Toxicity of an α-pore-forming toxin depends on the assembly mechanism on the target membrane as revealed by single molecule imaging

Journal of Biological Chemistry

Volumn 290, Issue 8, 2015, Pages 4856-4865

  Subburaj, Yamunadevi ^a,b   Ros, Uris ^c   Hermann, Eduard ^a,b,d   Tong, Rudi ^a   García Sáez, Ana J ^a,b,d  

^a MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c Center for Protein Studies Faculty of Biology   (Cuba)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; TOXIC MATERIALS;

ASSEMBLY MECHANISM; MOLECULAR MECHANISM; OLIGOMERIC STATE; PORE FORMING TOXINS; SINGLE-MOLECULE IMAGING;

TOXICITY;

DIMER; EQUINATOXIN; EQUINATOXIN II; HEXAMER; MONOMER; POLYMER; TETRAMER; UNCLASSIFIED DRUG; COELENTERATE VENOM; PORE FORMING CYTOTOXIC PROTEIN;

ARTICLE; CELL MEMBRANE; CELL PERMEABILIZATION; CELL SURFACE; CONTROLLED STUDY; CYTOTOXICITY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; MOLECULAR IMAGING; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; STOICHIOMETRY; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY; TOXIN STRUCTURE; CELL MEMBRANE PERMEABILITY; CHEMISTRY; ERYTHROCYTE MEMBRANE; HEMOLYSIS; PROTEIN MULTIMERIZATION;

CELL MEMBRANE PERMEABILITY; CNIDARIAN VENOMS; ERYTHROCYTE MEMBRANE; HEMOLYSIS; HUMANS; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN MULTIMERIZATION;

EID: 84928408131     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.600676     Document Type: Article

References (45)

