A molecular pin to study the dynamics of β-barrel formation in pore-forming toxins on erythrocytes: A sliding model

Cellular and Molecular Life Sciences

Volumn 65, Issue 2, 2008, Pages 312-323

  Viero, G ^a   Gropuzzo, A ^a   Joubert, O ^b,c   Keller, D ^b   Prevost G ^b   Dalla Serra, M ^a  

^a FONDAZIONE BRUNO KESSLER   (Italy)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c CNRS   (France)

Author keywords

barrel; Hemolysin; Membrane protein; Pore forming toxin; Protein motion

Indexed keywords

CYSTEINE; HEMOLYSIN;

ARTICLE; CHANNEL GATING; DYNAMICS; ERYTHROCYTE; GENE INSERTION; GENE MUTATION; PROTEIN CONFORMATION; PROTEIN FOLDING; TEMPERATURE DEPENDENCE;

ANIMALS; CYSTEINE; DISULFIDES; ELECTROPHYSIOLOGY; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; HEMOLYSIN PROTEINS; HEMOLYSIS; HUMANS; KINETICS; MEMBRANES, ARTIFICIAL; MODELS, BIOLOGICAL; MUTANT PROTEINS; MUTATION; OXIDATION-REDUCTION; PROTEIN STRUCTURE, SECONDARY; RABBITS; TEMPERATURE; TIME FACTORS;

EID: 38549109639     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-007-7491-2     Document Type: Article

References (46)

