Actinoporins from the sea anemones, tropical Radianthus macrodactylus and northern Oulactis orientalis: Comparative analysis of structure-function relationships

Toxicon

Volumn 56, Issue 8, 2010, Pages 1299-1314

  Monastyrnaya, Margarita ^a   Leychenko, Elena ^a   Isaeva, Marina ^a   Likhatskaya, Galina ^a   Zelepuga, Elena ^a   Kostina, Elena ^b   Trifonov, Evgenie ^c   Nurminski, Evgenie ^c   Kozlovskaya, Emma ^a  

^a PACIFIC INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b INSTITUTE OF MARINE BIOLOGY   (Russian Federation)

^c INSTITUTE OF AUTOMATION AND CONTROL PROCESSES   (Russian Federation)

Author keywords

Actinoporin; Amino acid sequence; Hemolytic activity; Homology model; N Terminus; Oulactis orientalis; Phylogenetic analysis; POC binding site; Radianthus macrodactylus; RGD motif; Structure function relationships

Indexed keywords

EQUINATOXIN II; MARINE TOXIN; OR A TOXIN; OR G TOXIN; RTX A TOXIN; RTX SII TOXIN; SEA ANEMONE TOXIN; STICHOLYSIN II; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; COMPARATIVE STUDY; CRYSTAL STRUCTURE; HEMOLYSIS; HYDROPHOBICITY; NONHUMAN; OULACTIS ORIENTALIS; PRIORITY JOURNAL; RADIANTHUS MACRODACTYLUS; SEA ANEMONE; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; TOXIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CLONING, MOLECULAR; CNIDARIAN VENOMS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INTEGRINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEA ANEMONES; SEQUENCE ALIGNMENT; STRUCTURE-ACTIVITY RELATIONSHIP;

ACTINIA EQUINA; ACTINIARIA; HETERACTIS CRISPA; OULACTIS; OULACTIS ORIENTALIS; RADIANTHUS; STICHODACTYLA HELIANTHUS;

EID: 77958474950     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2010.07.011     Document Type: Article

References (120)