1. Iacovache, I., van der Goot, F. G., and Pernot, L. (2008) Pore formation: an ancient yet complex form of attack. Biochim. Biophys. Acta 1778, 1611-1623
2. Potrich, C., Tomazzolli, R., Dalla Serra, M., Anderluh, G., Malovrh, P., Macek, P., Menestrina, G., and Tejuca, M. (2005) Cytotoxic activity of a tumor protease-activated pore-forming toxin. Bioconjug. Chem. 16, 369-376
3. Song, L., Hobaugh, M. R., Shustak, C., Cheley, S., Bayley, H., and Gouaux, J. E. (1996) Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1866
4. Heuck, A. P., Tweten, R. K., and Johnson, A. E. (2001) Beta-barrel pore-forming toxins: intriguing dimorphic proteins. Biochemistry 40, 9065-9073
5. Bayley, H. (2009) Membrane-protein structure: piercing insights. Nature 459, 651-652
6. Garcia-Saez, A. J., Buschhorn, S. B., Keller, H., Anderluh, G., Simons, K., and Schwille, P. (2011) Oligomerization and pore formation by equinatoxin II inhibit endocytosis and lead to plasma membrane reorganization. J. Biol. Chem. 286, 37768-37777
7. Hong, Q., Gutierrez-Aguirre, I., Barlic, A., Malovrh, P., Kristan, K., Podlesek, Z., Macek, P., Turk, D., Gonzalez-Manas, 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
8. Kristan, K., Podlesek, Z., Hojnik, V., Gutierrez-Aguirre, I., Guncar, G., Turk, D., Gonzalez-Mañas, J. M., Lakey, J. H., Macek, P., and Anderluh, G. (2004) Pore formation by equinatoxin, a eukaryotic pore-forming toxin, requires a flexible N-terminal region and a stable β-sandwich. J. Biol. Chem. 279, 46509-46517
9. Anderluh, G., Dalla Serra, M., Viero, G., Guella, G., Macek, 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
10. Belmonte, G., Pederzolli, C., Macek, 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
11. Tejuca, M., Dalla Serra, M., Potrich, C., Alvarez, C., and 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
12. Groulx, N., McGuire, H., Laprade, R., Schwartz, J. L., and Blunck, R. (2011) Single molecule fluorescence study of the Bacillus thuringiensis toxin Cry1Aa reveals tetramerization. J. Biol. Chem. 286, 42274-42282
13. Manchen?, J. M., Martin-Benito, J., Gavilanes, J. G., and Vazquez, L. (2006) A complementary microscopy analysis of Sticholysin II crystals on lipid films: atomic force and transmission electron characterizations. Biophys. Chem. 119, 219-223
14. Mueller, M., Grauschopf, U., Maier, T., Glockshuber, R., and Ban, N. (2009) The structure of a cytolytic α-helical toxin pore reveals its assembly mechanism. Nature 459, 726-730
15. Mechaly, A. E., Bellomio, A., Gil-Carton, D., Morante, K., Valle, M., Gonzalez-Mañas, J. M., and Guerin, D. M. (2011) Structural insights into the oligomerization and architecture of eukaryotic membrane pore-forming toxins. Structure 19, 181-191
16. Schmidt, T., Schutz, G. J., Gruber, H. J., and Schindler, H. (1996) Local stoichiometries determined by counting individual molecules. Anal. Chem. 68, 4397-4401
17. Meckel, T., Semrau, S., Schaaf, M. J., and Schmidt, T. (2011) Robust assessment of protein complex formation in vivo via single-molecule intensity distributions of autofluorescent proteins. J. Biomed. Opt. 16, 076016
18. Jaqaman, K., Loerke, D., Mettlen, M., Kuwata, H., Grinstein, S., Schmid, S. L., and Danuser, G. (2008) Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods 5, 695-702
19. Kusumi, A., Sako, Y., and Yamamoto, M. (1993) Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy): effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65, 2021-2040
20. Lee, G. M., Ishihara, A., and Jacobson, K. A. (1991) Direct observation of brownian motion of lipids in a membrane. Proc. Natl. Acad. Sci. U.S.A. 88, 6274-6278
21. Qian, H., Sheetz, M. P., and Elson, E. L. (1991) Single particle tracking: analysis of diffusion and flow in two-dimensional systems. Biophys. J. 60, 910-921
22. Saxton, M. J., and Jacobson, K. (1997) Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26, 373-399
23. Calebiro, D., Rieken, F., Wagner, J., Sungkaworn, T., Zabel, U., Borzi, A., Cocucci, E., Zurn, A., and Lohse, M. J. (2013) Single-molecule analysis of fluorescently labeled G-protein-coupled receptors reveals complexes with distinct dynamics and organization. Proc. Natl. Acad. Sci. U.S.A. 110, 743-748
