Labeling and Functionalizing Amphipols for Biological Applications

Journal of Membrane Biology

Volumn 247, Issue 9-10, 2014, Pages 797-814

  Le Bon, Christel ^a   Popot, Jean Luc ^a   Giusti, Fabrice ^a  

^a PSL Research University   (France)

Author keywords

A8 35; Amphipathic polymers; Fluorophores; Immobilization; Isotopic labeling; Membrane protein

Indexed keywords

AMINE; AMPHIPOL; FLUORESCENT DYE; IMIDAZOLE; OLIGODEOXYNUCLEOTIDE; POLYACRYLIC ACID; POLYHISTIDINE TAG; POLYMER; THIOL; UNCLASSIFIED DRUG; AMPHIPOL A8-35; LIPID BILAYER; MEMBRANE PROTEIN; PROPYLAMINE; SOLUTION AND SOLUBILITY; SURFACTANT; WATER;

ARTICLE; BIOTINYLATION; CHEMICAL LABELING; CHEMICAL MODIFICATION; FLUORESCENCE; ISOTOPE LABELING; NONHUMAN; SYNTHESIS; ANIMAL; CELL MEMBRANE; CHEMICAL PHENOMENA; CHEMISTRY; HUMAN; LIPID BILAYER; PROCEDURES; SOLUBILITY; SOLUTION AND SOLUBILITY; STAINING;

ANIMALS; CELL MEMBRANE; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; MEMBRANE PROTEINS; POLYMERS; PROPYLAMINES; SOLUBILITY; SOLUTIONS; STAINING AND LABELING; SURFACE-ACTIVE AGENTS; WATER;

EID: 84911003891     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-014-9655-y     Document Type: Article

References (103)

