Functional characterization of sticholysin I and W111C mutant reveals the sequence of the actinoporin's pore assembly

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Antonini, Valeria ^a   Pérez Barzaga, Victor ^b   Bampi, Silvia ^a   Pentón, David ^b   Martínez, Diana ^b   Serra, Mauro Dalla ^a   Tejuca, Mayra ^b  

^a FONDAZIONE BRUNO KESSLER   (Italy)

^b UNIVERSITY OF HAVANA   (Cuba)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOSOME; OLIGOMER; PHOSPHATIDYLCHOLINE; STICHOLYSIN I; TOXIN; UNCLASSIFIED DRUG; CYSTEINE; IMMUNOTOXIN; ION; LIPID; LIPID BILAYER; ORGANIC COMPOUND; RECOMBINANT PROTEIN; STYCHOLYSIN I;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ERYTHROCYTE; HEMOLYSIS; LIPID BILAYER; LIPID VESICLE; MEMBRANE LEAFLET; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN LIPID INTERACTION; RESIDUE ANALYSIS; SEQUENCE ANALYSIS; TOXIN ANALYSIS; ADSORPTION; ANIMAL; CHEMISTRY; CRYOELECTRON MICROSCOPY; DRUG EFFECTS; ELECTRIC CONDUCTIVITY; GENETICS; HUMAN; MUTATION; PERMEABILITY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEA ANEMONE;

ADSORPTION; ANIMALS; CRYOELECTRON MICROSCOPY; CYSTEINE; ELECTRIC CONDUCTIVITY; ERYTHROCYTES; HEMOLYSIS; HUMANS; IMMUNOTOXINS; IONS; LIPID BILAYERS; LIPIDS; LIPOSOMES; MUTATION; ORGANIC CHEMICALS; PERMEABILITY; PHOSPHATIDYLCHOLINES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEA ANEMONES;

EID: 84908577181     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110824     Document Type: Article

References (48)