1. Parker, M. W. and Feil, S. C. (2005) Pore-forming protein toxins: from structure to function. Prog. Biophys. Mol. Biol. 88, 91-142.
2. Olson, R., Nariya, H., Yokota, K., Kamio, Y. and Gouaux, J. E. (1999) Crystal structure of staphylococcal LukF delineates conformational changes accompanying formation of transmembrane channel. Nat. Struct. Biol. 6, 134-140.
3. Pédelacq, J. D., Maveyraud, L., Prévost, G., Baba-Moussa, L., Gonzalez, A., Courcelle, E., Shepard, W., Monteil, H., Samama, J. P. and Mourey, L. (1999) The structure of a Staphylococcus aureus leucocidin component (LukF-PV) reveals the fold of the water-soluble species of a family of transmembrane pore-forming toxins. Structure 7, 277-287.
4. Guillet, V., Roblin, P., Werner, S., Coraiola, M., Menestrina, G., Monteil, H., Prévost, G. and Mourey, L. (2004) Crystal structure of leucotoxin S component: new insight into the staphylococcal beta-barrel pore-forming toxins. J. Biol. Chem. 279, 41028-41037.
5. Song, L., Hobaugh, M. R., Shustak, C., Cheley, S., Bayley, H. and Gouaux, J. E. (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1866.
6. Menestrina, G., Dalla Serra, M., Comai, M., Coraiola, M., Viero, G., Werner, S., Colin, D. A., Monteil, H. and Prévost, G. (2003) Ion channels and bacterial infection: the case of beta-barrel pore-forming protein toxins of Staphylococcus aureus. FEBS Lett. 552, 54-60.
7. Gouaux, J. E., Hobaugh, M. and Song, L. Z. (1997) Alpha-hemolysin, gamma-hemolysin, and leukocidin from Staphylococcus aureus: distant in sequence but similar in structure. Protein Sci. 6, 2631-2635.
8. Miles, G., Movileanu, L. and Bayley, H. (2002) Subunit composition of a bicomponent toxin: staphylococcal leukocidin forms an octameric transmembrane pore. Protein Sci. 11, 894-902.
9. Jayasinghe, L. and Bayley, H. (2005) The leukocidin pore: evidence for an octamer with four LukF subunits and four LukS subunits alternating around a central axis. Protein Sci. 14, 2550-2561.
10. Viero, G., Cunaccia, R., Keller, D., Werner, S., Monteil, H., Prévost, G., Menestrina, G. and Dalla Serra, M. (2006) Homologous versus heterologous interactions in the pore of bicomponent staphylococcal γ-hemolysins. Biochem. J. 394, 217-225.
11. Joubert, O., Viero, G., Keller, D., Martinez, E., Colin, D. A., Monteil, H., Mourey, L., Dalla Serra, M. and Prévost, G. (2006) Engineered covalent leucotoxin heterodimers form functional pores: insights into S-F interactions Biochem. J. 396, 381-389.
12. Joubert, O., Voegelin, J., Guillet, V., Tranier, S., Werner, S., Colin, D. A., Dalla Serra, M., Keller, D., Monteil, H., Mourey, L. and Prévost, G. (2007) Distinction between pore assembly by staphylococcal α-toxin versus leucotoxins. J. Biomed. Biotechnol. ID 25935 1-13.
13. Hotze, E. M., Wilson-Kubalek, E. M., Rossjohn, J., Parker, M. W., Johnson, A. E. and Tweten, R. K. (2001) Arresting pore formation of a cholesterol-dependent cytolysin by disulfide trapping synchronizes the insertion of the transmembrane beta-sheet from a prepore intermediate. J. Biol. Chem. 276, 8261-8268.
14. Valeva, A., Palmer, M., and Bhakdi, S. (1997) Staphylococcal alpha-toxin: formation of the heptameric pore is partially cooperative and proceeds through multiple intermediate stages. Biochemistry 36, 13298-13304.
15. Nguyen, A. H., Nguyen, V. T., Kamio, Y. and Higuchi, H. (2006) Single-molecule visualization of environment-sensitive fluorophores inserted into cell membranes by staphylococcal gamma-hemolysin. Biochemistry 45, 2570-2576.
16. Valeva, A., Palmer, M., Hilgert, K., Kehoe, M. and Bhakdi, S. (1995) Correct oligomerization is a prerequisite for insertion of the central molecular domain of staphylococcal alpha-toxin into the lipid-bilayer. Biochim. Biophys. Acta 1236, 213-218.
17. Vecsey-Semjen, B., Knapp, S., Mollby, R. and van der Goot, F. G. (1999) The staphylococcal alpha-toxin pore has a flexible conformation. Biochemistry 38, 4296-4302.
18. Kawate, T. and Gouaux, E. (2003) Arresting and releasing Staphylococcal alpha-hemolysin at intermediate stages of pore formation by engineered disulfide bonds. Protein Sci. 12, 997-1006.
19. Nguyen, V. T., Higuchi, H. and Kamio, Y. (2002) Controlling pore assembly of staphylococcal gamma-haemolysin by low temperature and by disulphide bond formation in double-cysteine LukF mutants. Mol. Microbiol. 45, 1485-1498.
20. Chattopadhyay, K. and Banerjee, K. K. (2003) Unfolding of Vibrio cholerae hemolysin induces oligomerization of the toxin monomer. J. Biol. Chem. 278, 38470-38475.
21. Kristan, K., Podlesek, Z., Hojnik, V., Gutierrez-Aguirre, I., Guncar, G., Turk, D., Gonzalez-Manas, 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 beta-sandwich. J. Biol. Chem. 279, 46509-46517.
22. 2+-activation from the pore-forming function of the bi-component Panton-Valentine leucocidin in human PMNs. FEBS Lett., 461, 280-286.
