Amphipols: A general introduction and some protocols

Membrane Proteins Production for Structural Analysis

Volumn , Issue , 2014, Pages 173-203

  Zoonens, Manuela ^a   Zito, Francesca ^a   Martinez, Karen L ^b   Popot, Jean Luc ^a  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84911006106     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4939-0662-8_7     Document Type: Chapter

References (97)

1. 1. EMBO J 30:4652-4664
2. 4receptor. A structural basis for drug efficacy. J Biol Chem 280:20253-20260
3. Banères J-L, Popot J-L, Mouillac B (2011) New advances in production and functional folding of G protein-coupled receptors. Trends Biotechnol 29:314-322
4. Basit H, Sharma S, Van der Heyden A, Gondran C, Breyton C, Dumy P, Winnik FM, Labbé P (2012) Amphipol mediated surface immobilization of FhuA: a platform for label-free detection of the bacteriophage protein pb5. Chem Commun 48:6037-6039
5. Bazzacco P, Sharma KS, Durand G, Giusti F, Ebel C, Popot J-L, Pucci B (2009) Trapping and stabilization of integral membrane proteins by hydrophobically grafted glucose-based telomers. Biomacromolecules 10:3317-3326
6. 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, Popot J-L (2012) Non-ionic homopolymeric amphipols: application to membrane protein folding, cell-free synthesis, and solution NMR. Biochemistry 51:1416-1430
7. Bechara C, Bolbach G, Bazzacco P, Sharma SK, Durand G, Popot J-L, Zito F, Sagan S (2012) MALDI mass spectrometry analysis of membrane protein/amphipol complexes. Anal Chem 84:6128-6135
8. Bowie JU (2001) Stabilizing membrane proteins. Curr Opin Struct Biol 11:397-402
9. Breyton C, Chabaud E, Chaudier Y, Pucci B, Popot J-L (2004) Hemifluorinated surfactants: a non-dissociating environment for handling membrane proteins in aqueous solutions? FEBS Lett 564:312-318
10. Breyton C, Gabel F, Abla M, Pierre Y, Lebaupain F, Durand G, Popot J-L, Ebel C, Pucci B (2009) Micellar and biochemical properties of (hemi)fluorinated surfactants are controlled by the size of the polar head. Biophys J 97:1077-1086
11. Breyton C, Pucci B, Popot J-L (2010) Amphipols and fluorinated surfactants: two alternatives to detergents for studying membrane proteins in vitro. In: Mus-Veteau I (ed) Heterologous expression of membrane proteins: methods and protocols, vol 601. The Humana Press, Totowa, pp 219-245
12. Cao E, Liao M, Cheng Y, Julius D (2013) TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504:113-118
13. Catoire LJ, Zoonens M, van Heijenoort C, Giusti F, Popot J-L, Guittet E (2009) Inter- and intramolecular contacts in a membrane protein/surfactant complex observed by heteronuclear dipole-to-dipole cross-relaxation. J Magn Res 197:91-95
14. 4adopts a highly constrained conformation when associated to human BLT2. J Am Chem Soc 132:9049-9057
15. Catoire LJ, Zoonens M, van Heijenoort C, Giusti F, Guittet E, Popot J-L (2010b) Solution NMR mapping of water-accessible residues in the transmembrane ^-barrel of OmpX. Eur Biophys J 39:623-630
16. Catoire LJ, Damian M, Baaden M, Guittet E, Banères J-L (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
17. Chabaud E, Barthélémy P, Mora N, Popot J-L, Pucci B (1998) Stabilization of integral membrane proteins in aqueous solution using fluorinated surfactants. Biochimie 80:515-530