1. Alegre-Cebollada J., Lacadena V., Õnaderra M., Mancheño J.M., Gavílanes J.G., Martínez del Pozo A. Phenotypic selection and characterization of randomly produced non-haemolytic mutants of the toxic sea anemone protein sticholysin II. FEBS Lett. 2004, 575:14-18.
2. Allured V.S., Collier R.J., Carroll S.F., McKay D.B. Structure of exotoxin A of Pseudomonas aeruginosa 3.0 Ǻ at resolution. Proc. Natl. Acad. Sci. USA 1986, 83:1310-1324.
3. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol 1990, 215:403-410.
4. Alvarez Valcarcel C., Dalla Serra M., Potrich C., Bernhart I., Tejuca M., Martinez D., Pazos F., Lanio M.E., Menestrina G. Effects of lipid composition on membrane permeabilization by Sticholysin I and II, two cytolysins from the sea anemone Stichodactyla helianthus. Biophys. J. 2001, 80:2761-2774.
5. Alvarez C., Casallanovo F., Shida C.S., Nogueira L.V., Martínez D., Tejuca M., Pazos I.F., Lanio M.E., Menestrina G., Lissi E., Schreier S. Binding of sea anemone pore-forming toxins sticholysins I and II to interfaces-Modulation of conformation, activity, and lipid-protein interaction. Chem. Phys. Lipids 2003, 122(1-2):97-105.
6. Anderluh G., Pungerčar J., Štrukelj B., Maček P., Gubenšek F. Cloning, sequencing and expression of equinatoxin II. Biochem. Biophys. Res. Comm. 1996, 220:437-442.
7. Anderluh G., Pungerčar J., Križaj I., Štrukelj B., Gubenšek F., Maček P. N-terminal truncation mutagenesis of equinatoxin II, a pore-forming polypeptide from the sea anemone Actinia equina. Protein Eng. 1997, 10:751-755.
8. Anderluh G., Križaj I., Štrukelj B., Gubenšek F., Maček P., Pungerčar J. Equinatoxins, pore-forming proteins from sea anemone Actinia equina, belong to a multigene family. Toxicon 1999, 37:1391-1401.
9. Anderluh G., Barlič A., Podlesek Z., Maček P., Pungerčar J., Gubenšek F., Zecchini M.L., Dalla Serra M., Menestrina G. Cysteine-scanning mutagenesis of an eukaryotic pore-forming toxin from sea anemone. Topology in lipid membranes. Eur. J. Biochem. 1999, 263:128-136.
10. Anderluh G., Barlič A., Potrich C., Maček P., Menestrina G. Lysine 77 is a key residue in aggregation of equinatoxin II, a pore-forming toxin from the sea anemone Actinia equina. J. Membr. Biol. 2000, 173:47-55.
11. Anderluh G., Maček P. Cytolytic peptide and protein toxins from sea anemones (Anthozoa: Actiniaria). Toxicon 2002, 40:111-124.
12. Anderluh G., Dalla Serra M., Viero G., Guella G., Maček P., Menestrina G. Pore formation by equinatoxin II, a eukaryotic protein toxin, occurs by induction of nonlamellar lipid structures. J. Biol. Chem. 2003, 278:45216-45223.
13. Arnold K., Bordoli L., Kopp J., Schwede T. The SWISS-MODEL Workspace: a web-based environment for protein structure homology modeling. Bioinformatics 2006, 22:195-201.
14. Athanasiadis A., Anderluh G., Maček P., Turk D. Crystal structure of the soluble form of equinatoxin II, a pore-forming toxin from the sea anemone Actinia equina. Structure 2001, 9:341-346.
15. Bakrač B., Gutiérrez-Aguirre I., Podlesek Z., Sonnen A.F.-P., Gilbert R.J.C., Maček P., Lakey J.H., Anderluh G. Molecular determinants of sphingomyelin specificity of a eukaryotic pore forming toxin. J. Biol. Chem. 2009, 283:18665-18677.
16. Belmonte G., Pederzolli C., Maček P., Menestrina G. Pore formation by the sea anemone cytolysin equinatoxin II in red blood cells and model lipid membranes. J. Membr. Biol. 1993, 131:11-22.
17. Belmonte G., Menestrina G., Pederzolli C., Križaj I., Gubenšek F., Turk T., Maček P. Primary and secondary structure of a pore-forming toxin from the sea anemone, Actinia equina L., and its association with lipid vesicles. Biochim. Biophys. Acta 1994, 1192:197-204.
18. Berendsen H.J.C., van der Spoel D., van Drunen R. GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Comm. 1995, 91:43-56.
19. Bernheimer A.W., Avigad L.S. Properties of a toxin from the sea anemone Stoichactis helianthus, including specific binding to sphingomyelin. Proc. Natl. Acad. Sci. USA 1976, 73:467-471.