1. Burks R.L. , Lodge D.M. (2 002) Cued in: advances and opportunities in freshwater chemical ecology. J Chem Ecol 28: 1901-1917.
2. Sher D, Knebel A, Bsor T, Nesher N, Tal T, et al. (2005) Toxic polypeptides of the hydra-a bioinformatic approach to cnidarian allomones. Toxicon 45: 865-879.
3. Anderluh G, Macek P (2002) Cytolytic peptide and protein toxins from sea anemones (Anthozoa: Actiniaria). Toxicon 40: 111-124.
4. Kristan K, Viero G, Dalla Serra M, Macek P, Anderluh G (2009) Molecular mechanism of pore formation by actinoporins. Toxicon 54: 1125-1134.
5. Mancheno JM, Martin-Benito J, Martinez-Ripoll M, Gavilanes JG, Hermoso JA (2003) Crystal and electron microscopy structures of sticholysin II actinoporin reveal insights into the mechanism of membrane pore formation. Structure 11: 1319-1328.
6. Athanasiadis A, Anderluh G, Macek P, Turk D (2001) Crystal structure of the soluble form of equinatoxin II, a pore-forming toxin from the sea anemone Actinia equina. Structure 9: 341-346.
7. Hinds MG, Zhang W, Anderluh G, Hansen PE, Norton RS (2002) Solution structure of the eukaryotic pore-forming cytolysin equinatoxin II: Implications for pore formation. J Mol Biol 315: 1219-1229.
8. Mechaly AE, Bellomio A, Gil-Carton D, Morante K, Valle M, et al. (2011) Structural insights into the oligomerization and architecture of eukaryotic membrane pore-forming toxins. Structure 19: 181-191.
9. Garcia-Linares S, Castrillo I, Bruix M, Menendez M, Alegre-Cebollada J, et al. (2013) Three-dimensional structure of the actinoporin sticholysin I. Influence of long-distance effects on protein function. Arch Biochem Biophys 532: 39-45.
10. Gutierrez-Aguirre I, Barlic A, Podlesek Z, Macek P, Anderluh G, et al. (2004) Membrane insertion of the N-terminal alpha-helix of equinatoxin II, a sea anemone cytolytic toxin. Biochem J 384: 421-428.
11. Malovrh P, Viero G, Dalla Serra M, Podlesek Z, Lakey JH, et al. (2003) A novel mechanism of pore-formation: equinatoxin penetration of membrane by a Nterminal amphipatic region. J Biol Chem 278: 22678-22685.
12. Kristan K, Viero G, Macek P, Dalla Serra M, Anderluh G (2007) The Equinatoxin N-Terminus is transferred across planar bilayers and helps to stabilise the transmembrane pore. FEBS J 274: 539-550.
13. Rojko N, Kristan KC, Viero G, Zerovnik E, Macek P, et al. (2013) Membrane Damage by an alpha-Helical Pore-forming Protein, Equinatoxin II, Proceeds through a Succession of Ordered Steps. J Biol Chem 288: 23704-23715.
14. Anderluh G, Barlic A, Podlesek Z, Macek P, Pungercar J, et al. (1999) Cysteine scanning mutagenesis of an eucaryotic pore-forming toxin from sea anemone: topology in lipid membranes. Eur J Biochem 263: 128-136.
15. Malovrh P, Barlic A, Podlesek Z, Menestrina G, Macek P, et al. (2000) Structure/function studies of thryptophan mutants of equinatoxin II, a sea anemone pore-forming protein. Biochem J 346: 223-232.
16. Hong Q, Gutierrez-Aguirre I, Barlic A, Malovrh P, Kristan K, et al. (2002) Twostep 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.
17. Alegre-Cebollada J, Cunietti M, Herrero-Galan E, Gavilanes JG, Martinez-del-Pozo A (2008) Calorimetric scrutiny of lipid binding by sticholysin II toxin mutants. J Mol Biol 382: 920-930.
18. Castrillo I, Araujo NA, Alegre-Cebollada J, Gavilanes JG, Martinez-del-Pozo A, et al. (2010) Specific interactions of sticholysin I with model membranes: an NMR study. Proteins 78: 1959-1970.
19. Bakrac B, Gutierrez-Aguirre I, Podlesek Z, Sonnen AFP, Gilbert RJC, et al. (2008) Molecular Determinants of Sphingomyelin Specificity of a Eukaryotic Pore-forming Toxin. J Biol Chem 283: 18665-18677.
20. Tejuca M, Diaz I, Figueredo R, Roque L, Pazos F, et al. (2004) Construction of an immunotoxin with the pore forming protein StI and ior C5, a monoclonal antibody against a colon cancer cell line. Int Immunopharmacol 4: 731-744.
21. Penton D, Perez-Barzaga V, Diaz I, Reytor ML, Campos J, et al. (2011) Validation of a mutant of the pore-forming toxin sticholysin-I for the construction of proteinase-activated immunotoxins. Protein Eng Des Sel 24: 485-493.
22. Anderluh G, Razpotnik A, Podlesek Z, Macek P, Separovic F, et al. (2005) Interaction of the eukaryotic pore-forming cytolysin equinatoxin II with model membranes: 19F NMR studies. J Mol Biol 347: 27-39.
23. Belmonte G, Pederzolli C, Macek P, 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.
24. Tejuca M, Dalla Serra M, Ferreras M, Lanio ME, Menestrina G (1996) The mechanism of membrane permeabilisation by sticholysin I, a cytolysin isolated from the venom of the sea anemone Stichodactyla helianthus. Biochemistry 35: 14947-14957.