1. Alemdaroglu FE, Herrmann A (2007) DNA meets synthetic polymers—highly versatile hybrid materials. Org Biomol Chem 5:1311–1320
2. 1. EMBO J 30:4652–4664
3. Andreu D, Albericio F, Solé NA, Munson MC, Ferrer M, Barany G (1994) Formation of disulfide bonds in synthetic peptides and proteins. Methods Mol Biol, Springer, pp 91–169
4. Arjona O, Medel R, Rojas J, Costa AM, Vilarrasa J (2003) Chemoselective protection of thiols versus alcohols and phenols. The Tosvinyl group. Tetrahedron Lett 44:6369–6373
5. 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
6. 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
7. 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
8. Bernkop-Schnurch A, Schwarz V, Steininger S (1999) Polymers with thiol groups: a new generation of mucoadhesive polymers? Pharm Res 16:876–881
9. Bette-Bobillo P, Bienvenue A, Broquet C, Maurin L (1985) Synthesis and characterisation of a radioiodinated, photoreactive and physiologically active analog of platelet activating factor. Chem Phys Lipids 37:215–226
10. Blackburn S, Lee GR (1956) The reaction of wool keratin with alkali. Biochim Biophys Acta 19:505–512
11. 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
12. 4 adopts a highly constrained conformation when associated to human BLT2. J Am Chem Soc 132:9049–9057
13. 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 β-barrel of OmpX. Eur Biophys J 39:623–630
14. 2+-ATPase. J Biol Chem 275:18623–18637
15. 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 USA 106:405–410
16. 1 in the presence of amphipols (submitted for publication)
17. Collman JP, Devaraj NK, Chidsey CED (2004) “Clicking” functionality onto electrode surfaces. Langmuir 20:1051–1053
18. 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
19. Dahmane T, Giusti F, Catoire LJ, Popot J-L (2011) Sulfonated amphipols: synthesis, properties and applications. Biopolymers 95:811–823
20. 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
21. Danehy JP, Hunter WE (1967) The alkaline decomposition of organic disulfides. II. Alternative pathways as determined by structure. J Org Chem 32:2047–2053
22. Danehy JP, Kreuz JA (1961) The alkaline decomposition of organic disulfides. I. Some dithiodicarboxylic acids. J Am Chem Soc 83:1109–1113
23. Davis BG, Khumtaveeporn K, Bott RR, Jones JB (1999) Altering the specificity of subtilisin Bacillus lentus through the introduction of positive charge at single amino acid sites. Bioorg Med Chem 7:2303–2311
24. Delair T, Badey B, Charles MH, Laayoun A, Domard A, Pichot C, Mandrand B (1997) Conjugation of nucleic acid probes to 6-aminoglucose-based homo- and copolymers. 2. Application to diagnostics. Polym Adv Technol 8:545–555
25. Della Pia EA, Holm J, Lloret N, Le Bon C, Popot J-L, Zoonens M, Nygård J, Martinez KL (2014a) A step closer to membrane protein multiplexed nano-arrays using biotin-doped polypyrrole. ACS Nano 8:1844–1853
26. Della Pia EA, Westh Hansen R, Zoonens M, Martinez KL (2014b) Amphipols: a versatile toolbox suitable for applications of membrane proteins in synthetic biology (submitted for publication)
27. 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
28. 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
29. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77
30. Etzkorn M, Zoonens M, Catoire LJ, Popot J-L, Hiller S (2014) How amphipols embed membrane proteins: global solvent accessibility and interaction with a flexible protein terminus. J Membrane Biol (in press)
31. Feinstein HE, Tifrea D, Popot J-L, de la Maza LM, Cocco MJ (2014) Amphipols stabilize the Chlamydia major outer membrane protein vaccine formulation (submitted for publication)
32. 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 (submitted for publication)
33. 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 orthoses specific for membrane protein targets (submitted for publication)
34. Ferraton N, Delair T, Laayoun A, Cros P, Mandrand B (1997) Covalent immobilization of nucleic acid probes onto reactive synthetic polymers. J Appl Polym Sci 66:233–242
35. Frey A, Neutra MR, Robey FA (1997) Peptomer aluminum oxide nanoparticle conjugates as systemic and mucosal vaccine candidates: synthesis and characterization of a conjugate derived from the C4 domain of HIV-1(MN) gp120. Bioconjugate Chem 8:424–433
36. Gauvreau V, Chevallier P, Vallières K, Petitclerc E, Gaudreault RC, Laroche G (2004) Engineering surfaces for bioconjugation: developing strategies and quantifying the extent of the reactions. Bioconjugate Chem 15:1146–1156
37. c-haemocyanin of Helix pomatia. Eur J Biochem 248:879–888
38. 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
39. Giusti F, Kessler P, Westh Hansen R, Della Pia EA, Le Bon C, Mourier G, Popot JL, Martinez KL, Zoonens M (2014a) Synthesis of polyhistidine- or imidazole-bearing amphipols and their use for immobilized metal affinity chromatography and surface plasmon resonance studies of membrane proteins (in preparation)