20. Birck C., Damian L., Marty-Detraves C., Lougarre A., Schulze-Briese C., Koehl P., Fournier D., Paquereau L., Samama J.P. A new lectin family with structure similarity to actinoporins revealed by the crystal structure of Xerocomus chrysenteron lectin XCL. J. Mol. Biol. 2004, 344:1409-1420.
21. Blumenthal K.M., Kem W.R. Primary structure of Stoichactis helianthus cytolysin III. J. Biol. Chem. 1983, 258:5574-5581.
22. Bonev B.B., Lam Y.H., Anderluh G., Watts A., Norton R.S., Separovic F. Effects of the eukaryotic pore-forming cytolysin Equinatoxin II on lipid membranes and the role of sphingomyelin. Biophys. J. 2003, 84:2382-2392.
23. Brezhestovsky P.D., Monastyrnaya M.M., Kozlovskaya E.P., Elyakov G.B. The action of hemolysin from the sea anemone Radianthus macrodactylus on erythrocyte membrane. Dokl. Akad. Nauk USSR (Russian) 1988, 299:748-750.
24. Brosig B., Langosch D. The dimerization motif of the glycophorin A transmembrane segment in membranes: importance of glycine residues. Protein Sci. 1998, 7:1052-1056.
25. Burke R.D., Murray G., Rise M., Wang D. Integrins on eggs: the beta C subunit is essential for formation of the cortical actin cytoskeleton in sea urchin eggs. Dev. Biol. 2004, 265:53-60.
26. Casallanovo F., de Oliveira F.J.F., de Souza F.C., Ros U., Martínez Y., Pentón D., Tejuca M., Martínez D., Pazos F., Pertinhez T.A., Spisni A., Cilli E.M., Lanio M.E., Alvarez C., Schreier S. Model peptides mimic the structure and function of the N-terminus of the pore-forming toxin sticholysin II. Biopolymers 2006, 84(2):169-180.
27. Chanturiya A.N., Shatursky O.Ja., Lishko V.K., Monastyrnaya M.M., Kozlovskaya E.P. The interaction of toxin from Radianthus macrodactylus with bilayer phospholipid membranes. Biol. Membr. (Russian) 1990, 7:763-769.
28. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
29. De los Rios V., Mancheño J.M., Martinez del Pozo A., Alfonso C., Rivas G., Õnaderra M., Gavilanes J.G. Sticholysin II, a cytolysin from the sea anemone Stichodactyla helianthus, is a monomer-tetramer associating protein. FEBS Lett. 1999, 55:27-30.
30. Doyle J.W., Kem W.R. Binding of a radiolabeled sea anemone cytolysin to erythrocyte membranes. Biochim. Biophys. Acta 1989, 987:181-186.
31. Drechsler A., Potrich C., Sabo J.K., Frisanco M., Guella G., Dalla Serra M., Anderluh G., Separovic F., Norton R.S. Structure and activity of the N-terminal region of the eukaryotic cytolysin equinatoxin II. Biochemistry 2006, 45:1818-1828.
32. Eichacker L.A., Granvogl B., Mirus O., Müller B.C., Miess C., Schleiff E. Hiding behind hydrophobicity transmembrane segment in mass spectrometry. J. Biol. Chem. 2004, 279(49):50915-50922.
33. Eisenberg D., Weiss R.M., Terwilliger T.C. The helical hydrophobic moment: a measure of the amphiphilicity of a helix. Nature 1982, 299:371-374.
34. Eisenberg D., Schwarz E., Komaromy M., Wall R. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol. 1984, 179:125-142.
35. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 1997, 18:2714-2723.
36. Gutiérrez-Aguirre I., Barlič A., Podlesek Z., Maček P., Anderluh G., González-Mañas J.M. Membrane insertion of the N-terminal α-helix of equinatoxin II, a sea anemone cytolytic toxin. Biochem. J. 2004, 384(Pt. 2):421-428.
37. Gutiérrez-Aguirre I., Trontelj P., Maček P., Lakey J.H., Anderluh G. Membrane binding of zebrafish actinoporin-like protein: AF domains, a novel superfamily of cell membrane binding domains. Biochem. J. 2006, 398:381-392.
38. Hinds M.G., Zhang W., Anderluh G., Hansen P.E., Norton R.S. Solution structure of the eukaryotic pore-forming cytolysin equinatoxin II: implications for pore formation. J. Mol. Biol. 2002, 315:1219-1229.
39. Hong Q., Gutierrez-Aguirre I., Barlič A., Malovrh P., Kristan K., Podlesek Z., Maček P., Turk D., González-Mañas J.M., Lakey J.H., Anderluh G. 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. 2002, 277:41916-41924.
