 4 adopts a highly constrained conformation when associated to human BLT2. J Am Chem Soc 132:9049–9057
10. Catoire LJ, Zoonens M, van Heijenoort C, Giusti F, Guittet E, Popot JL (2010b) Solution NMR mapping of water-accessible residues in the transmembrane β-barrel of OmpX. Eur Biophys J 39:623–630
11. Catoire LJ, Damian M, Baaden M, Guittet E, Banères JL (2011) Electrostatically-driven fast association and perdeuteration allow detection of transferred cross-relaxation for G protein-coupled receptor ligands with equilibrium dissociation constants in the high-to-low nanomolar range. J Biomol NMR 50:191–195
12. Catoire LJ, Warnet XL, Warschawski DE (2014) Micelles, bicelles, amphipols, nanodiscs, liposomes or intact cells: the hitchhiker’s guide to the membrane protein study by NMR. In: Mus-Veteau I (ed) Membrane protein production for structural analysis. Springer, Berlin (in press)
13. Chae PS, Rasmussen SG, Rana RR, Gotfryd K, Chandra R, Goren MA, Kruse AC, Nurva S, Loland CJ, Pierre Y, Drew D, Popot JL, Picot D, Fox BG, Guan L, Gether U, Byrne B, Kobilka B, Gellman SH (2010) Maltose-neopentyl glycol (MNG) amphiphiles for solubilization, stabilization and crystallization of membrane proteins. Nat Methods 7:1003–1008
14. 2+-ATPase. J Biol Chem 275:18623–18637
15. Charvolin D, Perez JB, Rouvière F, Giusti F, Bazzacco P, Abdine A, Rappaport F, Martinez KL, Popot JL (2009) The use of amphipols as universal molecular adapters to immobilize membrane proteins onto solid supports. Proc Natl Acad Sci USA 106:405–410
16. Czerski L, Sanders CR (2000) Functionality of a membrane protein in bicelles. Anal Biochem 284:327–333
17. Dahmane T, Damian M, Mary S, Popot JL, Banères JL (2009) Amphipol-assisted in vitro folding of G protein-coupled receptors. Biochemistry 48:6516–6521
18. Dahmane T, Giusti F, Catoire LJ, Popot JL (2011) Sulfonated amphipols: synthesis, properties, and applications. Biopolymers 95:811–823
19. Dahmane T, Rappaport F, Popot JL (2013) Amphipol-assisted folding of bacteriorhodopsin in the presence and absence of lipids. Functional consequences. Eur Biophys J 42:85–101
20. Denisov IG, Grinkova YV, Lazarides AA, Sligar SG (2004) Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J Am Chem Soc 126:3477–3478
21. Diab C, Tribet C, Gohon Y, Popot JL, Winnik FM (2007) Complexation of integral membrane proteins by phosphorylcholine-based amphipols. Biochim Biophys Acta 1768:2737–2747
22. Dupont M, De E, Chollet R, Chevalier J, Pages J-M (2004) Enterobacter aerogenes OmpX, a cation-selective channel mar- and osmo-regulated. FEBS Lett 569:27–30
23. Elter S, Raschle T, Arens S, Gelev V, Etzkorn M, Wagner G (2014) The use of amphipols for NMR structural characterization of 7-TM proteins. J Membr Biol (in press)
24. Etzkorn M, Raschle T, Hagn F, Gelev V, Rice AJ, Walz T, Wagner G (2013) Cell-free expressed bacteriorhodopsin in different soluble membrane mimetics: biophysical properties and NMR accessibility. Structure 21:394–401
25. Etzkorn M, Zoonens M, Catoire LJ, Popot JL, Hiller S (2014) How amphipols embed membrane proteins: Global solvent accessibility and interaction with a flexible protein terminus. J Membr Biol (in press)
26. Fernández C, Adeishvili K, Wüthrich K (2001) Transverse relaxation-optimized NMR spectroscopy with the outer membrane protein OmpX in dihexanoyl phosphatidylcholine micelles. Proc Natl Acad Sci USA 98:2358–2363
27. Fiaux J, Bertelsen EB, Horwich AL, Wüthrich K (2002) NMR analysis of a 900 K GroEL GroES complex. Nature 418:207–211
28. Giusti F, Popot JL, 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 28:10372–10380
29. Giusti F, Rieger J, Catoire L, Qian, S, Calabrese AN, Watkinson TG, Radford S, Ashcroft A, Fradet A, Popot JL (2014) Synthesis, characterization and applications of a perdeuterated amphipol. J Membr Biol (in press)
30. Gohon Y, Pavlov G, Timmins P, Tribet C, Popot JL, Ebel C (2004) Partial specific volume and solvent interactions of amphipol A8-35. Anal Biochem 334:318–334
