Membrane insertion of the N-terminal α-helix of equinatoxin II, a sea anemone cytolytic toxin

Biochemical Journal

Volumn 384, Issue 2, 2004, Pages 421-428

  Gutiérrez Aguirre, Ion ^a,b   Barlič, Ariana ^a   Podlesek, Zdravko ^b   Maček, Peter ^b   Anderluh, Gregor ^b   González Mañas, Juan M ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Actinoporin; Amphipathic helix; Membrane interaction; Pore forming toxin

Indexed keywords

CELL MEMBRANES; LIPIDS; MONOLAYERS; MUTAGENESIS; POSITIVE IONS; PROTEINS;

CYTOTOXINS; LIPID MONOLAYERS; MEMBRANE INSERTION; OLIGOMERIZATION;

TOXIC MATERIALS;

ALANINE; CYTOTOXIN; EQUINATOXIN; EQUINATOXIN II; ISOLEUCINE; MUTANT PROTEIN; PHOSPHOLIPID; TRYPTOPHAN; UNCLASSIFIED DRUG; VALINE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; ERYTHROCYTE GHOST; FLUORESCENCE; GENE INSERTION SEQUENCE; LIPID MEMBRANE; LIPID MONOLAYER; MEMBRANE BINDING; MOLECULAR INTERACTION; NONHUMAN; OLIGOMERIZATION; PHARMACODYNAMICS; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN STRUCTURE; SEA ANEMONE;

ANIMALS; BRAIN CHEMISTRY; CATTLE; CNIDARIAN VENOMS; EGG YOLK; ERYTHROCYTES; HEMOLYSIS; HORSES; MEMBRANES, ARTIFICIAL; MUTATION; PEPTIDES; PHOSPHATIDYLCHOLINES; PROTEIN STRUCTURE, TERTIARY; SEA ANEMONES; SPECTROMETRY, FLUORESCENCE; SPHINGOMYELINS;

ACTINIARIA; ANEMONE; INSERTION SEQUENCES; INVERTEBRATA; UNIDENTIFIED INSERTION SEQUENCE;

EID: 10644243456     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040601     Document Type: Article

References (40)

