Advertisement

The Journal of Membrane Biology

, Volume 247, Issue 9–10, pp 797–814 | Cite as

Labeling and Functionalizing Amphipols for Biological Applications

  • Christel Le Bon
  • Jean-Luc Popot
  • Fabrice GiustiEmail author
Article

Abstract

Amphipols (APols) are short amphipathic polymers developed as an alternative to detergents for handling membrane proteins (MPs) in aqueous solution. MPs are, as a rule, much more stable following trapping with APols than they are in detergent solutions. The best-characterized APol to date, called A8-35, is a mixture of short-chain sodium polyacrylates randomly derivatized with octylamine and isopropylamine. Its solution properties have been studied in detail, and it has been used extensively for biochemical and biophysical studies of MPs. One of the attractive characteristics of APols is that it is relatively easy to label them, isotopically or otherwise, without affecting their physical-chemical properties. Furthermore, several variously modified APols can be mixed, achieving multiple functionalization of MP/APol complexes in the easiest possible manner. Labeled or tagged APols are being used to study the solution properties of APols, their miscibility, their biodistribution upon injection into living organisms, their association with MPs and the composition, structure and dynamics of MP/APol complexes, examining the exchange of surfactants at the surface of MPs, labeling MPs to follow their distribution in fractionation experiments or to immobilize them, increasing the contrast between APols and solvent or MPs in biophysical experiments, improving NMR spectra, etc. Labeling or functionalization of APols can take various courses, each of which has its specific constraints and advantages regarding both synthesis and purification. The present review offers an overview of the various derivatives of A8-35 and its congeners that have been developed in our laboratory and discusses the pros and cons of various synthetic routes.

Keywords

Membrane protein A8-35 Amphipathic polymers Fluorophores Immobilization Isotopic labeling 

Abbreviations

A8-35

Poly(sodium acrylate) based amphipol comprising 35 % of free carboxylate, 25 % of octyl chains, 40 % of isopropyl groups, and whose number-average molar mass is ~4.3 kDa

A8-75

Poly(sodium acrylate) based amphipol comprising 75 % of free carboxylate, 25 % of octylchains, and whose number-average molar mass is ~4 kDa

APol

Amphipol

AUC

Analytical ultracentrifugation

BAPol

Biotinylated A8-35

Ð

Molar mass dispersity

DAPol

A8-35 with deuterated octylamine and isopropylamine side chains

DCI

N,N′-dicyclohexylcarbodiimide

DCU

Dicyclohexylurea

DTT

Dithiothreitol

EDC

Ethyl-3-[3-dimethylaminopropyl]carbodiimide hydrochloride

FAPol

Fluorescently labeled A8-35

FAPolAF647

Alexa Fluor 647-labeled A8-35

FAPolNBD

Nitrobenzoxadiazole-labeled A8-35

FAPolrhod

Rhodamine-labeled A8-35

FRET

Förster resonance energy transfer

HAPol

Hydrogenated A8-35

HMPA

Hydrophobically modified poly(acrylic acid)

HMPAS

HMPA synthesis

His6PEG

N-(penta(histidyl)histidinamide)-8-amino-3,6-dioxa-octanamide

His-tag

Hexahistidine tag

HistAPol

Hexahistidine tag-carrying A8-35

HOBt

1-N-hydroxybenzotriazole

IMAC

Immobilized metal ion affinity chromatography

ImidAPol

Imidazole-carrying A8-35

INS

Inelastic neutron scattering

Mn

Number-average molar mass

MP

Membrane protein

NBD

7-Nitrobenz-2-oxa-1,3-diazol-4-yl

NHS

N-hydroxysuccinimide

NOE

Nuclear Overhauser effect

NTA

Nitrilotriacetic acid

ODN

Oligodeoxynucleotide

OligAPol

ODN-carrying A8-35

PAA

Poly(acrylic acid)