40. Hristova K., White S.H. Determination of the hydrocarbon core structure of fluid dioleoylphosphocholine (DOPC) bilayers by X-ray diffraction using specific bromination of the double-bonds: effect of hydration. Biophys. J. 1998, 74:2419-2433.
41. Huerta V., Morera V., Guanche Y., Chinea G., González L.J., Betancourt L., Martínez D., Alvarez C., Lanio M.E., Besada V. Primary structure of two cytolysin isoforms from Stichodactyla helianthus differing in their hemolytic activity. Toxicon 2001, 39:1253-1256.
42. Humphrey W., Dalke A., Schulten K. VMD: visual molecular dynamics. J. Mol. Graph 1996, 14:27-38.
43. Il'ina A.P., Monastyrnaya M.M., Sokotun I.W., Egorov Z.A., Nasarenko Ju.A., Likhatskaya G.N., Kozlovskaya E.P. Actinoporins from the sea anemone Oulactis orientalis of Japan see: isolation and some purification. Bioorg. Chem. (Russian) 2005, 31:39-48.
44. Il'ina A.P., Monastyrnaya M.M., Issaeva M.P., Guzev K.V., Rasskasov V.A., Kozlovskaya E.P. Primary structure of actinoporins from the sea anemone Oulactis orientalis. Bioorg. Chem. (Russian) 2005, 31:357-362.
45. Il'ina A., Lipkin A., Barsova E., Issaeva M., Leychenko E., Guzev K., Monastyrnaya M., Lukyanov S., Kozlovskaya E. Amino acid sequence of RTX-A's isoform actinoporin from the sea anemone Radianthus macrodactylus. Toxicon 2006, 47:517-520.
46. Ivanov A.S., Molnar A.A., Kozlovskaya E.P., Monastyrnaya M.M. The action of toxin from Radianthus macrodactylus on biological and model membrane permeability. Biol. Membr. (Russian) 1987, 4:243-248.
47. Jiang X.Y., Yang W.L., Chen H.P., Tu H.B., Wu W.Y., Wei J.W., Wang J., Liu W.H., Xu A.L. Cloning and characterization of an acidic cytolysin cDNA from sea anemone Sagartia rosea. Toxicon 2002, 40:1563-1569.
48. Kawashima Y., Nagai H., Ishida M., Nagashima Y., Shiomi K. Primary structure of echotoxin 2, an actinoporin-like hemolytic toxin from the salivary gland of the marine gastropod Monoplex echo. Toxicon 2003, 42:491-497.
49. Khoo K.S., Kam W.K., Khoo H.E., Gopalakrishnakone P., Chung M.C.M. Purification and partial characterization of two cytolysins from a tropical sea anemone, Heteractis magnifica. Toxicon 1993, 31:1567-1579.
50. Klyshko E.V., Il'ina A.P., Monastyrnaya M.M., Burtseva Yu.V., Kostina E.E., Zykova T.A., Menzorova N.I., Kozlovskaya E.P. Biologically active polypeptides and hydrolytic enzymes in sea anemones of northern temperate waters. Biologiya Morya (Russian) 2003, 29(3):189-194.
51. Klyshko E.V., Il'ina A.P., Likhatskaya G.N., Issaeva M.P., Guzev K.V., Monastyrnaya M.M., Monastyrnaya M.M., Kozlovskaya E.P., Lipkin A.V., Barsova E.I., Kryzhko I.V., Trofimov E.V., Nurminski E.A. Actinoporins: structure and action. Vestnik DVO RAN (Russian) 2004, 3:45-53.
52. Klyshko E.V., Issaeva M.P., Monastyrnaya M.M., Il'ina A.P., Guzev K.V., Vakorina T.I., Dmitrenok P.S., Zykova T.A., Kozlovskaya E.P. Isolation, properties and partial amino acid sequence of a new actinoporin from the sea anemone Radianthus macrodactylus. Toxicon 2004, 44:315-324.
53. Kopp J., Schwede T. The SWISS-MODEL repository of annotated three-dimensional protein structure homology models. Nucleic Acids Res. 2004, 32:D230-D234.
54. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph 1996, 14:51-55.
55. Kostina E.E. On the trophology of sea anemones of the sea of Japan. Distribution and Ecology of Modern and Fossil Marine Organisms 1990, 89-96. Dal. Vost. Otd. Acad. Nauk SSSR, Vladivostok. V.S. Levin, G.A. Evseev (Eds.).
56. Kozlovskaya E.P., Ivanov A.S., Molnar A.A., Grigoriev P.A., Monastyrnaya M.M., Khalilov E.M., Elyakov G.B. Ion channel in membranes induced by haemolysin from sea anemone Radianthus macrodactylus. Dokl. Akad. Nauk USSR (Russian) 1984, 277:1491-1493.
57. Kozlovskaya, E.P., 1990. Sea Anemone Toxins: Structure and Function. Doctoral Thesis, PIBOC FEB RAS, Vladivostok, Russia (in Russian).
