Kinetic intermediate reveals staggered pH-dependent transitions along the membrane insertion pathway of the diphtheria toxin T-domain

Biochemistry

Volumn 48, Issue 32, 2009, Pages 7584-7594

  Kyrychenko, Alexander ^a,b   Posokhov, Yevgen O ^a,b   Rodnin, Mykola V ^a   Ladokhin, Alexey S ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b V N KARAZIN KHARKIV NATIONAL UNIVERSITY   (Ukraine)

Author keywords

[No Author keywords available]

Indexed keywords

ANIONIC LIPIDS; DIPHTHERIA TOXIN; FLUORESCENCE CORRELATION SPECTROSCOPY; KINETIC BARRIER; KINETIC BEHAVIOR; LIPID VESICLES; MEMBRANE ASSOCIATION; MEMBRANE INSERTION; PH DEPENDENCE; PH VALUE; PH-DEPENDENT; SITE SELECTIVE; SPECTROSCOPIC TECHNIQUE; TRANSMEMBRANES;

CELL MEMBRANES; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; LABELS; LIPIDS; POTENTIOMETRIC SENSORS; QUENCHING;

MEMBRANES;

ANION; DIPHTHERIA TOXIN; FLUORESCENT DYE; LIPID;

ARTICLE; BINDING SITE; CELL MEMBRANE; FLUORESCENCE CORRELATION SPECTROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIPID BILAYER; LIPID VESICLE; MEMBRANE BINDING; PH; PRIORITY JOURNAL; PROTEIN DOMAIN;

CYSTEINE; DIPHTHERIA TOXIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROGEN-ION CONCENTRATION; LIPID BILAYERS; MEMBRANE LIPIDS; MEMBRANES; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 68849090174     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9009264     Document Type: Article

References (51)

