Chaperoning of insertion of membrane proteins into lipid bilayers by hemifluorinated surfactants: Application to diphtheria toxin

Biochemistry

Volumn 45, Issue 8, 2006, Pages 2629-2635

  Palchevskyy, Sergiy S ^a   Posokhov, Yevgen O ^a   Olivier, Blandine ^b   Popot, Jean Luc ^c   Pucci, Bernard ^b   Ladokhin, Alexey S ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF AVIGNON   (France)

^c INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOASSAY; FLUORIDE MINERALS; HYDROGENATION; LIPIDS; MONOMERS; RESONANCE; SURFACE ACTIVE AGENTS;

HEMIFLUORINATED COMPOUNDS; LIPID VESICLES; MEMBRANE PROTEINS; NONDISSOCIATING CONDITIONS;

PROTEINS;

CHAPERONE; COLICIN; DIPHTHERIA TOXIN; FLUORINE; MEMBRANE PROTEIN; SURFACTANT; TRANSLOCON;

ACIDIFICATION; ARTICLE; CHEMICAL STRUCTURE; CONFORMATIONAL TRANSITION; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIPID BILAYER; LIPID VESICLE; MICELLE; MISCIBILITY; PH; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN STABILITY; STEADY STATE; THERMODYNAMICS;

DIPHTHERIA TOXIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HYDROGEN-ION CONCENTRATION; LIPID BILAYERS; MEMBRANE PROTEINS; MICELLES; MODELS, MOLECULAR; MOLECULAR WEIGHT; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SURFACE-ACTIVE AGENTS;

EID: 33644530973     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052257l     Document Type: Article

References (42)

