Fluorinated amphiphiles control the insertion of α-hemolysin pores into lipid bilayers

Biochemistry

Volumn 50, Issue 10, 2011, Pages 1599-1606

  Raychaudhuri, Pinky ^a   Li, Qiuhong ^a,b   Mason, Amy ^a,c   Mikhailova, Ellina ^a   Heron, Andrew J ^a   Bayley, Hagan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BI-LAYER; CRITICAL MICELLE CONCENTRATION (CMC); ELECTRICAL RECORDING; HEAD GROUPS; ION CHANNEL; MEMBRANE PROTEINS; POTASSIUM CHANNELS; RAPID SCREENING; SENSOR DEVICE;

BIOLOGICAL MEMBRANES; BLOOD; CRITICAL MICELLE CONCENTRATION; LIPID BILAYERS; MICELLES; NANOPORES; OLIGOMERS; PROTEINS; SENSORS; SOAPS (DETERGENTS);

AMPHIPHILES;

ALPHA HEMOLYSIN; AMPHOLYTE; AMPHOPHILE; BETA CYCLODEXTRIN; FLUORINATED AMPHOPHILE; POTASSIUM CHANNEL; POTASSIUM CHANNEL KCV; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL SPORE; BILAYER MEMBRANE; CONTROLLED STUDY; CRITICAL MICELLE CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN TRANSPORT; STAPHYLOCOCCUS AUREUS;

BACTERIAL TOXINS; BETA-CYCLODEXTRINS; CELL MEMBRANE; HEMOLYSIN PROTEINS; LIPID BILAYERS; MOLECULAR STRUCTURE; POROSITY; PROTEIN STABILITY; STAPHYLOCOCCUS AUREUS; SURFACE-ACTIVE AGENTS;

EID: 79952367443     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1012386     Document Type: Article

References (47)