perDAPol

Perdeuterated A8-35

SANS

Small angle neutron scattering

SAPol

Sulfonated amphipol derived from A8-75, comprising 40 % of taurine moieties

SPR

Surface plasmon resonance

TES

Triethylsilane

TFA

Trifluoroacetic acid

ThiAPol

Thiol-carrying APol

Tsv

Tosvinyl group

UAPol

Universal amphipol

UAPol-NH2

Amine-carrying A8-35

Notes

Acknowledgments

This work was supported by the Center National de la Recherche Scientifique, by Université Paris-7 Denis Diderot, and by U.S. National grant R01AI092129 from the National Institute of Allergy and Infectious Diseases, French Agence Nationale pour la Recherche grant ‘X-Or,’ ANR SVSE5 2010-BLAN-1535, and grant ‘DYNAMO,’ ANR-11-LABX-0011-01 from the French ‘Initiative d’Excellence’ program. CLB has been the beneficiary of funding by the Fondation pour la Recherche Médicale, the Agence Nationale de la Recherche Scientifique (ANR-07-BLAN-0092 ‘Refolding GPCRs’ and SVSE5 2010-BLAN-1535 ‘X-Or’) and the Direction Innovation et Relations avec les Entreprises of the CNRS.

References

  1. Alemdaroglu FE, Herrmann A (2007) DNA meets synthetic polymers—highly versatile hybrid materials. Org Biomol Chem 5:1311–1320PubMedGoogle Scholar
  2. Althoff T, Mills DJ, Popot J-L, Kühlbrandt W (2011) Assembly of electron transport chain components in bovine mitochondrial supercomplex I1III2IV1. EMBO J 30:4652–4664PubMedPubMedCentralGoogle Scholar
  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 91–169Google Scholar
  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 44:6369–6373Google Scholar
  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 48:6037–6039Google Scholar
  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 10:3317–3326PubMedGoogle Scholar
  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 51:1416–1430CrossRefGoogle Scholar
  8. Bernkop-Schnurch A, Schwarz V, Steininger S (1999) Polymers with thiol groups: a new generation of mucoadhesive polymers? Pharm Res 16:876–881PubMedGoogle Scholar
  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 37:215–226PubMedGoogle Scholar
  10. Blackburn S, Lee GR (1956) The reaction of wool keratin with alkali. Biochim Biophys Acta 19:505–512PubMedGoogle Scholar
  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 197:91–95Google Scholar
  12. Catoire LJ, Damian M, Giusti F, Martin A, van Heijenoort C, Popot J-L, Guittet E, Banères J-L (2010a) Structure of a GPCR ligand in its receptor-bound state: leukotriene B4 adopts a highly constrained conformation when associated to human BLT2. J Am Chem Soc 132:9049–9057PubMedGoogle Scholar
  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 39:623–630PubMedGoogle Scholar
  14. Champeil P, Menguy T, Tribet C, Popot J-L, le Maire M (2000) Interaction of amphipols with the sarcoplasmic reticulum Ca2+-ATPase. J Biol Chem 275:18623–18637CrossRefGoogle Scholar
  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 106:405–410CrossRefGoogle Scholar
  16. Charvolin D, Picard M, Huang L-S, Berry EA, Popot J-L (2014) Solution behavior and crystallization of cytochrome bc 1 in the presence of amphipols (submitted for publication) Google Scholar
  17. Collman JP, Devaraj NK, Chidsey CED (2004) “Clicking” functionality onto electrode surfaces. Langmuir 20:1051–1053PubMedPubMedCentralGoogle Scholar
  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 48:6516–6521PubMedGoogle Scholar
  19. Dahmane T, Giusti F, Catoire LJ, Popot J-L (2011) Sulfonated amphipols: synthesis, properties and applications. Biopolymers 95:811–823PubMedGoogle Scholar
  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 42:85–101PubMedGoogle Scholar
  21. Danehy JP, Hunter WE (1967) The alkaline decomposition of organic disulfides. II. Alternative pathways as determined by structure. J Org Chem 32:2047–2053Google Scholar
  22. Danehy JP, Kreuz JA (1961) The alkaline decomposition of organic disulfides. I. Some dithiodicarboxylic acids. J Am Chem Soc 83:1109–1113Google Scholar
  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 7:2303–2311PubMedGoogle Scholar
  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 8:545–555Google Scholar
  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 8:1844–1853PubMedPubMedCentralGoogle Scholar
  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)Google Scholar
  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 1768:2737–2747PubMedGoogle Scholar