31. Gohon Y, Giusti F, Prata C, Charvolin D, Timmins P, Ebel C, Tribet C, Popot JL (2006) Well-defined nanoparticles formed by hydrophobic assembly of a short and polydisperse random terpolymer, amphipol A8-35. Langmuir 22:1281–1290
32. Gohon Y, Dahmane T, Ruigrok R, Schuck P, Charvolin D, Rappaport F, Timmins P, Engelman DM, Tribet C, Popot JL, Ebel C (2008) Bacteriorhodopsin/amphipol complexes: structural and functional properties. Biophys J 94:3523–3537
33. Griesinger C, Bennati M, Vieth HM, Luchinat C, Parigi G, Höfer P, Engelke F, Glaser SJ, Denysenkov V, Prisner TF (2012) Dynamic nuclear polarization at high magnetic fields in liquids. Prog Nucl Magn Reson Spectrosc 64:4–28
34. Hagn F, Etzkorn M, Raschle T, Wagner G (2013) Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J Am Chem Soc 135:1919–1925
35. Kang CB, Li Q (2011) Solution NMR study of integral membrane proteins. Curr Opin Struct Biol 15:560–569
36. Kelly E, Privé GG, Tieleman PD (2005) Molecular models of lipopeptide detergents: large coiled-coils with hydrocarbon interiors. J Am Chem Soc 127:13446–13447
37. Koutsopoulos S, Kaiser L, Eriksson HM, Zhang S (2012) Designer peptide surfactants stabilize diverse functional membrane proteins. Chem Soc Rev 41:1721–1728
38. Le Bon C, Popot JL, Giusti F (2014a) Labeling and functionalizing amphipols for biological applications. J Membr Biol (in press)
39. Le Bon C, Della Pia EA, Giusti F, Lloret N, Zoonens M, Martinez KL, Popot JL (2014b) Synthesis of an oligonucleotide-derivatized amphipol and its use to trap and immobilize membrane proteins. Nucleic Acids Res (in press)
40. Lee D, Walter KF, Brückner AK, 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
41. Martinez KL, Gohon Y, Corringer PJ, Tribet C, Mérola F, Changeux JP, Popot JL (2002) Allosteric transitions of Torpedo acetylcholine receptor in lipids, detergent and amphipols: molecular interactions vs. physical constraints. FEBS Lett 528:251–256
42. McGregor CL, Chen L, Pomroy NC, Hwang P, Go S, Chakrabartty A, Privé GG (2003) Lipopeptide detergents designed for the structural study of membrane proteins. Nat Biotechnol 21:171–176
43. Mouillac B, Banères JL (2010) Mammalian membrane receptors expression as inclusion bodies in Escherichia coli. Methods Mol Biol 601:39–48
44. Nath A, Atkins WM, Sligar SG (2007) Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins. Biochemistry 46:2059–2069
45. Pautsch A, Schulz GE (2000) High-resolution structure of the OmpA membrane domain. J Mol Biol 298:273–282
46. Perlmutter JD, Drasler WJ, Xie W, Gao J, Popot JL, Sachs JN (2011) All-atom and coarse-grained molecular dynamics simulations of a membrane protein stabilizing polymer. Langmuir 27:10523–10537
47. Perlmutter JD, Popot J-L, Sachs, JN (2014) Molecular dynamics simulations of a membrane protein/amphipol complex. Submitted for publication
48. 2+-ATPase from sarcoplasmic reticulum: a comparative study. Biochemistry 45:1861–1869
49. Plevin MJ, Boisbouvier J (2012) Isotope-labelling of methyl groups for NMR studies of large proteins In: Clore M, Potts J (eds) Recent developments in biomolecular NMR, RSC biomolecular sciences no. 25. Royal Society of Chemistry. doi:10.1039/9781849735391
50. Pocanschi CL, Dahmane T, Gohon Y et al (2006) Amphipathic polymers: tools to fold integral membrane proteins to their active form. Biochemistry 45:13954–13961
51. Poget SF, Girvin ME (2007) Solution NMR of membrane proteins in bilayer mimics: small is beautiful, but sometimes bigger is better. Biochim Biophys Acta 68:3098–3106
52. Popot JL (2010) Amphipols, nanodiscs, and fluorinated surfactants: three nonconventional approaches to studying membrane proteins in aqueous solutions. Ann Rev Biochem 79:737–775
53. Popot JL, Althoff T, Bagnard D et al (2011) Amphipols from A to Z. Ann Rev Biophys 40:379–408
54. Privé G (2009) Lipopeptide detergents for membrane protein studies. Curr Opin Struct Biol 19:1–7
55. Raschle T, Hiller S, Etzkorn M, Wagner G (2010) Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Curr Opin Struct Biol 20:471–479