40. Giusti F, Rieger J, Catoire L, Qian S, Calabrese AN, Watkinson TG, Radford SE, Ashcroft AE, Popot J-L (2014b) Synthesis, characterization and applications of a perdeuterated amphipol. J Membrane Biol (in press)
41. 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
42. 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
43. 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
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. Greene TW, Wuts PGM (2002) Protection for the thiol group. Protective groups in organic synthesis. Wiley, Hoboken, pp 454–493
46. Grover GN, Alconcel SNS, Matsumoto NM, Maynard HD (2009) Trapping of thiol-terminated acrylate polymers with divinyl sulfone to generate well-defined semitelechelic Michael acceptor polymers. Macromolecules 42:7657–7663
47. Hansen RE, Winther JR (2009) An introduction to methods for analyzing thiols and disulfides: reactions, reagents, and practical considerations. Anal Biochem 394:147–158
48. Harding RL, Henshaw J, Tilling J, Bugg TDH (2002) Thioester analogues of peptidoglycan fragment MurNAc-l-Ala-gamma-d-Glu as substrates for peptidoglycan hydrolase MurNAc- l-Ala amidase. J Chem Soc Perkin Trans 1:1714–1722
49. Humphrey RE, Potter JL (1965) Reduction of disulfides with tributylphosphine. Anal Chem 37:164–165
50. Huynh KW, Cohen MR, Moiseenkova-Bell VY (2014) Application of amphipols for structure-functional analysis of TRP channels (submitted for publication)
51. Javakhishvili I, Hvilsted S (2009) Gold nanoparticles protected with thiol-derivatized amphiphilic poly(epsilon-caprolactone)-β-poly(acrylic acid). Biomacromolecules 10:74–81
52. Jeong JH, Kim SH, Kim SW, Park TG (2005) Polyelectrolyte complex micelles composed of c-raf antisense oligodeoxynucleotide-poly(ethylene glycol) conjugate and poly(ethylenimine): effect of systemic administration on tumor growth. Bioconjugate Chem 16:1034–1037
53. Kast CE, Bernkop-Schnurch A (2001) Thiolated polymers-thiomers: development and in vitro evaluation of chitosan-thioglycolic acid conjugates. Biomaterials 22:2345–2352
54. Kikuzawa A, Kida T, Akashi M (2007) Synthesis of stimuli-responsive cyclodextrin derivatives and their inclusion ability control by ring opening and closing reactions. Org Lett 9:3909–3912
55. Klammt C, Perrin M-H, Maslennikov I, Renault L, Krupa M, Kwiatkowski W, Stahlberg H, Vale W, Choe S (2011) Polymer-based cell-free expression of ligand-binding family B G-protein coupled receptors without detergents. Prot Sci 20:1030–1041
56. 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
57. Krieg AM (2006) Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 5:471–484
58. Krieg AM, Yi AK, Matson S, Waldschmidt TJ, Bishop GA, Teasdale R, Koretzky GA, Klinman DM (1995) CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374:546–549
59. Le Bon C, Della Pia EA, Giusti F, Lloret N, Zoonens M, Martinez KL, Popot J-L (2014) Synthesis of an oligonucleotide-derivatized amphipol and its use to trap and immobilize membrane proteins. Nucleic Acids Res (accepted for publication)
60. 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:10.1186/1472-6750-13-41
61. 13C NMR. Polymer 33:3151–3154
62. 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
63. Morishima Y, Nomura S, Ikeda T, Seki M, Kamachi M (1995) Characterization of unimolecular micelles of random copolymers of sodium 2-(acrylamido)-2-methylpropanesulfonate and methacrylamides bearing bulky hydrophobic substituents. Macromolecules 28:2874–2881
64. Murphy WL, Mercurius KO, Koide S, Mrksich M (2004) Substrates for cell adhesion prepared via active site-directed immobilization of a protein domain. Langmuir 20:1026–1030
65. Nagy JK, Kuhn Hoffmann A, Keyes MH, Gray DN, Oxenoid K, Sanders CR (2001) Use of amphipathic polymers to deliver a membrane protein to lipid bilayers. FEBS Lett 501:115–120
66. Nicolet BH (1931) The mechanism of sulfur lability in cysteine and its derivatives. I. Some thio ethers readily split by alkali. J Am Chem Soc 53:3066–3072
67. Oishi M, Hayama T, Akiyama Y, Takae S, Harada A, Yarnasaki Y, Nagatsugi F, Sasaki S, Nagasaki Y, Kataoka K (2005) Supramolecular assemblies for the cytoplasmic delivery of antisense oligodeoxynucleotide: polylon complex (PIC) micelles based on poly(ethylene glycol)-SS-oligodeoxynucleotide conjugate. Biomacromolecules 6:2449–2454
68. Opačić M, Popot J-L, Durand G, Bosco M, Polidori A, Croce R (2014) Amphipols and photosynthetic light-harvesting pigment-protein complexes (submitted for publication)
69. Perlmutter JD, Drasler WJ, Xie W, Gao J, Popot J-L, Sachs JN (2011) All-atom and coarse-grained molecular dynamics simulations of a membrane protein stabilizing polymer. Langmuir 27:10523–10537
70. Perlmutter JD, Popot J-L, Sachs JN (2014) Molecular dynamics simulations of a membrane protein/amphipol complex (submitted for publication)
71. 2+-ATPase from sarcoplasmic reticulum: a comparative study. Biochemistry 45:1861–1869