24. Hoops, S., Sahle, S., Gauges, R., Lee, C., Pahle, J., Simus, N., Singhal, M., Xu, L., Mendes, P., and Kummer, U. (2006) COPASI: a COmplex PAthway SImulator. Bioinformatics 22, 3067-3074
25. Anderluh, G., Barlic, A., Krizaj, I., Menestrina, G., Gubensek, F., and Macek, P. (1998) Avidin-FITC topological studies with three cysteine mutants of equinatoxin II, a sea anemone pore-forming protein. Biochem. Biophys. Res. Commun. 242, 187-190
26. Rojko, N., Kristan, K.C ., Viero, G., Zerovnik, E., Macek, P., Dalla Serra, M., and Anderluh, G. (2013) Membrane damage by an α-helical pore-forming protein, Equinatoxin II, proceeds through a succession of ordered steps. J. Biol. Chem. 288, 23704-23715
27. Malovrh, P., Viero, G., Serra, M. D., Podlesek, Z., Lakey, J. H., Macek, 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
28. Serge A., de Keijzer, S., Van Hemert, F., Hickman, M. R., Hereld, D., Spaink, H. P., Schmidt, T., and Snaar-Jagalska, B. E. (2011) Quantification of GPCR internalization by single-molecule microscopy in living cells. Integr. Biol. 3, 675-683
29. Thompson, J. R., Cronin, B., Bayley, H., and Wallace, M. I. (2011) Rapid assembly of a multimeric membrane protein pore. Biophys. J. 101, 2679-2683
30. Anderluh, A., Klotzsch, E., Reismann, A. W., Brameshuber, M., Kudlacek, O., Newman, A. H., Sitte, H. H., and Schuz, G. J. (2014) Single molecule analysis reveals coexistence of stable serotonin transporter monomers and oligomers in the live cell plasma membrane. J. Biol. Chem. 289, 4387-4394
31. Cocucci, E., Aguet, F., Boulant, S., and Kirchhausen, T. (2012) The first five seconds in the life of a clathrin-coated pit. Cell 150, 495-507
32. Xia, T., Li, N., and Fang, X. (2013) Single-molecule fluorescence imaging in living cells. Annu. Rev. Phys. Chem. 64, 459-480
33. Baker, M. A., Rojko, N., Cronin, B., Anderluh, G., and Wallace, M. I. (2014) Photobleaching reveals heterogeneous stoichiometry for equinatoxin II oligomers. ChemBioChem 15, 2139-2145
34. Wieser, S., and Schuz, G. J. (2008) Tracking single molecules in the live cell plasma membrane: do's and don't's. Methods 46, 131-140
35. Garc-Ortega, L., Alegre-Cebollada, J., Garc-Linares, S., Bruix, M., Martez-Del-Pozo, A., and Gavilanes, J. G. (2011) The behavior of sea anemone actinoporins at the water-membrane interface. Biochim. Biophys. Acta 1808, 2275-2288
36. Landeta, O., Landajuela, A., Gil, D., Taneva, S., Di Primo, C., Sot, B., Valle, M., Frolov, V. A., and Basañez, G. (2011) Reconstitution of proapoptotic BAK function in liposomes reveals a dual role for mitochondrial lipids in the BAK-driven membrane permeabilization process. J. Biol. Chem. 286, 8213-8230
37. Sackmann, E. (2014) Endoplasmatic reticulum shaping by generic mechanisms and protein-induced spontaneous curvature. Adv. Colloid Interface Sci. 208, 153-160
38. Chappie, J. S., and Dyda, F. (2013) Building a fission machine: structural insights into dynamin assembly and activation. J. Cell Sci. 126, 2773-2784
39. Antonini, V., Peez-Barzaga, V., Bampi, S., Pento, D., Martez, D., Dalla Serra, M., and Tejuca, M. (2014) Functional characterization of sticholysin I and W111C mutant reveals the sequence of the actinoporin's pore assembly. PloS One 9, e110824
40. Fuertes, G., Gimeez, D., Esteban-Mart, S., Sachez-Muñoz, O. L., and Salgado, J. (2011) A lipocentric view of peptide-induced pores. Eur. Biophys. J. 40, 399-415
41. 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
42. Basañez, G., Sharpe, J. C., Galanis, J., Brandt, T. B., Hardwick, J. M., and Zimmerberg, J. (2002) Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J. Biol. Chem. 277, 49360-49365
43. Qian, S., Wang, W., Yang, L., and Huang, H. W. (2008) Structure of transmembrane pore induced by Bax-derived peptide: evidence for lipidic pores. Proc. Natl. Acad. Sci. U.S.A. 105, 17379-17383
44. Bleicken, S., Landeta, O., Landajuela, A., Basan?z, G., and Garc?-Sa?z, A. J. (2013) Proapoptotic Bax and Bak proteins form stable protein-permeable pores of tunable size. J. Biol. Chem. 288, 33241-33252
45. Valle, A., Lopez-Castilla, A., Pedrera, L., Martinez, D., Tejuca, M., Campos, J., Fando, R., Lissi, E., Alvarez, C., Lanio, M. E., Pazos, F., and Schreier, S. (2011) Cys mutants in functional regions of Sticholysin I clarify the participation of these residues in pore formation. Toxicon 58, 8-17