1. Chabaud, E., Barthelemy, P., Mora, N., Popot, J. L., and Pucci, B. (1998) Stabilization of integral membrane proteins in aqueous solution using fluorinated surfactants Biochimie 80, 515-530 (Pubitemid 28425398)
2. Palchevskyy, S. S., Posokhov, Y. O., Olivier, B., Popot, J. L., Pucci, B., and Ladokhin, A. S. (2006) Chaperoning of insertion of membrane proteins into lipid bilayers by hemifluorinated surfactants: Application to diphtheria toxin Biochemistry 45, 2629-2635
3. Rodnin, M. V., Posokhov, Y. O., Contino-Pépin, C., Brettmann, J., Kyrychenko, A., Palchevskyy, S. S., Pucci, B., and Ladokhin, A. S. (2008) Interactions of fluorinated surfactants with diphtheria toxin T-domain: Testing new media for studies of membrane proteins Biophys. J. 94, 4348-4357
4. Park, K. H., Berrier, C., Lebaupain, F., Pucci, B., Popot, J. L., Ghazi, A., and Zito, F. (2007) Fluorinated and hemifluorinated surfactants as alternatives to detergents for membrane protein cell-free synthesis Biochem. J. 403, 183-187 (Pubitemid 46569880)
5. Breyton, C., Chabaud, E., Chaudier, Y., Pucci, B., and Popot, J.-L. (2004) Hemifluorinated surfactants: A non-dissociating environment for handling membrane proteins in aqueous solutions? FEBS Lett. 564, 312-318 (Pubitemid 38520939)
6. Talbot, J. C., Dautant, A., Polidori, A., Pucci, B., Cohen-Bouhacina, T., Maali, A., Salin, B., Brethes, D., Velours, J., and Giraud, M. F. (2009) Hydrogenated and fluorinated surfactants derived from Tris(hydroxymethyl)- acrylamidomethane allow the purification of a highly active yeast F1-F0 ATP-synthase with an enhanced stability J. Bioenerg. Biomembr. 41, 349-360
7. Song, L., Hobaugh, M. R., Shustak, C., Cheley, S., Bayley, H., and Gouaux, J. E. (1996) Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore Science 274, 1859-1865
8. Bayley, H. and Cremer, P. S. (2001) Stochastic sensors inspired by biology Nature 413, 226-230 (Pubitemid 32867888)
9. Branton, D., Deamer, D. W., Marziali, A., Bayley, H., Benner, S. A., Butler, T., Di Ventra, M., Garaj, S., Hibbs, A., Huang, X., Jovanovich, S. B., Krstic, P. S., Lindsay, S., Ling, X. S., Mastrangelo, C. H., Meller, A., Oliver, J. S., Pershin, Y. V., Ramsey, J. M., Riehn, R., Soni, G. V., Tabard-Cossa, V., Wanunu, M., Wiggin, M., and Schloss, J. A. (2008) The potential and challenges of nanopore sequencing Nat. Biotechnol. 26, 1146-1153
10. Holden, M. A., Needham, D., and Bayley, H. (2007) Functional bionetworks from nanoliter water droplets J. Am. Chem. Soc. 129, 8650-8655 (Pubitemid 47066529)
11. Maglia, G., Heron, A. J., Hwang, W. L., Holden, M. A., Mikhailova, E., Li, Q., Cheley, S., and Bayley, H. (2009) Droplet networks with incorporated protein diodes show collective properties Nat. Nanotechnol. 4, 437-440
12. Faller, M., Niederweis, M., and Schulz, G. E. (2004) The structure of a mycobacterial outer-membrane channel Science 303, 1189-1192 (Pubitemid 38233583)
13. Plugge, B., Gazzarrini, S., Nelson, M., Cerana, R., Van Etten, J. L., Derst, C., DiFrancesco, D., Moroni, A., and Thiel, G. (2000) A potassium channel protein encoded by chlorella virus PBCV-1 Science 287, 1641-1644 (Pubitemid 30127763)
14. + channel Biochemistry 46, 1079-1090 (Pubitemid 46184995)
15. Maglia, M., Henricus, M., Wyss, R., Li, Q., Cheley, S., and Bayley, H. (2009) DNA strands from denatured duplexes are translocated through engineered protein nanopores at alkaline pH Nano Lett. 9, 3831-3836
16. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein Protein Sci. 4, 2411-2423
17. Heron, A. J., Thompson, J. R., Mason, A. E., and Wallace, M. I. (2007) Direct detection of membrane channels from gels using water-in-oil droplet bilayers J. Am. Chem. Soc. 129, 16042-16047
18. Mason, A. E. (2008) Single-channel characterisation of potassium channels with high temperature studies. Ph.D. Thesis, University of Oxford, Oxford, U.K.
19. Niven, R. W. and Schreier, H. (1990) Nebulization of liposomes. I. Effects of lipid composition Pharm. Res. 7, 1127-1133
20. Mercadal, M., Domingo, J. C., Bermudez, M., Mora, M., and De Madariaga, M. A. (1995) N-Palmitoylphosphatidylethanolamine stabilizes liposomes in the presence of human serum: Effect of lipidic composition and system characterization Biochim. Biophys. Acta 1235, 281-288
21. Montal, M. and Mueller, P. (1972) Formation of bimolecular membranes from lipid monolayers and study of their electrical properties Proc. Natl. Acad. Sci. U.S.A. 69, 3561-3566
22. Bhakdi, S., Bayley, H., Valeva, A., Walev, I., Walker, B., Weller, U., Kehoe, M., and Palmer, M. (1996) Staphylococcal α-toxin, streptolysin-O, and Escherichia coli hemolysin: Prototypes of pore-forming bacterial cytolysins Arch. Microbiol. 165, 73-79 (Pubitemid 26081834)