1. Johnson, A. E., and van Waes, M. A. (1999) The translocon: A dynamic gateway at the ER membrane, Annu. Rev. Cell Dev. Biol. 15, 799-842.
2. Alder, N. N., and Johnson, A. E. (2004) Cotranslational membrane protein biogenesis at the endoplasmic reticulum, J. Biol. Chem. 279, 22787-22790.
3. Rapoport, T. A., Goder, V., Heinrich, S. U., and Matlack, K. E. S. (2004) Membrane-protein integration and the role of the translocation channel, Trends Cell Biol. 14, 568-575.
4. Oh, K. J., Senzel, L., Collier, R. J., and Finkelstein, A. (1999) Translocation of the catalytic domain of diphtheria toxin across planar phospholipid bilayers by its own T domain, Proc. Natl. Acad. Sci. U.S.A. 96, 8467-8470.
5. Miller, C. J., Elliott, J. L., and Collier, R. J. (1999) Anthrax protective antigen: Prepore-to-pore conversion, Biochemistry 38, 10432-10441.
6. Shatursky, O., Heuck, A. P., Shepard, L. A., Rossjohn, J., Parker, M. W., Johnson, A. E., and Tweten, R. K. (1999) The mechanism of membrane insertion for a cholesterol-dependent cytolysin: A novel paradigm for pore-forming toxins, Cell 99, 293-299.
7. Senzel, L., Gordon, M., Blaustein, R. O., Oh, K. J., Collier, R. J., and Finkelstein, A. (2000) Topography of diphtheria toxin's T domain in the open channel state, J. Gen. Physiol. 115, 421-434.
8. Zakharov, S. D., Lindeberg, M., and Cramer, W. A. (1999) Kinetic description of structural changes linked to membrane import of the colicin El channel protein, Biochemistry 38, 11325-11332.
9. Tory, M. C., and Merrill, A. R. (1999) Adventures in membrane protein topology: A study of the membrane-bound state of colicin El, J. Biol. Chem. 274, 24539-24549.
10. Parker, M. W., Tucker, A. D., Tsernoglou, D., and Pattus, F. (1990) Insights into membrane insertion based on studies of colicins, Trends Biochem. Sci. 15, 126-129.
11. Hessa, T., Kim, H., Bihlmaler, K., Lundin, C., Boekel, J., Andersson, H., Nilsson, I., White, S. H., and von Heijne, G. (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon, Nature 433, 377-381.
12. Bowie, J. U. (2005) Border crossing, Nature 433, 367-369.
13. Ladokhin, A. S., Legmann, R., Collier, R. J., and White, S. H. (2004) Reversible refolding of the diphtheria toxin T-domain on lipid membranes, Biochemistry 43, 7451-7458.
14. Ladokhin, A. S., and Haigler, H. T. (2005) Reversible transition between the surface trimer and membrane-inserted monomer of annexin 12, Biochemistry 44, 3402-3409.
15. Bowie, J. U. (2001) Stabilizing membrane proteins, Curr. Opin. Struct. Biol. 11, 397-402.
16. Gohon, Y., and Popot, J.-L. (2003) Membrane protein-surfactant complexes, Curr. Opin. Colloid Interface Sci. 8, 15-22.
17. Popot, J.-L., Berry, E. A., Charvolin, D., Creuzenet, C., Ebel, C., Engelman, D. M., Flötenmeyer, M., Giusti, F., Gohon, Y., Herv́, P., Hong, Q., Lakey, J. H., Leonard, K., Shuman, H. A., Timmins, P., Warschawski, D. E., Zito, F., Zoonens, M., Pucci, B., and Tribet, C. (2003) Amphipols: Polymeric surfactants for membrane biology research, Cell. Mol. Life Sci. 60, 1559-1574.
18. Tribet, C., Audebert, R., and Popot, J.-L. (1996) Amphipols: Polymers that keep membrane proteins soluble in aqueous solutions, Proc. Natl. Acad. Sci. U.S.A. 93, 15047-15050.
19. Sanders, C. R., Kuhn Hoffmann, A., Gray, D. N., Keyes, M. H., and Ellis, C. D. (2004) French swimwear for membrane proteins, ChemBioChem 5, 423-426.
20. 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.
21. Barthelemy, P., Ameduri, B., Chabaud, E., Popot, J.-L., and Pucci, B. (1999) Synthesis and preliminary assessments of ethyl-terminated perfluoroalkyl nonionic surfactants derived from tris(hydroxymethyl)acrylamidomethane, Org. Lett. 1, 1689-1692.
22. 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.
23. Sanders, C. R., and Myers, J. K. (2004) Disease-related misassembly of membrane proteins, Annu. Rev. Biophys. Biomol. Struct. 33, 25-51.
24. Gelman, M. S., and Kopito, R. R. (2002) Rescuing protein conformation: Prospects for pharmacological therapy in cystic fibrosis, J. Clin. Invest. 110, 1591-1597.
25. Loo, T. W., and Clarke, D. M. (2003) Application of chemical chaperones to the rescue of folding defects, Methods Mol. Biol. 232, 231-243.
26. Haugland, R. P. (1996) Handbook of Fluorescent Probes and Research Chemicals, 6th ed., Molecular Probes, Inc., Eugene, OR.
27. Mayer, L. D., Hope, M. J., and Cullis, P. R. (1986) Vesicles of variable sizes produced by a rapid extrusion procedure, Biochim. Biophys. Acta 858, 161-168.
28. Hope, M. J., Bally, M. B., Mayer, L. D., Janoff, A. S., and Cullis, P. R. (1986) Generation of multilamellar and unilamellar phospholipid vesicles, Chem. Phys. Lipids 40, 89-107.
29. Ladokhin, A. S., Wimley, W. C., Hristova, K., and White, S. H. (1997) Mechanism of leakage of contents of membrane vesicles determined by fluorescence requenching, Methods Enzymol. 278, 474-486.
30. Weiss, M. S., Blanke, S. R., Collier, R. J., and Eisenberg, D. (1995) Structure of the isolated catalytic domain of diphtheria toxin, Biochemistry 34, 773-781.
31. Oh, K. J., Zhan, H., Cui, C., Hideg, K., Collier, R. J., and Hubbell, W. L. (1996) Organization of diphtheria toxin T domain in bilayers: A site-directed spin labeling study, Science 273, 810-812.
32. Oh, K. J., Zhan, H., Cui, C., Altenbach, C., Hubbell, W. L., and Collier, R. J. (1999) Conformation of the diphtheria toxin T domain in membranes: A site-directed spin-labeling study of the TH8 helix and TL5 loop, Biochemistry 38, 10336-10343.
33. Rosconi, M. P., Zhao, G., and London, E. (2004) Analyzing topography of membrane-inserted diphtheria toxin T domain using BODIPY-streptavidin: At low pH, helices 8 and 9 form a transmembrane hairpin but helices 5-7 form stable nonclassical inserted segments on the cis side of the bilayer, Biochemistry 43, 9127-9139.
34. Wang, Y., Malenbaum, S. E., Kachel, K., Zhan, H. J., Collier, R. J., and London, E. (1997) Identification of shallow and deep membrane-penetrating forms of diphtheria toxin T domain that are regulated by protein concentration and bilayer width, J. Biol. Chem. 272, 25091-25098.
35. Chenal, A., Savarin, P., Nizard, P., Guillain, F., Gillet, D., and Forge, V. (2002) Membrane protein insertion regulated by bringing electrostatic and hydrophobic interactions into play. A case study with the translocation domain of the diphtheria toxin, J. Biol. Chem. 277, 43425-43432.
36. Hoch, D. H., Romero-Mira, M., Ehrlich, B. E., Finkelstein, A., DasGupta, B. R., and Simpson, L. L. (1985) Channels formed by botulinum, tetanus, and diphtheria toxins in planar lipid bilayers: Relevance to translocation of proteins, Proc. Natl. Acad. Sci. U.S.A. 82, 1692-1696.
37. Silverman, J. A., Mindell, J. A., Finkelstein, A., Shen, W. H., and Collier, R. J. (1994) Mutational analysis of the helical hairpin region of diphtheria toxin transmembrane domain, J. Biol. Chem. 269, 22524-22532.
38. Bell, C. E., Poon, P. H., Schumaker, V. N., and Eisenberg, D. (1997) Oligomerization of a 45 kilodalton fragment of diphtheria toxin at pH 5.0 to a molecule of 20-24 subunits, Biochemistry 36, 15201-15207.
39. 2+-dependent membrane-binding properties, Biochemistry 44, 2833-2844.
40. Sharpe, J. C., and London, E. (1999) Diphtheria toxin forms pores of different sizes depending on its concentration in membranes: Probable relationship to oligomerization, J. Membr. Biol. 171, 209-221.
41. Langen, R., Isas, J. M., Hubbell, W. L., and Haigler, H. T. (1998) A transmembrane form of annexin XII detected by site-directed spin labeling, Proc. Natl. Acad. Sci. U.S.A. 95, 14060-14065.
42. Nagy, J. K., Kuhn Hoffmann, A., Keyes, M. H., Gray, D. N., Oxenoid, K., and Sanders, C. R. (2001) Use of amphipathic polymers to deliver a membrane protein to lipid bilayers, FEBS Lett. 501, 115-120.