  28. Diab C, Winnik FM, Tribet C (2007b) Enthalpy of interaction and binding isotherms of non-ionic surfactants onto micellar amphiphilic polymers (amphipols). Langmuir 23:3025–3035PubMedGoogle Scholar
  29. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77PubMedGoogle Scholar
  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)Google Scholar
  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)Google Scholar
  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)Google Scholar
  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)PubMedGoogle Scholar
  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 66:233–242Google Scholar
  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 8:424–433Google Scholar
  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 15:1146–1156Google Scholar
  37. Gielens C, De Geest N, Xin X-Q, Devreese B, Van Beeumen J, Préaux JG (1997) Evidence for a cysteine-histidine thioether bridge in functional units of molluscan haemocyanins and location of the disulfide bridges in functional units d and g of the β c-haemocyanin of Helix pomatia. Eur J Biochem 248:879–888PubMedGoogle Scholar
  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 28:10372–10380PubMedGoogle Scholar
  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)Google Scholar
  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)Google Scholar
  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 334:318–334PubMedGoogle Scholar
  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 22:1281–1290PubMedGoogle Scholar
  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 94:3523–3537PubMedPubMedCentralGoogle Scholar
  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 124:11594–11595PubMedGoogle Scholar
  45. Greene TW, Wuts PGM (2002) Protection for the thiol group. Protective groups in organic synthesis. Wiley, Hoboken, pp 454–493Google Scholar
  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 42:7657–7663PubMedPubMedCentralGoogle Scholar
  47. Hansen RE, Winther JR (2009) An introduction to methods for analyzing thiols and disulfides: reactions, reagents, and practical considerations. Anal Biochem 394:147–158PubMedGoogle Scholar
  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 1:1714–1722Google Scholar
  49. Humphrey RE, Potter JL (1965) Reduction of disulfides with tributylphosphine. Anal Chem 37:164–165Google Scholar
  50. Huynh KW, Cohen MR, Moiseenkova-Bell VY (2014) Application of amphipols for structure-functional analysis of TRP channels (submitted for publication)PubMedPubMedCentralGoogle Scholar
  51. Javakhishvili I, Hvilsted S (2009) Gold nanoparticles protected with thiol-derivatized amphiphilic poly(epsilon-caprolactone)-β-poly(acrylic acid). Biomacromolecules 10:74–81PubMedGoogle Scholar
  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 16:1034–1037Google Scholar
  53. Kast CE, Bernkop-Schnurch A (2001) Thiolated polymers-thiomers: development and in vitro evaluation of chitosan-thioglycolic acid conjugates. Biomaterials 22:2345–2352PubMedGoogle Scholar
  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 9:3909–3912PubMedGoogle Scholar
  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 20:1030–1041Google Scholar
  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 131:7484–7485PubMedGoogle Scholar
  57. Krieg AM (2006) Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 5:471–484PubMedGoogle Scholar
  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 374:546–549PubMedGoogle Scholar
  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)Google Scholar
  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 PubMedPubMedCentralGoogle Scholar
  61. Magny B, Lafuma F, Iliopoulos I (1992) Determination of microstructure of hydrophobically modified water-soluble polymers by 13C NMR. Polymer 33:3151–3154Google Scholar
  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 528:251–256PubMedGoogle Scholar
  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 28:2874–2881Google Scholar
  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 20:1026–1030PubMedGoogle Scholar
  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 501:115–120PubMedGoogle Scholar
  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 53:3066–3072Google Scholar
  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 6:2449–2454PubMedGoogle Scholar
  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)PubMedGoogle Scholar