18. Chae PS, Rasmussen SGF, Rana R, 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 BK, Gellman SH (2010) Maltose-neopentyl glycol (MNG) amphiphiles for solubilization, stabilization and crystallization of membrane proteins. Nat Methods 7:1003-1008
19. 2+-ATPase. J Biol Chem 275:18623-18637
20. Charvolin D, Perez J-B, Rouvière F, Giusti F, Bazzacco P, Abdine A, Rappaport F, Martinez KL, Popot J-L (2009) The use of amphipols as universal molecular adapters to immobilize membrane proteins onto solid supports. Proc Natl Acad Sci U S A 106:405-410
21. 1in the presence of amphipols J Membr Biol, in the press
22. Cvetkov TL, Huynh KW, Cohen MR, Moiseenkova-Bell VY (2011) Molecular architecture and subunit organization of TRPA1 ion channel revealed by electron microscopy. J Biol Chem 286:38168-38176
23. Dahmane T, Damian M, Mary S, Popot J-L, Banères J-L (2009) Amphipol-assisted in vitro folding of G protein-coupled receptors. Biochemistry 48:6516-6521
24. Dahmane T, Giusti F, Catoire LJ, Popot J-L (2011) Sulfonated amphipols: synthesis, properties and applications. Biopolymers 95:811-823
25. Dahmane T, Rappaport F, Popot J-L (2013) Amphipol-assisted folding of bacteriorhodopsin in the presence and absence of lipids. Functional consequences. Eur Biophys J 42:85-101
26. Damian M, Martin A, Mesnier D, Pin J-P, Banères J-L (2006) Asymmetric conformational changes in a GPCR dimer controlled by G-proteins. EMBO J 13:5693-5702
27. Damian M, Marie J, Leyris J-P, Fehrentz J-A, Verdié P, Martinez J, Banères J-L, Mary S (2012) High constitutive activity is an intrinsic feature of ghrelin receptor protein: a study with a functional monomeric GHS-R1a receptor reconstituted in lipid discs. J Biol Chem 287:3630-3641
28. Diab C, Tribet C, Gohon Y, Popot J-L, Winnik FM (2007a) Complexation of integral membrane proteins by phosphorylcholine-based amphipols. Biochim Biophys Acta 1768:2737-2747
29. Diab C, Winnik FM, Tribet C (2007b) Enthalpy of interaction and binding isotherms of non-ionic surfactants onto micellar amphiphilic polymers (amphipols). Langmuir 23:3025-3035
30. Elter S, Raschle T, Arens S, Viegas A, Gelev V, Etzkorn M, Wagner G (2014) The use of amphipols for NMR structural characterization of 7-TM proteins. J Membr Biol, in the press
31. 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
32. Feinstein HE, Tifrea D, Popot J-L, de la MLM, Cocco MJ (2014) Amphipols stabilize the Chlamydia major outer membrane protein vaccine formulation J Membr Biol, in the press
33. Fernandez A, Le Bon C, Baumlin N, Giusti F, Crémel G, Popot J-L, Bagnard D (2014) In vivo characterization of the biodistribution profile of amphipols J Membr Biol, in the press
34. Ferrandez Y, Dezi M, Bosco M, Urvoas A, Valério M, Le Bon C, Giusti F, Broutin I, Durand G, Polidori A, Popot J-L, Picard M, Minard P (2014) Amphipol-mediated screening of molecular ortheses specific for membrane protein targets J Membr Biol, in the press
35. Flotenmeyer M, Weiss H, Tribet C, Popot J-L, Leonard K (2007) The use of amphipathic polymers for cryo-electron microscopy of NADH: ubiquinone oxidoreductase (complex I). J Microsc 227:229-235
36. Garavito RM, Ferguson-Miller S (2001) Detergents as tools in membrane biochemistry. J Biol Chem 276:32403-32406
37. Giusti F, Popot J-L, 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
