The sticholysin family of pore-forming toxins induces the mixing of lipids in membrane domains

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 11, 2013, Pages 2757-2762

  Ros, Uris ^a   Edwards, Michelle A ^b   Epand, Raquel F ^c   Lanio, Maria E ^a   Schreier, Shirley ^d   Yip, Christopher M ^b   Alvarez, Carlos ^a   Epand, Richard M ^c  

^a UNIVERSITY OF HAVANA   (Cuba)

^b UNIVERSITY OF TORONTO   (Canada)

^c MCMASTER UNIVERSITY MEDICAL CENTRE   (Canada)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Actinoporin; Lipid mixing; Lipid phase separation; Pore forming toxin; Sticholysin; Toroidal pore

Indexed keywords

DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIOLEOYLPHOSPHATIDYLCHOLINE; PORE FORMING CYTOTOXIC PROTEIN; SEA ANEMONE TOXIN; SPHINGOMYELIN; STICHOLYSIN I; STICHOLYSIN II; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; DIFFERENTIAL SCANNING CALORIMETRY; LIPID ANALYSIS; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE BINDING; MEMBRANE FORMATION; MEMBRANE PORE FORMATION; MEMBRANE STRUCTURE; PHASE SEPARATION; PHASE TRANSITION; PRIORITY JOURNAL;

ΔH; ACTINOPORIN; AFM; ATOMIC FORCE MICROSCOPY; CALORIMETRIC ENTHALPIES; CHOL; CHOLESTEROL; DIFFERENTIAL SCANNING CALORIMETRY; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIOLEOYLPHOSPHATIDYLCHOLINE; DIPALMITOYLPHOSPHATIDYLCHOLINE; DMPC; DOPC; DPPC; DSC; EGG SPHINGOMYELIN; EQTII; EQUINATOXIN II; ESM; FRAC; FRAGACEATOXIN C; LD; LIPID MIXING; LIPID PHASE SEPARATION; LIQUID-DISORDERED DOMAIN; LIQUID-ORDERED DOMAIN; LO; MLV; MULTILAMELLAR VESICLES; PFTS; PORE FORMING TOXINS; PORE-FORMING TOXIN; SM; SMALL UNILAMELLAR VESICLES; SPHINGOMYELIN; STI AND STII; STICHOLYSIN; STICHOLYSIN I AND II; SUV; T(M); TEMPERATURE OF TRANSITION; TOROIDAL PORE;

ANIMALS; CALORIMETRY, DIFFERENTIAL SCANNING; CNIDARIAN VENOMS; LIPIDS; MEMBRANE MICRODOMAINS; MICROSCOPY, ATOMIC FORCE; ORGANIC CHEMICALS; SEA ANEMONES;

ACTINIARIA; EUKARYOTA; STICHODACTYLA HELIANTHUS;

EID: 84883191834     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.08.001     Document Type: Article

References (47)