  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 27:10523–10537PubMedPubMedCentralGoogle Scholar
  70. Perlmutter JD, Popot J-L, Sachs JN (2014) Molecular dynamics simulations of a membrane protein/amphipol complex (submitted for publication)Google Scholar
  71. Picard M, Dahmane T, Garrigos M, Gauron C, Giusti F, le Maire M, Popot J-L, Champeil P (2006) Protective and inhibitory effects of various types of amphipols on the Ca2+-ATPase from sarcoplasmic reticulum: a comparative study. Biochemistry 45:1861–1869PubMedGoogle Scholar
  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)Google Scholar
  73. Popot J-L (2010) Amphipols, nanodiscs, and fluorinated surfactants: three non-conventional approaches to studying membrane proteins in aqueous solutions. Annu Rev Biochem 79:737–775PubMedGoogle Scholar
  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 60:1559–1574PubMedGoogle Scholar
  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 40:379–408PubMedGoogle Scholar
  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 56:77–84Google Scholar
  77. Rajesh S, Knowles TJ, Overduin M (2011) Production of membrane proteins without cells or detergents. New Biotech 28:250–254Google Scholar
  78. Ringsdorf H, Venzmer J, Winnik FM (1991) Fluorescence studies of hydrophobically modified poly(N-isopropylacrylamides). Macromolecules 24:1678–1686Google Scholar
  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 120:6548–6555Google Scholar
  80. Roth PJ, Jochum FD, Zentel R, Theato P (2010) Synthesis of hetero-telechelic alpha, omega bio-functionalized polymers. Biomacromolecules 11:238–244PubMedGoogle Scholar
  81. Sanders CR, Hoffmann AK, Gray DN, Keyes MH, Ellis CD (2004) French swimwear for membrane proteins. ChemBioChem 5:423–426PubMedGoogle Scholar
  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 10:3684–3691PubMedGoogle Scholar
  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 24:13581–13590PubMedGoogle Scholar
  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 28:4625–4639PubMedGoogle Scholar
  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 135:113–118Google Scholar
  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 4:42–46Google Scholar
  87. Tehei M, Giusti F, Popot J-L, Zaccai G (2014) Thermal fluctuations in amphipol A8-35 measured by neutron scattering. (submitted for publication)Google Scholar
  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 11:1917–1925PubMedPubMedCentralGoogle Scholar
  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 29:4623–4631PubMedPubMedCentralGoogle Scholar
  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)Google Scholar
  91. Tribet C, Audebert R, Popot J-L (1996) Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc Natl Acad Sci USA 93:15047–15050PubMedGoogle Scholar
  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 13:5570–5576Google Scholar
  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 25:12623–12634PubMedGoogle Scholar
  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 21:853–862PubMedGoogle Scholar
  95. Wang TK, Iliopoulos I, Audebert R (1988) Viscometric behavior of hydrophobically modified poly(sodium acrylate). Polymer Bull20:577–582Google Scholar
  96. Warnecke A, Kratz F (2003) Maleimide-oligo(ethylene glycol) derivatives of camptothecin as albumin-binding prodrugs: synthesis and antitumor efficacy. Bioconjugate Chem 14:377–387Google Scholar
  97. Woghiren C, Sharma B, Stein S (1993) Protected thiol polyethylene-glycol. A new activated polymer for reversible protein modification. Bioconjugate Chem 4:314–318Google Scholar
  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 24:9623–9629PubMedGoogle Scholar
  99. Zoonens M, Popot J-L (2014) Amphipols for each season. (submitted for publication)PubMedPubMedCentralGoogle Scholar
  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 102:8893–8898PubMedGoogle Scholar
  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 46:10392–10404PubMedGoogle Scholar
  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) Google Scholar
  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 128:12726–12734PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Christel Le Bon
    • 1
  • Jean-Luc Popot
    • 1
  • Fabrice Giusti
    • 1
    Email author
  1. 1.Laboratoire de Biologie Physico-Chimique des Protéines Membranaires, UMR 7099, Institut de Biologie Physico-Chimique (FRC 550)CNRS/Université Paris 7ParisFrance

Personalised recommendations