1. 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.
2. 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.
3. Neale, E. A. (2003) Moving across membranes. Nat. Struct. Biol. 10, 2-3.
4. Collier, R. J., and Young, J. A. (2003) Anthrax toxin. Annu. Rev. Cell Dev. Biol. 19, 45-70.
5. Bennett, M. J., and Eisenberg, D. (1994) Refined structure of monomeric diphtheria toxin at 2.3 Å resolution. Protein Sci. 3, 1464-1475.
6. 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.
7. 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.
8. Kachel, K., Ren, J. H., Collier, R. J., and London, E. (1998) Identifying transmembrane states and defining the membrane insertion boundaries of hydrophobic helices in membrane-inserted diphtheria toxin T domain. J. Biol. Chem. 273, 22950-22956.
9. 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.
10. Zhao, G., and London, E. (2005) Behavior of diphtheria toxin T domain containing substitutions that block normal membrane insertion at Pro345 and Leu307: Control of deep membrane insertion and coupling between deep insertion of hydrophobic subdomains. Biochemistry 44, 4488-4498.
11. 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.
12. 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.
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. 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.
15. Montagner, C., Perier, A., Pichard, S., Vernier, G., Menez, A., Gillet, D., Forge, V., and Chenal, A. (2007) Behavior of the N-terminal helices of the diphtheria toxin t domain during the successive steps of membrane interaction. Biochemistry 46, 1878-1887.
16. Posokhov, Y. O., Rodnin, M. V., Lu, L., and Ladokhin, A. S. (2008) Membrane insertion pathway of annexin B12: Thermodynamic and kinetic characterization by fluorescence correlation spectroscopy and fluorescence quenching. Biochemistry 47, 5078-5087.
17. Haugland, R. P. (1996) Handbook of Fluorescent Probes and Research Chemicals , 6th ed., Molecular Probes, Eugene, OR.
18. Ladokhin, A. S., Isas, J. M., Haigler, H. T., and White, S. H. (2002) Determining the membrane topology of proteins: Insertion pathway of a transmembrane helix of annexin 12. Biochemistry 41, 13617-13626.
19. 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.
20. 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.
21. Bartlett, G. R. (1959) Phosphorus assay in column chromatography. J. Biol. Chem. 234, 466-468.
22. Posokhov, Y. O., and Ladokhin, A. S. (2006) Lifetime fluorescence method for determining membrane topology of proteins. Anal. Biochem. 348, 87-93.
23. Hess, S. T., Huang, S., Heikal, A. A., and Webb, W. W. (2002) Biological and chemical applications of fluorescence correlation spectroscopy: A review. Biochemistry 41, 697-705.
24. Rusu, L., Gambhir, A., McLaughlin, S., and Radler, J. (2004) Fluorescence correlation spectroscopy studies of peptide and protein binding to phospholipid vesicles. Biophys. J. 87, 1044-1053.
25. Rhoades, E., Ramlall, T. F., Webb, W. W., and Eliezer, D. (2006) Quantification of alpha-synuclein binding to lipid vesicles using fluorescence correlation spectroscopy. Biophys. J. 90, 4692-700.
26. Clamme, J. P., Azoulay, J., and Mely, Y. (2003) Monitoring of the formation and dissociation of polyethylenimine/DNA complexes by two photon fluorescence correlation spectroscopy. Biophys. J. 84, 1960-1968.
27. 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.
28. Perier, A., Chassaing, A., Raffestin, S., Pichard, S., Masella, M., Menez, A., Forge, V., Chenal, A., and Gillet, D. (2007) Concerted protonation of key histidines triggers membrane interaction of the diphtheria toxin T domain. J. Biol. Chem. 282, 24239-24245.
29. Ladokhin, A. S., Jayasinghe, S., and White, S. H. (2000) How to measure and analyze tryptophan fluorescence in membranes properly, and why bother? Anal. Biochem. 285, 235-245.
30. Ladokhin, A. S., and White, S. H. (2004) Interfacial folding and membrane insertion of a designed helical peptide. Biochemistry 43, 5782-5791.
31. Ladokhin, A. S., and White, S. H. (2001) Protein chemistry at membrane interfaces: Non-additivity of electrostatic and hydrophobic interactions. J. Mol. Biol. 309, 543-552.
32. Posokhov, Y. O., Gottlieb, P. A., Morales, M. J., Sachs, F., and Ladokhin, A. S. (2007) Is lipid bilayer binding a common property of inhibitor cysteine knot ion-channel blockers? Biophys. J. 93, L20-L22.
33. Ladokhin, A. S., and White, S. H. (1999) Folding of amphipathic α-helices on membranes: Energetics of helix formation by melittin. J. Mol. Biol. 285, 1363-1369.
34. Fernandez-Vidal, M., Jayasinghe, S., Ladokhin, A. S., and White, S. H. (2007) Folding amphipathic helices into membranes: Amphiphilicity trumps hydrophobicity. J. Mol. Biol. 370, 459-470.
35. Moore, J. W., and Pearson, R. G. (1981) Kinetics and Mechanism , 3rd ed., Wiley, New York.
36. Beechem, J. M. (1997) Picosecond fluorescence decay curves collected on millisecond time scale: Direct measurement of hydrodynamic radii, local/global mobility, and intramolecular distances during protein-folding reactions. Methods Enzymol. 278, 24.
37. Rodnin, M. V., Posokhov, Y. O., Contino-Pepin, 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.
38. Lai, B., Zhao, G., and London, E. (2008) Behavior of the deeply inserted helices in diphtheria toxin T domain: helices 5, 8, and 9 interact strongly and promote pore formation, while helices 6/7 limit pore formation. Biochemistry 47, 4565-4574.
39. Ren, J., Sharpe, J. C., Collier, R. J., and London, E. (1999) Membrane translocation of charged residues at the tips of hydrophobic helices in the T domain of diphtheria toxin. Biochemistry 38, 976-984.
40. Khandogin, J., and Brooks, C. L.III (2006) Toward the accurate first-principles prediction of ionization equilibria in proteins. Biochemistry 45, 9363-9373.
41. Gordon, J. C., Myers, J. B., Folta, T., Shoja, V., Heath, L. S., and Onufriev, A. (2005) H++: A server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Res. 33, W368-W371.
42. Li, W., Nicol, F., and Szoka, F. C.Jr. (2004) GALA: A designed synthetic pH-responsive amphipathic peptide with applications in drug and gene delivery. Adv. Drug Deliv. Rev. 56, 967-985.
43. Reshetnyak, Y. K., Segala, M., Andreev, O. A., and Engelman, D. M. (2007) A monomeric membrane peptide that lives in three worlds: In solution, attached to, and inserted across lipid bilayers. Biophys. J. 93, 2363-2372.
44. Kamp, F., and Hamilton, J. A. (2006) How fatty acids of different chain length enter and leave cells by free diffusion. Prostaglandins, Leukotrienes Essent. Fatty Acids 75, 149-159.
45. Bechinger, B. (1996) Towards membrane protein design: pH-sensitive topology of histidine-containing polypeptides. J. Mol. Biol. 263, 768-775.
46. Wimley, W. C., and White, S. H. (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3, 842-848.
47. Zhang, W., Bogdanov, M., Pi, J., Pittard, A. J., and Dowhan, W. (2003) Reversible topological organization within a polytopic membrane protein is governed by a change in membrane phospholipid composition. J. Biol. Chem. 278, 50128-50135.
48. Lu, Y., Turnbull, I. R., Bragin, A., Carveth, K., Verkman, A. S., and Skach, W. R. (2000) Reorientation of aquaporin-1 topology during maturation in the endoplasmic reticulum. Mol. Biol. Cell 11, 2973-2985.
49. Rapp, M., Granseth, E., Seppala, S., and von Heijne, G. (2006) Identification and evolution of dual-topology membrane proteins. Nat. Struct. Mol. Biol. 13, 112-116.
50. Bogdanov, M., Xie, J., and Dowhan, W. (2009) Lipid-protein interactions drive membrane protein topogenesis in accordance with the positive inside rule. J. Biol. Chem. 284, 9637-9641.
51. Sanders, C. R., and Myers, J. K. (2004) Disease-related misassembly of membrane proteins. Annu. Rev. Biophys. Biomol. Struct. 33, 25-51.