56. Renault M (2008) Etudes structurales et dynamiques de la protéine membranaire KpOmpA par RMN en phase liquide et solide. Ph. D. Thesis Université Paul Sabatier, Toulouse, France
57. Renault M, Tommassen-van Boxtel R, Bos MP, Post JA, Tommassen J, Baldus M (2012) Cellular solid-state nuclear magnetic resonance spectroscopy. Proc Natl Acad Sci USA 109:4863–4868
58. Riek R, Wider G, Pervushin K, Wüthrich K (1999) Polarization transfer by cross-correlated relaxation in solution NMR with very large molecules. Proc Natl Acad Sci USA 96:4918–4923
59. Ritchie TK, Grinkova YV, Bayburt TH, Denisov IG, Zolnerciks JK, Atkins WM, Sligar SG (2009) Chapter 11—reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Methods Enzymol 464:211–213
60. Ruschak AM, Religa TL, Breuer S, Witt S, Kay LE (2010) The proteasome antechamber maintains substrates in an unfolded state. Nature 467:868–871
61. Sanders CR 2nd, Landis GC (1995) Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies. Biochemistry 34:4030–4040
62. Sharma KS, Durand G, Gabel F, Bazzacco P, Le Bon C, Billon-Denis E, Catoire LJ, Popot JL, Ebel C, Pucci B (2012) Non–ionic amphiphilic homopolymers: synthesis, solution properties, and biochemical validation. Langmuir 28:4625–4639
63. Takeda M, Kainosho M (2012) Cell-free protein synthesis using E. coli cell extract for NMR studies. Adv Exp Med Biol 992:167–177
64. Tifrea DF, Sun G, Pal S, Zardeneta G, Cocco MJ, Popot JL, de la Maza LM (2011) Amphipols stabilize the Chlamydia major outer membrane protein and enhance its protective ability as a vaccine. Vaccine 29:4623–4631
65. Triba MN, Warschawski DE, Devaux PF (2005) Reinvestigation by phosphorus NMR of lipid distribution in bicelles. Biophys J 88:1887–1901
66. Tribet C, Audebert R, Popot JL (1996) Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc Natl Acad Sci USA 93:15047–15050
67. Tribet C, Diab C, Dahmane T, Zoonens M, Popot JL, Winnik FM (2009) Thermodynamic characterization of the exchange of detergents and amphipols at the surfaces of integral membrane proteins. Langmuir 25:12623–12634
68. Vogt J, Schulz GE (1999) The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence. Structure 7:1301–1309
69. Vold RR, Prosser RS, Deese AJ (1997) Isotropic solutions of phospholipid bicelles: a new membrane mimetic for high-resolution NMR studies of polypeptides. J Biomol NMR 9:329–335
70. Wang X, Corin K, Baaske P, Wienken CJ, Jerabek-Willemsen M, Duhr S, Braun D, Zhang S (2011) Peptide surfactants for cell-free production of functional G protein-coupled receptors. Proc Natl Acad Sci USA 108:9049–9054
71. Warschawski DE, Arnold AA, Beaugrand M, Gravel A, Chartrand E, Marcotte I (2011) Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim Biophys Acta 1808:1957–1974
72. Wüthrich K (1986) NMR of proteins and nucleic acids. Wiley, New York
73. Yokomizo T, Kako K, Terawaki K, Izumi T, Shimizu T (2000) A second leukotriene B(4) receptor, BLT2. A new therapeutic target in inflammation and immunological disorders. J Exp Med 192:421–432
74. Zhao X, Nagai Y, Reeves PJ, Kiley P, Khorana HG, Zhang S (2006) Designer short peptide surfactants stabilize G protein-coupled receptor bovine rhodopsin. Proc Natl Acad Sci USA 103:17707–17712
75. Zhou HX, Cross TA (2013) Influences of membrane mimetic environments on membrane protein structures. Annu Rev Biophys 42:361–392
76. Zoonens M, Catoire LJ, Giusti F, Popot JL (2005) NMR study of a membrane protein in detergent–free aqueous solution. Proc Natl Acad Sci USA 102:8893–8898
77. Zoonens M, Giusti F, Zito F, Popot JL (2007) Dynamics of membrane protein/amphipol association studied by Förster resonance energy transfer. Implications for in vitro studies of amphipol-stabilized membrane proteins. Biochemistry 46:10392–10404
78. Zoonens M, Zito F, Martinez KL, Popot JL (2014) Amphipols: a general introduction and some protocols. In: Mus-Veteau I (ed) Membrane protein production for structural analysis. Springer, Berlin