72. 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 (submitted for publication)
73. 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
74. Popot J-L, Berry EA, Charvolin D, Creuzenet C, Ebel C, Engelman DM, Flötenmeyer 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 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, 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 tris(hydroxymethyl)-acrylamidomethane keep membrane proteins soluble and native in the absence of detergent. Biopolymers 56:77–84
77. Rajesh S, Knowles TJ, Overduin M (2011) Production of membrane proteins without cells or detergents. New Biotech 28:250–254
78. Ringsdorf H, Venzmer J, Winnik FM (1991) Fluorescence studies of hydrophobically modified poly(N-isopropylacrylamides). Macromolecules 24:1678–1686
79. Roberts C, Chen C, Mrksich M, Martichonok V, Ingber DE, Whitesides GM (1998) Using mixed self-assembled monolayers presenting RGD and (EG)(3)OH groups to characterize long-term attachment of bovine capillary endothelial cells to surfaces. J Am Chem Soc 120:6548–6555
80. Roth PJ, Jochum FD, Zentel R, Theato P (2010) Synthesis of hetero-telechelic alpha, omega bio-functionalized polymers. Biomacromolecules 11:238–244
81. Sanders CR, Hoffmann AK, Gray DN, Keyes MH, Ellis CD (2004) French swimwear for membrane proteins. ChemBioChem 5:423–426
82. Sauer AM, Schlossbauer A, Ruthardt N, Cauda V, Bein T, Brauchle C (2010) Role of endosomal escape for disulfide-based drug delivery from colloidal mesoporous silica evaluated by live-cell imaging. Nano Lett 10:3684–3691
83. Sharma KS, Durand G, Giusti F, Olivier B, Fabiano A-S, Bazzacco P, Dahmane T, Ebel C, Popot J-L, Pucci B (2008) Glucose-based amphiphilic telomers designed to keep membrane proteins soluble in aqueous solutions: synthesis and physicochemical characterization. Langmuir 24:13581–13590
84. 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
85. Stefano JE, Hou LH, Honey D, Kyazike J, Park A, Zhou Q, Pan CQ, Edmunds T (2009) In vitro and in vivo evaluation of a non-carbohydrate targeting platform for lysosomal proteins. J Controlled Release 135:113–118
86. Takei YG, Aoki T, Sanui K, Ogata N, Okano T, Sakurai Y (1993) Temperature-responsive bioconjugates. 1. Synthesis of temperature-responsive oligomers with react-ive end groups and their coupling to biomolecules. Bioconjugate Chem 4:42–46
87. Tehei M, Giusti F, Popot J-L, Zaccai G (2014) Thermal fluctuations in amphipol A8-35 measured by neutron scattering. (submitted for publication)
88. Terrettaz S, Ulrich WP, Vogel H, Hong Q, Dover LG, Lakey JH (2002) Stable self-assembly of a protein engineering scaffold on gold surfaces. Protein Sci 11:1917–1925
89. Tifrea DF, Sun G, Pal S, Zardeneta G, Cocco MJ, Popot J-L, 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
90. 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. (submitted for publication)
91. Tribet C, Audebert R, Popot J-L (1996) Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc Natl Acad Sci USA 93:15047–15050
92. Tribet C, Audebert R, Popot J-L (1997) Stabilization of hydrophobic colloidal dispersions in water with amphiphilic polymers: application to integral membrane proteins. Langmuir 13:5570–5576
93. 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
94. Vial F, Rabhi S, Tribet C (2005) Association of octyl-modified poly(acrylic acid) onto unilamellar vesicles of lipids and kinetics of vesicle disruption. Langmuir 21:853–862
95. Wang TK, Iliopoulos I, Audebert R (1988) Viscometric behavior of hydrophobically modified poly(sodium acrylate). Polymer Bull20:577–582
96. Warnecke A, Kratz F (2003) Maleimide-oligo(ethylene glycol) derivatives of camptothecin as albumin-binding prodrugs: synthesis and antitumor efficacy. Bioconjugate Chem 14:377–387
97. Woghiren C, Sharma B, Stein S (1993) Protected thiol polyethylene-glycol. A new activated polymer for reversible protein modification. Bioconjugate Chem 4:314–318
98. Yoshimoto K, Hirase T, Nemoto S, Hatta T, Nagasaki Y (2008) Facile construction of sulfanyl-terminated poly(ethylene glycol)-brushed layer on a gold surface for protein immobilization by the combined use of sulfanyl-ended telechelic and semitelechelic poly(ethylene glycol)s. Langmuir 24:9623–9629
99. Zoonens M, Popot J-L (2014) Amphipols for each season. (submitted for publication)
100. 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 USA 102:8893–8898
101. Zoonens M, Giusti F, Zito F, 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 46:10392–10404
102. Zoonens M, Zito F, Martinez KL, Popot J-L (2014) Amphipols: a general introduction and some protocols, In: Membrane protein production for structural analysis (I Mus-Veteau, ed.), Springer (in press)
103. Zugates GT, Anderson DG, Little SR, Lawhorn IEB, Langer R (2006) Synthesis of poly(beta-amino ester)s with thiol-reactive side chains for DNA delivery. J Am Chem Soc 128:12726–12734