58. Kristan K., Podlesek Z., Hojnik V., Gutierrez-Aguirre I., Gunčar G., Turk D., González-Mañas J.M., Lakey J.H., Maček P., Anderluh G. Pore formation by equinatoxin, an eukaryotic pore-forming toxin, requires a flexible N-terminal region and a stable β-sandwich. J. Biol. Chem. 2004, 279:46509-46517.
59. Kristan K., Viero G., Maček P., Dalla Serra M., Anderluh G. The equinatoxin N-terminus is transferred across planar lipid membranes and helps to stabilize the transmembrane pore. FEBS J. 2007, 274:539-550.
60. Kuznetsova S., Emelyanenko V., Monastyrnaya M., Zadan G., Shnyrov V. Fluorescence study of structural properties of cytolysins from the sea anemone Radianthus macrodactylus. Spectroscopy of Biological Molecules: Modern Trends 1997, 49-50. Kluwer Academic publishers, Dordrecht, Boston, London. P. Carmona, R. Navarro, A. Hernanz (Eds.).
61. Ladokhin A.S., White S.H. Interfacial folding and membrane insertion of a designed helical peptide. Biochemistry 2004, 43:5782-5791.
62. Lanio M.E., Morera V., Alvarez C., Tejuca M., Gómez T., Pazos F., Besada V., Martínez D., Huerta V., Padrón G., Chávez M. Purification and characterization of two hemolysins from Stichodactyla helianthus. Toxicon 2001, 39:187-194.
63. Lee K.H., Hong S.Y., Oh J.E., Kwon M., Yoon J.H., Lee J., Lee B.L., Moon H.M. Identification and characterization of the antimicrobial peptide corresponding to C-terminal β-sheet domain of tenecin 1, an antibacterial protein of larvae of Tenebrio molitor. Biochem. J. 1998, 334:99-105.
64. Li J., Koni P.A., Ellar D.J. Structure of the mosquitocidal endotoxin cytB from Bacillus thuringiensis sp. Kyushuensis. J. Mol. Biol. 1996, 257:129-152.
65. Lindahl E., Hess B., Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 2001, 7:306-317.
66. Maček P., Zecchini M., Pederzolli C., Dalla Serra M., Menestrina G. 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. 1995, 234:329-335.
67. Malovrh P., Barlič A., Podlesek Z., Maček P., Menestrina G., Anderluh G. Structure-function studies of tryptophan mutants of equinatoxin II, a sea anemone pore-forming protein. Biochem. J. 2000, 346:223-232.
68. Malovrh P., Viero G., Dalla Serra M., Podlesek Z., Lakey J.H., Maček P., Menestrina G., Anderluh G. A novel mechanism of pore formation. Membrane penetration by the N-terminal amphipathic region of equinatoxin. J. Biol. Chem. 2003, 278:22678-22685.
69. Mancheño J.M., De Los Ríos V., Martínez Del Pozo A., Lanio M.E., Oñaderra M., Gavilanes J.G. Partially folded states of the cytolytic protein sticholysin II. Biochim. Biophys. Acta 2001, 1545(1-2):122-131.
70. Mancheño J.M., Martin-Benito J., Martínez M., Gavilanes J.G., Hermoso J.A. Crystal and electron microscopy structures of sticholysin II actinoporin reveal insights into the mechanism of membrane pore formation. Structure 2003, 11:1-20.
71. Mancheño J.M., Martin-Benito J., Gavilanes J.G., Vázquez L. A complementary microscopy analysis of sticholysin II crystals on lipid films: atomic force and transmission electron characterizations. Biophys. Chem. 2006, 119:219-223.
72. Martin-Benito J., Gavilanes F., De los Rios V., Mancheño J.M., Fernandez J.J., Gavilanes J.G. Two-dimensional crystallization on lipid monolayers and three-dimensional structure of sticholysin II, a cytolysin from the sea anemone Stichodactyla helianthus. Biophys. J. 2000, 78:3186-3194.
73. Menestrina G., Cabiaux V., Tejuca M. Secondary structure of sea anemone cytolysins in soluble and membrane bound form by infrared spectroscopy. Biochem. Biophys. Res. Commun. 1999, 254:174-180.
74. Monastyrnaya M.M., Zykova T.A., Apalikova O.V., Shwets T.V., Kozlovskaya E.P. Biologically active polypeptides from the tropical sea anemone Radianthus macrodactylus. Toxicon 2002, 40:1197-1217.
75. Nagai H., Oshiro N., Takuwa-Kuroda K., Iwanaga S., Nozaki M., Nakajima T.A. A new polypeptide toxin from the nematocyst venom of an Okinawan sea anemone Phyllodiscus semoni (Japanese name "unbachi-isoginchaku"). Biosci. Biotechnol. Biochem. 2002, 66:2621-2625.