1. M.R. Yeaman, and N.Y. Yount Mechanisms of antimicrobial peptide action and resistance Pharmacol. Rev. 55 2003 27 55 (Pubitemid 36268398)
2. M.E. Lanio, V. Morera, C. Álvarez, M. Tejuca, T. Gómez, F. Pazos, V. Besada, D. Martínez, V. Huerta, G. Padrón, and M.A. Chávez Purification and characterization of two hemolysins from Stichodactyla helianthus Toxicon 39 2001 187 194
3. W.R. Kem The biology of the nematocyst Sea Anemone Toxins: Structure and Action 1988 Academic Press New York 375 405
4. G. Anderluh, and P. Macek Cytolytic peptide and protein toxins from sea anemones (Anthozoa: Actiniaria) Toxicon 40 2002 111 124 (Pubitemid 33016540)
5. M. Tejuca, M. Dalla Serra, M. Ferreras, M.E. Lanio, and G. Menestrina Mechanism of membrane permeabilization by sticholysin I, a cytolysin isolated from the venom of the sea anemone Stichodactyla helianthus Biochemistry 35 1996 14947 14957 (Pubitemid 26423831)
6. A. Athanasiadis, G. Anderluh, P. Macek, and D. Turk Crystal structure of the soluble form of equinatoxin II, a pore-forming toxin from the sea anemone Actinia equina Structure 9 2001 341 346 (Pubitemid 32772579)
7. M.G. Hinds, W. Zhang, G. Anderluh, P.E. Hansen, and R.S. Norton Solution structure of the eukaryotic pore-forming cytolysin equinatoxin II: implications for pore formation J. Mol. Biol. 315 2002 1219 1229 (Pubitemid 34729299)
8. S. García-Linares, I. Castrillo, M. Bruix, M. Menéndez, J. Alegre-Cebollada, A. Martínez-Del-Pozo, and J.G. Gavilanes Three-dimensional structure of the actinoporin sticholysin I. Influence of long distance effects on protein function Arch. Biochem. Biophys. 532 2013 39 45
9. J.M. Mancheño, J. Martin-Benito, M. Martínez-Ripoll, J.G. Gavilanes, and J.A. Hermoso Crystal and electron microscopy structures of sticholysin II actinoporin reveal insights into the mechanism of membrane pore formation Structure 11 2003 1319 1328 (Pubitemid 37412414)
10. A.E. Mechaly, A. Bellomio, D. Gil-Cartón, K. Morante, M. Valle, J.M. González-Mañas, and M.A. Guérin Structural insights into the oligomerization and architecture of eukaryotic membrane pore-forming toxins Structure 19 2011 181 191
11. G. Anderluh, J. Pungercar, I. Krizaj, B. Strukelj, F. Gubensek, and P. Macek N-Terminal truncation mutagenesis of equinatoxin II, a pore-forming protein from the sea anemone Actinia equina Protein Eng. 10 1997 751 755 (Pubitemid 27405921)
12. Q. Hong, I. Gutiérrez-Aguirre, A. Barlič, P. Malovrh, K. Kristan, Z. Podlesek, P. Maček, D. Turk, J.M. Gonzalez-Mañas, J.H. Lakey, and G. Anderluh 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 2002 41916 41924 (Pubitemid 35257504)
13. P. Malovrh, G. Viero, M. Dalla Serra, Z. Podlesek, J.H. Lakey, P. Macek, G. Menestrina, and G. Anderluh A novel mechanism of pore formation: membrane penetration by the N-terminal amphipathic region of equinatoxin J. Biol. Chem. 278 2003 22678 22685 (Pubitemid 36830327)
14. K. Kristan, Z. Podlesek, V. Hojnik, I. Gutiérrez-Aguirre, G. Guncar, D. Turk, J.M. González-Mañas, J.H. Lakey, P. Macek, and G. Anderluh Pore formation by equinatoxin, a eukaryotic pore-forming toxin, requires a flexible N-terminal region and a stable β-sandwich J. Biol. Chem. 279 2004 46509 46517 (Pubitemid 39518294)
15. F. Pazos, A. Valle, D. Martínez, A. Ramírez, L. Calderón, A. Pupo, M. Tejuca, V. Morera, J. Campos, R. Fando, F. Dyszy, S. Schreier, E. Horjales, C. Álvarez, M.E. Lanio, and E. Lissi Structural and functional characterization of a recombinant sticholysin I (rSt I) from the sea anemone Stichodactyla helianthus Toxicon 48 2006 1083 1094 (Pubitemid 44737891)