38. Giusti F, Kessler P, Westh Hansen R, Lloret N, Le Bon C, Mourier G, Popot J-L, Martinez KL, Zoonens M (2014a) Synthesis of polyhistidine-bearing amphipols and its use for immobilization of membrane proteins. In submission
39. Giusti F, Rieger J, Catoire L, Qian S, Calabrese AN, Watkinson TG, Casiraghi M, Radford SE, Ashcroft AE, Popot J-L (2014b) Synthesis, characterization and applications of a perdeuterated amphipol. J Membr Biol, DOI 10.1007/s00232-014-9656-x
40. Gohon Y, Pavlov G, Timmins P, Tribet C, Popot J-L, Ebel C (2004) Partial specific volume and solvent interactions of amphipol A8-35. Anal Biochem 334:318-334
41. Gohon Y, Giusti F, Prata C, Charvolin D, Timmins P, Ebel C, Tribet C, Popot J-L (2006) Well-defined nanoparticles formed by hydrophobic assembly of a short and polydisperse random terpolymer, amphipol A8-35. Langmuir 22:1281-1290
42. Gohon Y, Dahmane T, Ruigrok R, Schuck P, Charvolin D, Rappaport F, Timmins P, Engelman DM, Tribet C, Popot J-L, Ebel C (2008) Bacteriorhodopsin/amphipol complexes: structural and functional properties. Biophys J 94:3523-3537
43. Gohon Y, Vindigni J-D, Pallier A, Wien F, Celia H, Giuliani A, Tribet C, Chardot T, Briozzo P (2011) High water solubility and fold in amphipols of proteins with large hydrophobic regions: oleosins and caleosin from seed lipid bodies. Biochim Biophys Acta 1808:706-716
44. Gorzelle BM, Hoffman AK, Keyes MH, Gray DN, Ray DG, Sanders CR II (2002) Amphipols can support the activity of a membrane enzyme. J Am Chem Soc 124:11594-11595
45. Hong W-X, Baker KA, Ma X, Stevens RC, Yeager M, Zhang Q (2011) Design, synthesis and properties of branch-chained maltoside detergents for stabilization and crystallization of integral membrane proteins: human connexin 26. Langmuir 26:8690-8696
46. Hovers J, Potschies M, Polidori A, Pucci B, Raynal S, Bonnete F, Serrano-Vega M, Tate C, Picot D, Pierre Y, Popot J-L, Nehme R, Bidet M, Mus-Veteau I, Bußkamp H, Jung K-H, Marx A, Timmins PA, Welte W (2011) A class of mild surfactants that keep integral membrane proteins water-soluble for functional studies and crystallization. Mol Membr Biol 28:171-181
47. Jonkheijm P, Weinrich D, Schröder H, Niemeyer CM, Waldmann H (2008) Chemical strategies for generating protein biochips. Angew Chem Int Ed Engl 47:9618-9647
48. Karlsson R, Fält A (1997) Experimental design for kinetic analysis of protein-protein interactions with surface plasmon resonance biosensors. J Immunol Method 200:121-133
49. Kigawa T, Yabuki T, Yoshida Y, Tsutsui M, Ito Y, Shibata T, Yokoyama S (1999) Cell-free production and stable-isotope labeling of milligram quantities of proteins. FEBS Lett 442:15-19
50. Knowles TJ, Finka R, Smith C, Lin Y-P, Dafforn T, Overduin M (2009) Membrane proteins solubilized intact in lipid containing nanoparticles bounded by styrene maleic acid copolymer. J Am Chem Soc 131:7484-7485
51. Koutsopoulos S, Kaiser L, Eriksson HM, Zhang S (2012) Designer peptide surfactants stabilize diverse functional membrane proteins. Chem Soc Rev 41:1721-1728
52. Le Bon C, Della Pia EA, Giusti F, Lloret N, Zoonens M, Martinez KL, Popot J-L (2014a) Synthesis of an oligonucleotide-derivatized amphipol and its use to trap and immobilize membrane proteins Nucleic Acids Res, DOI: 10.1093/nar/gku250.