76. Norton R.S., Bobek G., Ivanov J.O., Thomson M., Fiala-Beer E.F., Moritz R.L., Simpson R.G. Purification and characterization of proteins with cardiac stimulatory and haemolytic activity from the anemone Actinia tenebrosa. Toxicon 1990, 28:29-41.
77. Orzaez M., Perez-Paya E., Mingarro I. Influence of the C-terminus of the glycophorin A transmembrane fragment on the dimerization process. Protein Sci. 2000, 9:1246-1253.
78. Ottaway J.R. Predators of sea anemones. Tuatara 1977, 22:213-221.
79. Parker M.W., Feil S.C. Pore-forming protein toxins: from structure to function. Prog. Biophys. Mol. Biol. 2005, 88:91-142.
80. Parker M.W., Tucker A.D., Tsernoglou D., Pattus F. Insights into membrane insertion based on studies of colicins. Trends Biochem. Sci. 1990, 15:126-129.
81. Pazos F., Valle A., Martínez D., Ramírez A., Calderón L., Pupo A., Tejuca M., Morera V., Campos J., Fando R., Dyszy F., Schreier S., Horjales E., Alvarez C., Lanio M.E., Lissi E. Structural and functional characterization of a recombinant sticholysin I (rStI) from the sea anemone Stichodactyla helianthus. Toxicon 2006, 48:1083-1094.
82. Piehler J. New methodologies for measuring protein interactions in vivo and in vitro. Curr. Opin. Struct. Biol. 2005, 15:4-14.
83. Poklar N., Lah J., Salobir M., Maček P., Vesnaver G. pH and temperature-induced molten globule-like denatured states of equinatoxin II: a study by UV-melting, DSC, far- and near-UV CD spectroscopy, and ANS fluorescence. Biochemistry 1997, 36:14345-14352.
84. Ramos O.H., Kauskot A., Cominetti M.R., Bechyne I., Salla Pontes C.L., Chareyre F., Manent J., Vassy R., Giovannini M., Legrand C., Selistre-de-Araujo H.S., Crépin M., Bonnefoy A. A novel alpha(v)beta(3)-blocking disintegrin containing the RGD motive, DisBa-01, inhibits bFGF-induced angiogenesis and melanoma metastasis. Clin. Exp. Metastasis 2008, 25(1):53-64.
85. Rudnev V.S., Likhatskaya G.N., Kozlovskaya E.P., Monastyrnaya M.M., Elyakov G.B. Influence of hemolysin from the sea anemone Radianthus macrodactylus on lipid membrane conductivity. Biol. Membr. (Russian) 1984, 1:1019-1024.
86. Ruoslahti E. RGD and other recognition sequences for integrins. Annu. Rev. Cell. Dev. Biol. 1996, 12:697-715.
87. Russ W.P., Engelman D.M. The GXXXG Motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 2000, 296:911-919.
88. Saier M.H., McCaldon P. Statistical and functional analyses of viral and cellular proteins with N-terminal amphipathic α-helices with large hydrophobic moments: importance to macromolecular recognition and organelle targeting. J. Bacteriol. 1988, 170:2296-2300.
89. Samejima Y., Yanagisawa M., Aoki-Tomomatsu Y., Iwasaki E., Ando J., Mebs D. Amino acid sequence studies on cytolytic toxins from sea anemone Heteractis magnifica, Entacmaea quadricolor and Stichodactyla mertensii (Anthozoa). Toxicon 2000, 38:259-264.
90. Sanger F., Nicklen S., Coulson A.R. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 1977, 74:5463-5467.
91. Sanina N.M., Kostetskiy E.Ja Thermotropic behavior of the sea invertebrate's sphingophospholipids. J. Evol. Biochem. Physiol. (Russian) 2000, 36:192-197.
92. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
93. Schiffer M., Edmundson A.B. Use of helical wheels to represent the structures of protein and to identify segments with helical potential. Biophys. J. 1967, 7:121-135.
94. Schwede T., Kopp J., Guex N., Peitsch M.C. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 2003, 31:3381-3385.
95. Seelig J. Thermodynamics of lipid-peptide interactions. Biochim. Biophys. Acta 2004, 1666(1-2):40-50.
96. Shatursky O., Heuck A.P., Shepard L.A., Rossjohn J., Parker M.W., Johnson A.E., Tweten R.K. The mechanism of membrane insertion for a cholesterol-dependent cytolysin: a novel paradigm for pore-forming toxins. Cell 1999, 99:293-299.
97. Sher D., Knebel A., Bsor T., Nesher N., Tal T., Morgenstern D., Cohen E., Fishman Y., Zlotkin E. Toxic polypeptides of the hydra - a bioinformatic approach to cnidarian allomones. Toxicon 2005, 45:865-879.