23. Weinstein, J. N., Yoshikami, S., Henkart, P., Blumenthal, R., and Hagins, W. A. (1977) Liposome-cell interaction: Transfer and intracellular release of a trapped fluorescent marker Science 195, 489-492
24. Chen, R. F. and Knutson, J. R. (1988) Mechanism of fluorescence concentration quenching of carboxyfluorescein in liposomes: Energy transfer to nonfluorescent dimers Anal. Biochem. 172, 61-77
25. Bayley, H. (2009) Membrane-protein structure: Piercing insights Nature 459, 651-652
26. Braha, O., Walker, B., Cheley, S., Kasianowicz, J. J., Song, L., Gouaux, J. E., and Bayley, H. (1997) Designed protein pores as components for biosensors Chem. Biol. 4, 497-505 (Pubitemid 27335764)
27. Guo, W., Brown, T. A., and Fung, B. M. (1991) Micelles and aggregates of fluorinated surfactants J. Phys. Chem. 95, 1829-1836
28. Krafft, M. P., Giulieri, F., and Riess, J. G. (1993) Can single-chain perfluoroalkylated amphiphiles alone form vesicles and other organized supramolecular systems? Angew. Chem., Int. Ed. 32, 741-743
29. Riess, J. G. (1994) Fluorinated vesicles J. Drug Targeting 2, 455-468
30. Giulieri, F., Krafft, M. P., and Riess, J. G. (1994) Stable, flexible fibers and rigid tubules made from single-chain perfluoroalkylated amphiphiles Angew. Chem., Int. Ed. 33, 1514-1515 (Pubitemid 24986793)
31. Giulieri, F. and Krafft, M. P. (1996) Self-organization of single-chain fluorinated amphiphiles with fluorinated alcohols Thin Solid Films 284-285, 195-199 (Pubitemid 126387346)
32. Hoffmann, H. and Würtz, J. (1997) Unusual phenomena in perfluorosurfactants J. Mol. Liq. 72, 191-230 (Pubitemid 127375790)
33. Giulieri, F. and Krafft, M. P. (2003) Tubular microstructures made from nonchiral single-chain fluorinated amphiphiles: Impact of the structure of the hydrophobic chain on the rolling-up of bilayer membrane J. Colloid Interface Sci. 258, 335-344 (Pubitemid 36293365)
34. Lu, R. C., Cao, A. N., Lai, L. H., and Xiao, J. X. (2008) Protein-surfactant interaction: Differences between fluorinated and hydrogenated surfactants Colloids Surf., B 64, 98-103
35. Breyton, C., Gabel, F., Abla, M., Pierre, Y., Lebaupain, F., Durand, G., Popot, J. L., Ebel, C., and 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
36. Benz, R., Schmid, A., Nakae, T., and Vos-Scheperkeuter, G. H. (1986) Pore formation by LamB of Escherichia coli in lipid bilayer membranes J. Bacteriol. 165, 978-986 (Pubitemid 16071434)
37. Slatin, S. L., Qiu, X.-Q., Jakes, K. S., and Finkelstein, A. (1994) Identification of a translocated protein segment in a voltage-dependent channel Nature 371, 158-161 (Pubitemid 24284014)
38. Bayley, H., Cronin, B., Heron, A., Holden, M. A., Hwang, W., Syeda, R., Thompson, J., and Wallace, M. (2008) Droplet interface bilayers Mol. BioSyst. 4, 1191-1208
39. Walker, B., Braha, O., Cheley, S., and Bayley, H. (1995) An intermediate in the assembly of a pore-forming protein trapped with a genetically-engineered switch Chem. Biol. 2, 99-105
40. Valeva, A., Hellmann, N., Walev, I., Strand, D., Plate, M., Boukhallouk, F., Brack, A., Hanada, K., Decker, H., and Bhakdi, S. (2006) Evidence that clustered phosphocholine head groups serve as sites for binding and assembly of an oligomeric protein pore J. Biol. Chem. 281, 26014-26021 (Pubitemid 44401807)
41. Wilke, G. A. and Bubeck Wardenburg, J. (2010) Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus α-hemolysin-mediated cellular injury Proc. Natl. Acad. Sci. U.S.A. 107, 13473-13478
42. Li, L., Xu, Z. S., and Song, W. W. (2009) Study on the Langmuir aggregation of fluorinated surfactants on protein J. Fluorine Chem. 130, 225-230
43. Li, L., Wang, Y., Song, G., Wu, S., Chu, P. K., and Xu, Z. S. (2009) Binding strength of fluorinated and hydrogenated surfactant to bovine serum albumin J. Fluorine Chem. 130, 870-877
44. Posokhov, Y. O., Rodnin, M. V., Das, S. K., Pucci, B., and Ladokhin, A. S. (2008) FCS study of the thermodynamics of membrane protein insertion into the lipid bilayer chaperoned by fluorinated surfactants Biophys. J. 95, L54-L56
45. Sanderson, K. (2008) Personal genomes: Standard and pores Nature 456, 23-28
46. Gu, L.-Q. and Bayley, H. (2000) Interaction of the non-covalent molecular adapter, β-cyclodextrin, with the staphylococcal α-hemolysin pore Biophys. J. 79, 1967-1975
47. Greiner, J., Manfredi, A., and Riess, J. G. (1989) Synthesis and preliminary evaluation of 2-(F-alkyl)-ethyl glycosides, a series of new F-alkylated surfactants for in vivo uses New J. Chem. 13, 247-254