53. Le Bon C, Popot J-L, Giusti F (2014b) Labeling and functionalizing amphipols for biological applications. J Membr Biol, DOI 10.1007/s00232-014-9655-y
54. Leney AC, Mc Morran LM, Radford SE, Ashcroft AE (2012) Amphipathic polymers enable the study of functional membrane proteins in the gas phase. Anal Chem 84:9841-9847
55. Liao M, Cao E, Julius D, Cheng Y (2013) Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504:107-112
56. Long AR, O’Brien CC, Malhotra K, Schwall CT, Albert AD, Watts A, Alder NN (2013) A detergent-free strategy for the reconstitution of active enzyme complexes from native biological membranes into nanoscale discs. BMC Biotechnol 13:41. doi:10.1186/1472-6750-1113-1141
57. Martinez KL, Gohon Y, Corringer P-J, Tribet C, Mérola F, Changeux J-P, Popot J-L (2002) Allosteric transitions of Torpedo acetylcholine receptor in lipids, detergent and amphipols: molecular interactions vs. physical constraints. FEBS Lett 528:251-256
58. Matar-Merheb R, Rhimi M, Leydier A, Huché F, Galiân C, Desuzinges-Mandon E, Ficheux D, Flot D, Aghajari H, Kahn R, Di Pietro A, Jault J-M, Coleman AW, Falson P (2011) Structuring detergents for extracting and stabilizing functional membrane proteins. PLoS ONE 6:e18036
59. Mc Gregor C-L, 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
60. Nagy JK, Kuhn Hoffmann A, Keyes MH, Gray DN, Oxenoid K, Sanders CR (2001) Use of am-phipathic polymers to deliver a membrane protein to lipid bilayers. FEBS Lett 501:115-120
61. Ning Z, Hawley B, Seebun D, Figeys D (2014) APols aided protein precipitation: a rapid method for protein concentrating for proteomic analysis. J Membr Biol, in the press
62. Opacic M, Giusti F, Broos J, Popot J-L (2014) Amphipol A8-35 preserves the activity of detergentsensitive mutants of Escherichia coli mannitol permease ElImtl. J Membr Biol, in the press
63. Park K-H, Billon-Denis E, Dahmane T, Lebaupain F, Pucci B, Breyton C, Zito F (2011) In the cauldron of cell-free synthesis of membrane proteins: playing with new surfactants. New Biotech 28:255-261
64. Perlmutter JD, Drasler WJ, Xie W, Gao J, Popot J-L, Sachs JN (2011) All-atom and coarsegrained molecular dynamics simulations of a membrane protein stabilizing polymer. Langmuir 27:10523-10537
65. Perlmutter JD, Popot J-L, Sachs JN (2014) Molecular dynamics simulations of a membrane pro-tein/amphipol complex. J Membr Biol, in the press
66. 2+-ATPase from sarcoplasmic reticulum: a comparative study. Biochemistry 45:1861-1869
67. Planchard N, Point E, Dahmane T, Giusti F, Renault M, Le Bon C, Durand G, Milon A, Guittet E, Zoonens M, Popot J-L, Catoire LJ (2014) The use of amphipols for solution NMR studies of membrane proteins: advantages and limitations as compared to other solubilizing media. J Membr Biol, DOI 10.1007/s00232-014-9654-z
68. Pocanschi CL, Dahmane T, Gohon Y, Rappaport F, Apell H-J, Kleinschmidt JH, Popot J-L (2006) Amphipathic polymers: tools to fold integral membrane proteins to their active form. Biochemistry 45:13954-13961
69. Pocanschi C, Popot J-L, Kleinschmidt JH (2013) Folding and stability of outer membrane protein A (OmpA) from Escherichia coli in an amphipathic polymer, amphipol A8-35. Eur Biophys J 42:103-118
70. Polovinkin V, Gushchin I, Balandin T, Chervakov P, Round E, Schevchenko V, Popov A, Borshchevskiy V, Popot J-L, Gordeliy V (2014) High-resolution structure of a membrane protein transferred from amphipol to a lipidic mesophase. J Membr Biol, in the press
71. Popot J-L (2010) Amphipols, nanodiscs, and fluorinated surfactants: three non-conventional approaches to studying membrane proteins in aqueous solutions. Annu Rev Biochem 79:737-775
72. Popot J-L, Engelman DM (2000) Helical membrane protein folding, stability and evolution. Annu Rev Biochem 69:881-923
73. Popot J-L, Gerchman S-E, Engelman DM (1987) Refolding of bacteriorhodopsin in lipid bilayers: a thermodynamically controlled two-stage process. J Mol Biol 198:655-676
74. Popot J-L, Berry EA, Charvolin D, Creuzenet C, Ebel C, Engelman DM, Flotenmeyer M, Giusti F, Gohon Y, Hervé P, Hong Q, Lakey JH, Leonard K, Shuman HA, Timmins P, Warschawski DE, Zito F, Zoonens M, Pucci B, Tribet C (2003) Amphipols: polymeric surfactants for membrane biology research. Cell Mol Life Sci 60:1559-1574
