High resolution crystallographic studies of α-hemolysin-phospholipid complexes define heptamer-lipid head group interactions: Implication for understanding protein-lipid interactions

Protein Science

Volumn 13, Issue 6, 2004, Pages 1503-1511

  Galdiero, Stefania ^a,b   Gouaux, Eric ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Integral membrane protein; Pore forming toxin; Protein membrane interactions

Indexed keywords

ALPHA HEMOLYSIN; AMMONIUM DERIVATIVE; ARGININE; BACTERIAL PROTEIN; DIPROPANOYLGLYCEROPHOSPHOCHOLINE; GLYCEROPHOSPHORYLCHOLINE; HEMOLYSIN; LIPID; PHOSPHOLIPID; PHOSPHORYLCHOLINE; PORE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CHANNEL GATING; COMPLEX FORMATION; CRYSTALLOGRAPHY; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LIPID INTERACTION; PROTEIN SECRETION; SOLUBILITY; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; BACTERIAL TOXINS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; HEMOLYSIN PROTEINS; MODELS, MOLECULAR; PHOSPHOLIPIDS; PROTEIN CONFORMATION; SENSITIVITY AND SPECIFICITY; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 2442650172     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.03561104     Document Type: Article

References (41)

1. Bayley, H. and Cremer, P.S. 2001. Stochastic sensors inspired by biology. Nature 413: 226-230.
2. Bhakdi, S. and Tranum-Jensen, J. 1991. S. aureus α-toxin. Microbiol. Rev. 55: 733-751.
3. Bhakdi, S., Fussle, R., and Tranum-Jensen, J. 1981. Staphylococcal α-toxin: Oligomerization of hydrophilic monomers to form amphiphilic hexamers induced through contact with deoxycholate micelles. Proc. Natl. Acad. Sci. 78: 5475-5479.
4. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kusrewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54: 905-921.
5. Chattopadhyay, A. and McNamee, M.G. 1991. Average membrane penetration depth of tryptophan residues of the nicotinic acetylcholine receptor by the parallax method. Biochemistry 30, 29: 7159-7164.
6. Collaborative Computational Project Number 4. 1994. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D 50: 760-763.
7. Ferguson, A.D., Welte, W., Hofmann, E., Lindner, B., Holst, O., Coulton, J.W., and Diederichs, K. 2000a. A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure Fold. Des. 8: 585-592.
8. Ferguson, A.D., Braun, V., Fiedler, H.P., Coulton, J.W., Diederichs, K., and Welte, W. 2000b. Crystal structure of the antibiotic albomycin in complex with the outer membrane transporter FhuA. Protein Sci. 5: 956-963.
9. Ferreras, M., Hoper, F., Dalla Serra, M., Colin, D.A., Prevost, G., and Menestrina, G. 1998. The interaction of Staphylococcus aureus bi-component γ-hemolysins and leucocidins with cells and lipid membranes. Biochim. Biophys. Acta 1414: 108-126.
10. Fyfe, P.K., McAuley, K.E., Roszak, A.W., Isaacs, N.W., Cogdell, R.J., and Jones, M.R. 2001. Probing the interface between membrane proteins and membrane lipids by X-ray crystallography. Trends Biochem. Sci. 26: 106-112.
11. Gennis, R. 1989. Biomembranes. Springer-Verlag, New York.
12. Gouaux, E. 1998. α-Hemolysin from S. aureus: An archetype of β-barrel, channel forming toxin. J. Struct. Biol. 121: 110-122.
13. Gu, L.Q., Braha, O., Conlan, S., Cheley, S., and Bayley, H. 1999. Stochastic sensing of organic analytes by a pore-forming protein containing a molecular adapter. Nature 398: 686-690.
14. Gu, L.Q., Cheley, S., and Bayley, H. 2001. Capture of a single molecule in a nanocavity. Science 291: 636-640.
15. Hunter, S.E., Brown, J.E., Oyston, P.C., Sakurai, J., and Titball, R.W. 1993. Molecular genetic analysis of β-toxin of Clostridium perfringens reveals sequence homology with α-toxin, γ-toxin, and leukocidin of Staphylococcus aureus. Infect. Immunol. 61: 3958-3965.
16. Jacobs, R.E. and White, S.H. 1989. The nature of the hydrophobic binding of small peptides at the bilayer interface: Implications for the insertion of transbilayer helices. Biochemistry 28: 3421-3437.
17. Jones, T.A., Cowan, S., Zou, J.-Y., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
18. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
19. Luecke, H., Schobart, B., Richter, H.T., Cartailler, P., and Lanyi, J.K. 1999. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291: 899-911.