98. Shnyrov V.L., Monastyrnaya M.M., Zhadan G.G., Kuznetsova S.M., Kozlovskaya E.P. Calorimetric study of interaction of toxin from Radianthus macrodactylus with erythrocyte membrane. Biochem. Int. 1992, 26:219-229.
99. Silverman J.A., Mindell J.A., Zhan H., Finkelstein A., Collier R.J. Structure-function relationships in diphtheria toxin channels: I. Determining a minimal channel-forming domain. J. Membr. Biol. 1994, 137:17-28.
100. Song L., Hobaugh M.R., Shustak C., Cheley S., Bayley H., Gouaux J.E. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 1996, 274(5294):1859-1866.
101. Schön P., García-Sáez A.J., Malovrh P., Bacia K., Anderluh G., Schwille P. Equinatoxin II permeabilizing activity depends on the presence of sphingomyelin and lipid phase coexistence. Biophys. J. 2008, 95:691-698.
102. Steck T.L. The organization of proteins in the human red blood cell membrane: a review. J. Cell Biol. 1974, 62:1-19.
103. Takagi J. Molecular environment of integrins. Structural basis for ligand recognition by RGD (Arg-Gly-Asp)-dependent integrins. Biochem. Soc. Trans. 2004, 32:403-406.
104. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 10.1093/molbev/msm092.
105. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
106. Tomich J. Amphipathic helices in channel forming structures. The Amphipathic Helix 1993, 221-254. CRC Press, Florida, USA. R.M. Epand (Ed.).
107. Trigueros V., Lougarre A., Ali-Ahmed D., Rahbé Y., Guillot J., Chavant L., Fournier D., Paquereau L. Xerocomus chrysenteron lectin: identification of a new pesticidal protein. Biochim. Biophys. Acta 2003, 1621:292-298.
108. Turk T. Cytolytic toxins from sea anemones. J. Toxicol.-Toxin Rev. 1991, 10:223-262.
109. Uechi G., Toma H., Arakawa T., Sato Y. Biochemical and physiological analyses of a hemolytic toxin isolated from a sea anemone Actineria villosa. Toxicon 2005, 45:761-766.
110. Vakorina T.I., Klyshko E.V., Monastyrnaya M.M., Kozlovskaya E.P. Conformational stability and hemolytic activity of actinoporin RTX-SII from the sea anemone Radianthus macrodactylus. Biochem. (Russian) 2005, 70:957-966.
111. Van Praët M. Amylase-, trypsin- and chymotrypsin-like proteases from Actinia equina L.; their role in the nutrition of this sea anemone. Comp. Biochem. Physiol. 1982, 72(A):523-528.
112. Varanda A., Finkelstein A. Ion and non electrolyte permeability properties of channels formed in planar lipid bilayer membranes by the cytolytic toxin from the sea anemone, Stoichactis helianthus. J. Membr. Biol. 1980, 55:203-211.
113. Wang Y., Chua K.L., Khoo H.E. A new cytolysin from the sea anemone, Heteractis magnifica: isolation, cDNA cloning and functional expression. Biochem. Biophys. Acta 2000, 1478:8-18.
114. White K.L., Passipiery M., Bunch T.D., Campbell K.D., Pate B. Effects of Arginine-Glycine-Aspartic acid (RGD) containing snake venom peptides on parthenogenetic development and in vitro fertilization of bovine oocytes. Mol. Reprod. Dev. 2007, 74:88-96.
115. White S.H., Wimley W.C. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 1999, 28:319-365.
116. Wimley W.C., White S.H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 1996, 3:842-848.
117. Yang L., Harroun T.A., Weiss T.M., Ding L., Huang H.W. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 2001, 81:1475-1485.
118. Yue L.M., Zhang L., He Y.P., Zhang J.H., Zheng J., He Y.F., Zheng Y., Zhang J., Zhang L. Reorganization of cytoskeletal proteins of mouse oocytes mediated by integrins. Sci. China, Ser. C Life Sci. 2004, 47:540-544.
119. Zhang W., Hinds M.G., Anderluh G., Hansen P.E., Norton R.S. Sequence-specific resonance assignments of the potent cytolysin equinatoxin II. J. Biomol. NMR 2000, 18:281-282.
120. Zuckerkandl E., Pauling L. Evolutionary divergence and convergence in proteins. Evolving Genes and Proteins 1965, 97-166. Academic Press, New York, USA. V. Bryson, H.J. Vogel (Eds.).