16. E.M. Cilli, F.T. Pigossi, E. Crusca Jr., U. Ros, D. Martínez, M.E. Lanio, C. Alvarez, and S. Schreier Correlations between differences in amino-terminal sequences and different hemolytic activity of sticholysins Toxicon 50 2007 1201 1204 (Pubitemid 350087175)
17. J. Alegre-Cebollada, M. Cunietti, E. Herrero-Galán, J.G. Gavilanes, and A. Martínez-del-Pozo Calorimetric scrutiny of lipid binding by sticholysin II toxin mutants J. Mol. Biol. 382 2008 920 930
18. A.W. Bernheimer, and L.S. Avigad Properties of a toxin from the sea anemone Stoichactis helianthus, including specific binding to sphingomyelin Proc. Natl. Acad. Sci. 73 1976 467 471
19. V. de los Ríos, J.M. Mancheño, A. Martínez del Pozo, C. Alfonso, G. Rivas, M. Oñaderra, and J.G. Gavilanes Mechanism of the leakage induced on lipid model membranas by the hemolytic protein sticholysin II from the sea anemone Stichodactyla helianthus FEBS Lett. 455 1999 27
20. B.B. Bonev, Y.H. Lam, G. Anderluh, A. Watts, R.S. Norton, and F. Separovic Effects of the eukaryotic pore-forming cytolysin equinatoxin II on lipid membranes and the role of sphingomyelin Biophys. J. 84 2003 2382 2392 (Pubitemid 36373561)
21. B. Bakrač, I. Gutiérrez-Aguirre, Z. Podlesek, A. Sonnen, R. Gilbert, P. Maček, J. Lakey, and G. Anderluh Molecular determinants of sphingomyelin specificity of a eukaryotic pore-forming toxin J. Biol. Chem. 283 2008 18665 18677
22. A. Drechsler, G. Anderluh, R.S. Norton, and F. Separovic Solid-state NMR study of membrane interactions of the pore-forming cytolysin, equinatoxin II Biochim. Biophys. Acta 1798 2010 244 251
23. A. Barlič, I. Gutiérrez-Aguirre, J.M. Caaveiro, A. Cruz, M.B. Ruiz-Argüello, J. Pérez-Gil, and J.M. González- Mañas Lipid fase cohexistence favours membrane insertion of equinatoxin-II, a pore-forming toxin from Actinia equina J. Biol. Chem. 279 2004 34209 34216 (Pubitemid 39318044)
24. J. Alegre-Cebollada, I. Rodríguez-Crespo, J.G. Gavilanes, and A. Martínez del Pozo Detergent-resistant membranes are platforms for actinoporin pore-forming activity on intact cells FEBS J. 273 2006 863 871
25. P. Schön, A.J. García-Sáez, P. Malovrh, K. Bacia, G. Anderluh, and P. Schwille Equinatoxin II permeabilizing activity depends on the presence of sphingomyelin and lipid phase coexistence Biophys. J. 95 2008 691 698
26. C. Álvarez, J.M. Mancheño, D. Martínez, M. Tejuca, F. Pazos, and M.E. Lanio Sticholysins, two pore-forming toxins produced by the Caribbean Sea anemone Stichodactyla helianthus: their interaction with membranes Toxicon 3457 2009 1 14
27. A. Filippov, B. Munavirov, G. Gröbner, and M. Rudakova Lateral diffusion in equimolar mixtures of natural sphingomyelins with dioleoylphosphatidylcholine Magn. Reson. Imaging 3 2012 413 421
28. T.P.W. McMullen, and R.N. McElhaney New aspects of the interaction of cholesterol with dipalmitoylphosphatidylcholine bilayers as revealed by high-sensitivity differential scanning calorimetry Biochim. Biophys. Acta 1234 1995 90 98
29. M.H. Chiu, C.P. Leon Wang, P.M.M. Weers, and E.J. Prenner Apolipophorin III interaction with model membranes composed of phosphatidylcholine and sphingomyelin using differential scanning calorimetry Biochim. Biophys. Acta 1788 2009 2160 2168
30. D.A. Mannock, R.N.A.H. Lewis, T.P.W. McMullen, and R.N. McElhaney The effect of variations in phospholipid and sterol structure on the nature of lipid-sterol interactions in lipid bilayer model membranes Chem. Phys. Lipids 163 2010 403 448