75. 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 MLM, Ebel C, Gabel F, Giusti F, Go-hon Y, Goormaghtigh E, Guittet E, Kleinschmidt JH, Kühlbrandt W, Le Bon C, Martinez KL, Picard M, Pucci B, Rappaport F, Sachs JN, Tribet C, van Heijenoort C, Wien F, Zito F, Zoonens M (2011) Amphipols from A to Z. Annu Rev Biophys 40:379-408
76. Prata C, Giusti F, Gohon Y, Pucci B, Popot J-L, Tribet C (2001) Non-ionic amphiphilic polymers derived from trA(hydroxymethyl)-acrylamidomethane keep membrane proteins soluble and native in the absence of detergent. Biopolymers 56:77-84
77. Privé G (2009) Lipopeptide detergents for membrane protein studies. Curr Opin Struct Biol 19:1-7
78. Rahmeh R, Damian M, Cottet M, Orcel H, Mendre C, Durroux T, Sharma KS, Durand G, Pucci B, Trinquet E, Zwier JM, Deupi X, Bron P J-LB, Mouillac B, Granier S (2012) Structural insights into biased G protein-coupled receptor signaling revealed by fluorescence spectroscopy. Proc Natl Acad Sci U S A 109:6733-6738
79. Rajesh S, Knowles TJ, Overduin M (2011) Production of membrane proteins without cells or detergents. N Biotech 28:250-254
80. 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
81. Rich RL, Myszka DG (2005) Survey of the year 2004 commercial optical biosensor literature. J Mol Recognit 18:431-478
82. Schafmeister CE, Miercke LJW, Stroud RA (1993) Structure at 2.5 Â of a designed peptide that maintains solubility of membrane proteins. Science 262:734-738
83. Sharma KS, Durand G, Gabel F, Bazzacco P, Le Bon C, Billon-Denis E, Catoire LJ, Popot J-L, Ebel C, Pucci B (2012) Non-ionic amphiphilic homopolymers: synthesis, solution properties, and biochemical validation. Langmuir 28:4625-4639
84. Stenberg E, Persson B, Roos H, Urbaniczky C (1991) Quantitative determination of surface concentration of protein with surface plasmon resonance using radio-labeled proteins. J Colloid Interface Sci 143:513-526
85. Tifrea D, Pal S, Cocco MJ, Popot J-L, de la Maza LM (2014) Increased immuno accessibility of MOMP epitopes in a vaccine formulated with amphipols may account for the very robust protection elicited against a vaginal challenge with C. muridarum. J Immunol, in the press
86. Tifrea DF, Sun G, Pal S, Zardeneta G, Cocco MJ, Popot J-L, de la MLM (2011) Amphipols stabilize the Chlamydia major outer membrane protein and enhance its protective ability as a vaccine. Vaccine 29:4623-4631
87. Tribet C, Audebert R, Popot J-L (1996) Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc Natl Acad Sci U S A 93:15047-15050
88. Tribet C, Audebert R, Popot J-L (1997) Stabilisation of hydrophobic colloidal dispersions in water with amphiphilic polymers: application to integral membrane proteins. Langmuir 13:5570-5576
89. 6f complexes. Biochimie 80:475-482
90. Tribet C, Diab C, Dahmane T, Zoonens M, Popot J-L, Winnik FM (2009) Thermodynamic characterization of the exchange of detergents and amphipols at the surfaces of integral membrane proteins. Langmuir 25:12623-12634
91. 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 U S A 108:9049-9054
92. 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 U S A 103:17707-17712
93. Zoonens M (2004) Caractérisation des complexes formés entre le domaine transmembranaire de la protéine OmpA et des polymères amphiphiles, les amphipols. Application à l’étude structurale des protéines membranaires par RMN à haute résolution. Thèse de Doctorat, Université Paris-6, Paris
94. Zoonens M, Popot J-L (2014) Amphipols for each season. J Membr Biol, in the press
95. Zoonens M, Catoire LJ, Giusti F, Popot J-L (2005) NMR study of a membrane protein in detergent-free aqueous solution. Proc Natl Acad Sci U S A 102:8893-8898
96. Zoonens M, Giusti F, Zito F, Popot J-L (2007) Dynamics of membrane protein/amphipol association studied by Forster resonance energy transfer. Implications for in vitro studies of amphipol-stabilized membrane proteins. Biochemistry 46:10392-10404
97. Zubay G (1973) In vitro synthesis of protein in microbial systems. Annu Rev Genet 7:267-287