23. Werner, S., Colin, D. A., Coraiola, M., Menestrina, G., Monteil, H. and Prévost, G. (2002) Retrieving biological activity from LukF-PV mutants combined with different S-components implies compatibility between stem domains of these staphylococcal bi-component leucotoxins. Infect. Immun. 70, 1310-1318.
24. Ferreras, M., Hoeper, F., Dalla Serra, M., Colin, D. A., Prévost, G. and Menestrina, G. (1998) The interaction of Staphylococcus aureus bi-component gamma hemolysins and leucocidins with cells and model membranes. Biochim. Biophys. Acta 1414, 108-126.
25. Loo, T. W., Bartlett, M. C. and Clarke, D. M. (2004) Disulfide cross-linking analysis shows that transmembrane segments 5 and 8 of human P-glycoprotein are close together on the cytoplasmic side of the membrane. J. Biol. Chem. 279, 7692-7697.
26. Alvarez, C., Dalla Serra, M., Potrich, C., Bernhart, I., Tejuca, M., Martinez, D., Pazos, I. 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.
27. Dalla Serra, M. and Menestrina, G. (2000) Characterisation of molecular properties of pore-forming toxins with planar lipid bilayers. In: Holst, O. (ed.), Bacterial Toxins, Methods and Protocols, pp. 171-188, Humana Press, Totowa, NJ.
28. Gerstein, M., Lesk, A. M. and Chothia, C. (1994) Structural mechanisms for domain movements in proteins. Biochemistry 33, 6739-6749.
29. Gerstein, M. and Chothia, C. (1999): Signal transduction: proteins in motion. Science 285, 1682-1683.
30. Katz, B. A. and Kossiakoff, A. (1986) The crystallographically determined structures of atypical strained disulfides engineered into subtilisin. J. Biol. Chem. 261, 15480-15485.
31. Comai, M., Dalla Serra, M., Coraiola, M., Werner, S., Colin, D. A., Prévost, G. and Menestrina, G. (2002) Protein engineering modulates the transport properties and ion selectivity of the pores formed by staphylococcal gamma-hemolysins in lipid membranes. Mol. Microbiol. 44, 1251-1268.
32. Menestrina, G. (1986) Ionic channels formed by Staphylococcus aureus alpha-toxin: voltage dependent inhibition by di- and trivalent cations. J. Membr. Biol. 90, 177-190.
33. Galdiero, S. and Gouaux, E. (2004) High resolution crystallographic studies of alpha-hemolysin-phospholipid complexes define heptamer-lipid head group interactions: implication for understanding protein-lipid interactions. Protein Sci. 13, 1503-1511.
34. Iacovache, I., Paumard, P., Scheib, H., Lesieur, C., Sakai, N., Matile, S., Parker, M. W. and van der Goot, F. G. (2006) A rivet model for channel formation by aerolysin-like pore-forming toxins EMBO J. 25, 457-466.
35. Wimley, W. C., Hristova, K., Ladokhin, A. S., Silvestro, L., Axelsen, P. H. and White, S. H. (1998) Folding of beta-sheet membrane proteins: a hydrophobic hexapeptide model. J. Mol. Biol. 277, 1091-1110.
36. Bishop, C. R., Walkenhorst, W. F. and Wimley, W. C. (2001) Folding of beta-sheets in membranes: specificity and promiscuity in peptide model systems. J. Mol. Biol. 309, 975-988.
37. Tamm, L. K., Hong, H. and Liang, B. (2004) Folding and assembly of beta-barrel membrane proteins. Biochim. Biophys. Acta 1666, 250-263.
38. Hotze, E. M., Heuck, A. P., Czajkowsky, D. M., Shao, Z., Johnson, A. E. and Tweten, R. K. (2002) Monomer-monomer interactions drive the prepore to pore conversion of a beta-barrel-forming cholesterol-dependent cytolysin. J. Biol. Chem. 277, 11597-11605.
39. Vécsey-Semjén, B., Lesieur, S., Mollby, R. and van der Goot, F. G. (1997) Conformational changes due to membrane binding and channel formation by staphylococcal alpha-toxin. J. Biol. Chem. 272, 5709-5717.
40. Valeva, A., Weisser, A., Walker, B., Kehoe, M., Bayley, H., Bhakdi, S. and Palmer, M. (1996) Molecular architecture of a toxin pore: a 15-residue sequence lines the transmembrane channel of staphylococcal alpha-toxin. EMBO J. 15, 1857-1864.
41. Qa'dan, M., Christensen, K. A., Zhang, L., Roberts, T. M. and Collier, R. J. (2005) Membrane insertion by anthrax protective antigen in cultured cells. Mol. Cell. Biol. 25, 5492-5498.
42. Tilley, S. J. and Saibil, H. R. (2006) The mechanism of pore formation by bacterial toxins. Curr. Opin. Struct. Biol. 16, 230-236.
43. Benson, E. L., Huynh, P. D., Finkelstein, A. and Collier, R. J. (1998) Identification of residues lining the anthrax protective antigen channel. Biochemistry 37, 3941-3948.
44. Olson, R. and Gouaux, E. (2005) Crystal structure of the Vibrio cholerae cytolysin (VCC) pro-toxin and its assembly into a heptameric transmembrane pore. J. Mol. Biol. 350, 997-1016.
45. Loo, T. W., Bartlett, M. C. and Clarke, D. M. (2003) Substrate-induced conformational changes in the transmembrane segments of human P-glycoprotein. Direct evidence for the substrate-induced fit mechanism for drug binding. J. Biol. Chem. 278, 13603-13606.
46. Loo, T. W. and Clarke, D. M. (2000) The packing of the transmembrane segments of human multidrug resistance P-glycoprotein is revealed by disulfide cross-linking analysis, J. Biol. Chem. 275, 5253-5256.