1. Gouaux, E. (1997) Channel-forming toxins: tales of transformation. Curr. Opin. Struct. Biol. 7, 566-573
2. Heuck, A. P., Tweten, R. K. and Johnson, A. E. (2001) Beta-barrel pore-forming toxins: intriguing dimorphic proteins. Biochemistry 40, 9065-9073
3. Lakey, J. H. and Slatin, S. L. (2001) Pore-forming colicins and their relatives. Curr. Top. Microbiol. Immunol. 257, 131-161
4. Anderluh, G. and Maček, P (2002) Cytolytic peptide and protein toxins from sea anemones (Anthozoa: Actiniaria). Toxicon 40, 111-124
5. Giese, C., Mebs, D. and Werding, B. (1996) Resistance and vulnerability of crustaceans to cytolytic sea anemone toxins. Toxicon 34, 955-958
6. Mebs, D. (1994) Anemonefish symbiosis: vulnerability and resistance of fish to the toxin of the sea anemone. Toxicon 32, 1059-1068
7. Maček, P. and Lebez, D. (1988) Isolation and characterization of three lethal and hemolytic toxins from the sea anemone Actinia equina L. Toxicon 26, 441-451
8. Teng, C. M., Lee, L. G., Lee, C. Y. and Ferlan, I. (1988) Platelet aggregation induced by equinatoxin. Thromb. Res. 52, 401-411
9. Lafranconi, W. M., Ferlan, I., Russell, F. E. and Huxtable, R. J. (1984) The action of equinatoxin, a peptide from the venom of the sea anemone, Actinia equina, on isolated lung. Toxicon 22, 347-352
10. Bunc, M., Drevenšek, G., Budihna, M. and Šuput, D. (1999) Effects of equinatoxin II from Actinia equina (L.) on isolated rat heart: the role of direct cardiotoxic effects in equinatoxin II lethality. Toxicon 37, 109-123
11. Athanasiadis, A., Anderluh, G., Maček, P. and Turk, D. (2001) Crystal structure of the soluble form of equinatoxin II, a pore-forming toxin from the sea anemone Actinia equina. Structure (Cambridge) 9, 341-346
12. Hinds, M. G., Zhang, W., Anderluh, G., Hansen, P. E. and Norton, R. S. (2002) Solution structure of the eukaryotic pore-forming cytolysin equinatoxin II: implications for pore formation. J. Mol. Biol. 315, 1219-1229
13. Mancheño, J. M., Martín-Benito, J., Martínez-Ripoll, M., Gavilanes, J. G. and Hermoso, J. A. (2003) Crystal and electron microscopy structures of sticholysin II actinoporin reveal insights into the mechanism of membrane pore formation. Structure (Cambridge) 11, 1319-1328
14. Hong, Q., Gutiérrez-Aguirre, I., Barlič, A., Malovrh, P., Kristan, K., Podlesek, Z., Maček, P, Turk, D., González- Mañas, J. M., Lakey, J. H. and Anderluh, G. (2002) Two-step membrane binding by Equinatoxin II, a pore-forming toxin from the sea anemone, involves an exposed aromatic cluster and a flexible helix. J. Biol. Chem. 277, 41916-41924
15. Malovrh, P., Barlič, A., Podlesek, Z., Maček, P., Menestrina, G. and Anderluh, G. (2000) Structure-function studies of tryptophan mutants of equinatoxin II, a sea anemone pore-forming protein. Biochem. J. 346, 223-232
16. Malovrh, P., Viero, G., Dalla Serra, M., Podlesek, Z., Lakey, J. H., Maček, P., Menestrina, G. and Anderluh, G. (2003) A novel mechanism of pore formation: membrane penetration by the N-terminal amphipathic region of equinatoxin. J. Biol. Chem. 278, 22678-22685
17. Belmonte, G., Pederzolli, C., Maček, P. and Menestrina, G. (1993) Pore formation by the sea anemone cytolysin equinatoxin II in red blood cells and model lipid membranes. J. Membr. Biol. 131, 11-22
18. Tejuca, M., Dalla Serra, M., Ferreras, M., Lanio, M. E. and Menestrina, G. (1996) Mechanism of membrane permeabilization by sticholysin I, a cytolysin isolated from the venom of the sea anemone Stichodactyla helianthus. Biochemistry 35, 14947-14957
19. Valcarcel, C. A., Dalla Serra, M., Potrich, C., Bernhart, I., Tejuca, M., Martinez, D., Pazos, F., Lanio, M. E. and Menestrina, G. (2001) Effects of lipid composition on membrane permeabilization by sticholysin I and II, two cytolysins of the sea anemone Stichodactyla helianthus. Biophys. J. 80, 2761-2774
20. Anderluh, G., Dalla Serra, M., Viero, G., Guella, G., Maček, P. and Menestrina, G. (2003) Pore formation by equinatoxin II, a eukaryotic protein toxin, occurs by induction of nonlamellar lipid structures. J. Biol. Chem. 278, 45216-45223
21. Perkins, S. J. (1986) Protein volumes and hydration effects. Eur. J. Biochem. 157, 169-180
22. Anderluh, G., Barlič, A., Podlesek, Z., Maček, P., Pungerčar, J., Gubenšek, F., Zecchini, M. L., Dalla Serra, M. and Menestrina, G. (1999) Cysteine-scanning mutagenesis of an eukaryotic pore-forming toxin from sea anemone. Eur. J. Biochem. 263, 128-136
23. Anderluh, G., Pungerčar, J., Štrukelj, B., Maček, P. and Gubenšek, F. (1996) Cloning, sequencing, and expression of equinatoxin II. Biochem. Biophys. Res. Commun. 220, 437-442
24. Louw, A. and Visser, L. (1977) Kinetics of erythrocyte lysis by snake cardiotoxins. Biochim. Biophys. Acta 498, 143-153
25. Steck, T. L. and Kant, J. A. (1974) Preparation of impermeable ghosts and inside-out vesicles from human erythrocyte membranes. Methods Enzymol. 31, 172-180
26. Stryer, L. (1965) The interaction of a naphthalene sulfonate dye with apomyoglobin and apohemoglobin. A fluorescent probe for nonpolar sites. J. Mol. Biol. 13, 482-495
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. 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
29. Lehrer, S. S. (1971) Solute perturbation of protein fluorescence. Quenching of tryptophyl fluorescence of model compounds and of lysozyme by iodide ion. Biochemistry 10, 3254-3263
30. Eftink, M. R. and Ghiron, C. A. (1976) Exposure of tryptophanyl residues in proteins. Quantitative determination by quenching studies. Biochemistry 15, 672-682
31. Shepard, L. A., Heuck, A. P., Hamman, B. D., Rossjohn, J., Parker, M. W., Ryan, K. R., Johnson, A. E. and Tweten, R. K. (1998) Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens Perfringolysin 0: an α-helical to β-sheet transition identified by fluorescence spectroscopy. Biochemistry 37, 14563-14574
32. Heuck, A. P. and Jonson, A. E. (2002) Pore-forming protein structure analysis in membranes using multiple independent fluorescence techniques. Cell. Biochem. Biophys. 36, 89-101
33. Merrill, A. R., Palmer, L. R. and Szabo, A. G. (1993) Acrylamide quenching of the intrinsic fluorescence of tryptophan residues genetically engineered into the soluble colicin E1 channel peptide. Structural characterization of the insertion-competent state. Biochemistry 32, 6974-6981
34. Malenbaum, S. E., Collier, R. J. and London, E. (1998) Membrane topography of the T domain of diphtheria toxin probed with single tryptophan mutants. Biochemistry 37, 17915-17922
35. Tory, M. C. and Merrill, A. R. (1999) Adventures in membrane protein topology. A study of the membrane-bound state of colicin E1. J. Biol. Chem. 274, 24539-24549
36. White, S. H. and Wimley, W. C. (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3, 842-848
37. Escrive, C. and Laguerre, M. (2001) Molecular dynamics simulations of the insertion of two ideally amphipathic lytic peptides LK15 and LK9 in a 1,2-dimyristoyl-phosphatidylcholine monolayer. Biochim. Biophys. Acta 1513, 63-74
38. Maček, P., Zecchini, M., Pederzolli, C., Dalla Serra, M. and Menestrina, G. (1995) Intrinsic tryptophan fluorescence of equinatoxin II, a pore-forming polypeptide from the sea anemone Actinia equina L. monitors its interaction with lipid membranes. Eur. J. Biochem. 234, 329-335
39. Caaveiro, J. M. M., Echabe, I., Gutiérrez-Aguirre, I., Nieva, J. L., Arrondo, J. L. R. and González-Mañas, J. M. (2001) Differential interaction of Equinatoxin II with model membranes in response to lipid composition. Biophys. J. 80, 1343-1353
40. Bolen, E. J. and Holloway, P. W. (1990) Quenching of tryptophan fluorescence by brominated phospholipid. Biochemistry 29, 9638-9643