20. McAuley, K.E., Fyfe, P.K., Ridge, J.P., Isaacs, N.W., Cogdell, R.J., and Jones, M.R. 1999. Structural details of an interaction between cardiolipin and an integral membrane protein. Proc. Natl. Acad. Sci. 95: 14706-14711.
21. Menestrina, G., Serra, M.D., and Prevost, G. 2001. Mode of action of β-barrel pore-forming toxins of the staphylococcal α-hemolysin family. Toxicon 39: 1661-1672.
22. Olson, R. and Gouaux, J. 2003. Vibrio cholerae cytolysin is composed of an α-hemolysin-like core. Protein Sci. 12: 379-383.
23. Olson, R., Nariya, H., Yokota, K., Kamio, Y., and Gouaux, E. 1999. Crystal structure of staphylococcal lukF delineates conformational changes accompanying formation of a transmembrane channel. Nature Struct. Biol. 6: 134-140.
24. Pédelacq, J.D., Maveyraud, L., Prevost, 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 Fold. Des. 7: 277-287.
25. Petosa, C., Collier, R.J., Klimpel, K.R., Leppla, S.H., and Liddington, R.C. 1997. Crystal structure of the anthrax toxin protective antigen. Nature 385: 833-838.
26. Rossjohn, J., Feil, S.C., McKinstry, W.J., Tsernoglou, D., van der Goot, G., Buckley, J.T., and Parker, M.W. 1998a. Aerolysin - A paradigm for membrane insertion of β-sheet protein toxins. J. Struct. Biol. 121: 92-100.
27. Rossjohn, J., Raja, S.M., Nelson, K.L., Feil, S.C., van der Goot, F.G., Parker, M.W., and Buckley, J.T. 1998b. Movement of a loop in domain 3 of aerolysin is required for channel formation. Biochemistry 37: 741-746.
28. Roth, M., Arnoux, B., Ducruix, A., and Reiss-Husson, F. 1991. Structure of the detergent phase and protein-detergent interactions in crystals of the wild-type (strain-Y) Rhodobacter sphaeroides photochemical reaction center. Biochemistry 30: 9403-9413.
29. Satow, Y., Cohen, G.H., Padlan, E.A., and Davies, D.V. 1986. Phosphocholine binding immunoglobulin Fab McPC603. An X-ray diffraction study at 2.7 Å. J. Mol. Biol. 190: 593-596.
30. Song, L., Hohaugh, M.R., Shustak, C., Cheley, S., Bayley, H., and Gouaux, J.E. 1996. Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 274: 1859-1865.
31. Tomita, T. and Kamio, Y. 1997. Molecular biology of the pore-forming cytolysins from Staphylococcus aureus, α- and γ-hemolysins and leukocidin. Biosci. Biotechnol. Biochem. 61: 565-572.
32. Tsukihara, T. and Yoshikawa, S. 1998. Crystal structural studies of a membrane protein complex, cytochrome c oxidase from bovine heart. Acta Crystallogr. A 54: 895-904.
33. Valeva, A., Weisse, 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 α-toxin. EMBO J. 15: 1857-1864.
34. Valeva, A., Palmer, M., and Bhakdi, S. 1997a. Staphylococcal α-toxin: Formation of the heptameric pore is partially cooperative and proceeds through multiple intermediate stages. Biochemistry 36: 13298-13304.
35. Valeva, A., Pongs, J., Bhakdi, S., and Palmer, M. 1997b. Staphylococcal α-toxin: The role of the N-terminus in formation of the heptameric pore - a fluorescence study. Biochim. Biophys. Acta 1325: 281-286.
36. Valiyaveetil, F.I., Zhou, Y., and Mackinnon, R. 2002. Lipids in the structure, folding and function of the KcsA K+channel. Biochemistry 41: 10771-10777.
37. Wah, D.A., Fernandez-Tomero, C., Sanz, L., Romero, A., and Calvete, J.J. 2002. Sperm coating mechanism from the 1.8 Å crystal structure of PDC-109-Phosphorylcholine complex. Structure 10: 505-514.
38. Walker, B. and Bayley, H. 1995. Key residues for membrane binding, oligomerization, and pore-forming activity of staphylococcal α-hemolysin identified by cysteine scanning mutagenesis and targeted chemical modification. J. Biol. Chem. 270: 23065-23071.
39. Walker, B., Braha, O., Cheley, S., and Bayley, H. 1995. An intermediate in the assembly of a pore-forming protein trapped with a genetically-engineered switch. Chem. Biol. 2: 99-105.
40. Watanabe, M., Tomita, T., and Yasuda, T. 1987. Membrane-damaging action of staphylococcal α-toxin on phospholipid-cholesterol liposomes. Biochim. Biophys. Acta 898: 257-65.
41. Zitzer, A., Walev, I., Palmer, M., and Bhakdi, S. 1995. Characterization of Vibrio cholerae El Tor cytolysin as an oligomerizing pore-forming toxin. Med. Microbiol. Immunol. 184: 37-44.