31. T.P.W. McMullen, R.N.A.H. Lewis, and R.N. McElhaney Differential scanning calorimetric study of the effect of cholesterol on the thermotropic phase behavior of a homologous series of linear saturated phosphatidylcholines Biochemistry 32 1993 516 522 (Pubitemid 23034888)
32. T.P.W. McMullen, C. Vilcheze, R.N. McElhaney, and R. Bittman Differential scanning calorimetric study of the effect of sterol side chain length and structure on dipalmitoylphosphatidylcholine thermotropic phase behavior Biophys. J. 69 1995 169 176
33. M. Bretscher Membrane structure: some general principles Science 181 1973 622 629
34. B. Engelmann, S. Streich, U.M. Schönthier, W.O. Richter, and J. Duhm Changes of membrane phospholipid composition of human erythrocytes in hyperlipidemias. I: increased phosphatidylcholine and reduced sphingomyelin in patients with elevated levels of triacylglycerol-rich lipoprotein Biochim. Biophys. Acta 1165 1992 32 37
35. R.M. Epand, A. Thomas, R. Brasseur, and R.F. Epand Cholesterol interaction with proteins that partition into membrane domains; an overview R.J. Harris, Cholesterol Binding and Cholesterol Transport Proteins 2010 Springer New York 253 278
36. H.A. Rinia, and B. de Kruijff Imaging domains in model membranes with atomic force microscopy FEBS Lett. 504 2001 194 199 (Pubitemid 32787069)
37. J.C. Lawrence, D.E. Saslowsky, J.M. Edwardson, and R.M. Henderson Real-time analysis of the effects of cholesterol on lipid raft behavior using atomic force microscopy Biophys. J. 84 2003 1827 1832 (Pubitemid 36322944)
38. S. Chiantia, J. Ries, N. Kahya, and P. Schwille Combined AFM and two-focus SFCS study of raft-exhibiting model membranes Chemphyschem 7 2006 2409 2418
39. L. García-Ortega, J.A. Alegre-Cebollada, S. García-Linares, M. Bruix, A. Martínez-del-Pozo, and J.G. Gavilanes The behavior of sea anemone actinoporins at the water-membrane interface Biochim. Biophys. Acta 1808 2011 2275 2288
40. N. Poklar, J. Fritz, P. Macek, G. Vesnaver, and T.V. Chalikian Interaction of the pore-forming protein equinatoxin II with model lipid membranes: a calorimetric and spectroscopic study Biochemistry 38 1999 14999 15008
41. I. Castrillo, N.A. Araujo, J. Alegre-Cebollada, J.G. Gavilanes, A. Martinez-del-Pozo, and M. Bruix Specific interactions of sticholysin I with model membranes: an NMR study Proteins 78 2010 1959 1970
42. P. Sanchez-Garcia, G. Chieppa, A. Desideri, S. Cannata, E. Romano, P. Luly, and S. Rufini Sticholysin II: a pore-forming toxin as a probe to recognize sphingomyelin in artificial and cellular membranes Toxicon 60 2012 724 733
43. D. Martínez, A. Otero, C. Álvarez, F. Pazos, M. Tejuca, M.E. Lanio, I. Gutiérrez-Aguirre, A. Barlič, I. Iloro, J.L. Arrondo, J.M. González-Mañas, and E. Lissi Effect of sphingomyelin and cholesterol in the interaction of St II with lipidic interfaces Toxicon 49 2007 68 81 (Pubitemid 44920241)
44. J.M. Mancheño, J. Martín-Benito, J.G. Gavilanes, and L. Vázquez A complementary microscopy analysis of Sticholysin II crystals on lipid films: atomic force and transmission electron characterizations Biophys. Chem. 119 2006 219 223 (Pubitemid 43202269)
45. K.C. Kristan, G. Viero, M. Dalla Serra, P. Maček, and G. Anderluh Molecular mechanism of pore formation by actinoporins Toxicon 54 2009 1125 1134
46. A.J. GarcIa-Saez, S. Chiantia, J. Salgado, and P. Schwille Pore formation by a Bax-derived peptide: effect on the line tension of the membrane probed by AFM Biophys. J. 93 2007 103 112 (Pubitemid 47041655)
47. A. Pokorny, and P.F.F. Almeida Permeabilization of raft-containing lipid vesicles by alpha-lysin: a mechanism for cell sensitivity to cytotoxic peptides Biochemistry 44 2005 9538 9544 (Pubitemid 40962052)