25. Baker MA, Rojko N, Cronin B, Anderluh G, Wallace MI (2014) Photobleaching Reveals Heterogeneous Stoichiometry for Equinatoxin II Oligomers. Chembiochem 15: 2139-2145.
26. Dalla Serra M, Tejuca Martínez M (2011) Pore-forming Toxins. In: eLS. John Wiley & Sons, Ltd: Chinchester. Available: http://onlinelibrary.wiley.com/doi/ 10.1002/9780470015902.a0002655.pub2.
27. Fradin C, Satsoura D, Andrews DW (2009) Punching holes in membranes: how oligomeric pore-forming proteins and lipids cooperate to form aqueous channels in membranes. In: Faller R, Jue T, Longo ML, Risbud SH, editors. Biomembrane frontiers. Nanostructures, models, and the design of life. Dordrecht: Humana Press. 223-262.
28. Mueller M, Grauschopf U, Maier T, Glockshuber R, Ban N (2009) The structure of a cytolytic a-helical toxin pore reveals its assembly mechanism. Nature 459: 726-730.
29. Alvarez C, Dalla Serra M, Potrich C, Bernhart I, Tejuca M, et al. (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.
30. Anderluh G, Dalla Serra M, Viero G, Guella G, Macek P, et al. (2003) Pore formation by equinatoxin II, an eukaryotic protein toxin, occurs by induction of non-lamellar lipid structures. J Biol Chem 278: 45216-45223.
31. Pazos F, Valle A, Martinez D, Ramirez A, Calderon L, et al. (2006) Structural and functional characterization of a recombinant sticholysin I (rSt I) from the sea anemone Stichodactyla helianthus. Toxicon 48: 1083-1094.
32. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
33. Renkin EM (1954) Filtration, diffusion, and molecular sieving through porous cellulose membranes. J Gen Physiol 38: 225-243.
34. Ginsburg H, Stein WD (1987) Biophysical analysis of novel transport pathways induced in red blood cell membranes. J Membr Biol 96: 1-10.
35. Carneiro CMM, Krasilnikov OV, Yuldasheva LN, de Carvalho ACC, Nogueira RA (1997) Is the mammalian porin channel, VDAC, a perfect cylinder in the high conductance state? FEBS Lett 416: 187-189.
36. Kuga S (1981) Pore size distribution analysis of gel substances by size exclusion chromatography. Journal of Chromatography 206: 449-461.
37. Muller P, Schiller S, Wieprecht T, Dathe M, Herrmann A (2000) Continuous measurement of rapid transbilayer movement of a pyrene-labeled phospholipid analogue. Chemistry and Physics of Lipids 106: 89-99.
38. Dalla Serra M, Menestrina G (2000) Characterisation of molecular properties of pore-forming toxins with planar lipid bilayers. In: Holst O, editors. Bacterial toxins, methods and protocols. Totowa, New Jersey: Humana Press. 171-188.
39. Pederzolli C, Belmonte G, Dalla Serra M, Macek P, Menestrina G (1995) Biochemical and cytotoxic properties of conjugates of transferrin with equinatoxin II, a cytolysin from a sea anemone. Bioconjug Chem 6: 166-173.
40. Tejuca M, Dalla Serra M, Alvarez C, Potrich C, Menestrina G (2001) Sizing the radius of the pore formed in erythrocytes and lipid vesicles by the toxin sticholysin I from the sea anemone Stichodactyla helianthus . J Membr Biol 183: 125-135.
41. García-Sáez AJ, Coraiola M, Dalla Serra M, Mingarro I, Muller P, et al. (2006) Peptides corresponding to helices 5 and 6 of Bax can independently form large lipid pores. FEBS Journal 273: 971-981
42. Brockman H (1999) Lipid monolayers: why use half a membrane to characterize protein-membrane interactions? Curr Opin Struct Biol 9: 438-443.
43. Tosatto L, Andrighetti AO, Plotegher N, Antonini V, Tessari I, et al. (2012) Alpha-synuclein pore forming activity upon membrane association. Biochim Biophys Acta 1818: 2876-2883.
44. Kyte I, Doolittle RF (1982) A simple method of displaying the hydropathic character of a protein. J Mol Biol 157: 105-132.
45. Los Rios V, Mancheno JM, Lanio ME, Onaderra M, Gavilanes JG (1998) Mechanism of the leakage induced on lipid model membranes by the hemolytic protein sticholysin II from the sea anemone Stichodactyla helianthus. Eur J Biochem 252: 284-289.
46. Epand RM (1998) Lipid polymorphism and protein-lipid interactions. Biochim Biophys Acta - Biomembranes 1376: 353-368.
47. Stoddart D, Ayub M, Hofler L, Raychaudhuri P, Klingelhoefer JW, et al. (2014) Functional truncated membrane pores. Proc Natl Acad Sci U S A 111: 2425-2430.
48. Anderluh G, Lakey JH (2005) Lipid interactions of alpha-Helical Protein Toxins. In Protein-Lipid Interactions. In: Tamm LK, editor. Membrane Domains to Cellular Networks. Weinheim, Germany: Wiley-VCH. 141-162.