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

Volumn 7, Issue 3, 1999, Pages 277-287

  Pédelacq, Jean Denis ^a   Maveyraud, Laurent ^a   Prévost, Gilles ^b   Baba Moussa, Lamine ^b   González, Ana ^c   Courcelle, Emmanuel ^a   Shepard, William ^d   Monteil, Henri ^b   Samama, Jean Pierre ^a   Mourey, Lionel ^a  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Bi component leucotoxins; Crystal structure; LukF PV; MAD; Transmembrane pore

Indexed keywords

HEMOLYSIN; LEUKOCIDIN; STAPHYLOCOCCUS TOXIN;

ARTICLE; CRYSTAL STRUCTURE; HEMOLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; STAPHYLOCOCCUS AUREUS; TOXIN STRUCTURE;

EID: 0033103175     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(99)80038-0     Document Type: Article

References (53)

1. Woodin, A.M. (1960). Purification of the two components of leucocidin from staphylococcus aureus. Biochem. J. 75, 158-165.
2. Cooney, J., Kienle, Z., Foster, T.J. & O'Toole, P.W. (1993). The gamma-hemolysin locus of staphylococcus aureus comprises three linked genes, two of which are identical to the genes for the F and S components of leukocidin. Infect. Immun. 61, 768-771.
3. Prévost, G., & Piémont, Y., Et Al. (1995). Panton-Valentine leucocidin and gamma-hemolysin from staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect. Immun. 63, 4121-4129.
4. Prévost, G., Bouakham, T., Piémont, Y. & Monteil, H. (1995). Characterisation of a synergohymenotropic toxin produced by staphylococcus intermedius. FEBS Lett. 376, 135-140.
5. Sugawara, N., Tomita, T. & Kamio, Y. (1997). Assembly of staphylococcus aureus γ-hemolysin into a pore-forming ring-shaped complex on the surface of human erythrocytes. FEBS Lett. 410, 333-337.
6. Kaneko, J., Muramoto, K. & Kamio, Y. (1997). Gene of LukF-PV-like component of panton-Valentine leukocidin in staphylococcus aureus P83 is linked with lukm. Biosci. Biotech. Biochem. 61, 541-544.
7. Tomita, T. & Kamio, Y. (1997). Molecular biology of the pore-forming cytolysins from staphylococcus aureus, α-and γ-hemolysins and leukocidin. Biosci. Biotech. Biochem. 61, 565-572.
8. Finck-Barbançon, V., Duportail, G., Meunier, O. & Colin, D.A. (1993). Pore formation by a two-component leukocidin from staphylococcus aureus within the membrane of human polymorphonuclear leukocytes. Biochim. Biophys. Acta 1182, 275-282.
9. Rahman, A., Izaki, K. & Kamio, Y. (1993). Gamma-hemolysin genes in the same family with lukF and lukS genes in methicillin resistant staphylococcus aureus. Biosci. Biotech. Biochem. 57, 1234-1236.
10. Supersac, G., Prévost, G. & Piémont, Y. (1993). Sequencing of leucocidin R from staphylococcus aureus P83 suggests that staphylococcal leucocidins and gamma-hemolysin are members of a single, two-component family of toxins. Infect. Immun. 61, 580-587.
11. Gravet, A., Colin, D.A., Keller, D., Girardot, R., Monteil, H. & Prévost, G. (1998). Characterization of a novel member, LukE-LukD, of the bi- Component staphylococcal leucotoxins family. FEBS Lett. 436, 202-208.
12. Panton, P.N. & Valentine, F.C.O. (1932). Staphylococcal toxin. Lancet 222, 506-508.
13. Finck-Barbançon, V., Prévost, G. & Piémont, Y. (1991 ). Improved purification of leukocidin from Staphylococcus aureus and toxin distribution among hospital strains. Res. Microbiol. 142, 75-85.
14. Cribier, B., Prévost, G., Couppié, P., Finck-Barbançon, V., Grosshans, E. & Piémont, Y. (1992). Staphylococcus aureus leukocidin: A new virulence factor in cutaneous infections? An epidemiological and experimental study. Dermatology 185, 175-180.
15. Couppié, P., Cribier, B. & Prévost, G. (1994). Leukocidin from Staphylococcus aureus and cutaneous infections: An epidemiologic study. Arch. Dermatol. 130, 1208-1209.
16. Colin, D.A., Mazurier, I., Sire, S. & Finck-Barbançon, V. (1994). Interaction of the two components of leukocidin from Staphylococcus aureus with human polymorphonuclear leukocyte membranes: Sequential binding and subsequent activation. Infect. Immun, 62, 3184-3188.
17. Woodin, A.M. & Wieneke, A.A. (1968). The cation-sensitive phosphatases of the leucocyte cell membrane. Biochem. Biophys. Res. Commun. 33, 558-562.
18. 125i- Labeled S and F components of leucocidin to rabbit polymorphonuclear leukocytes and leucocidin activity. Infect. Immun. 34, 362-367.
19. Meunier, O., Falkenrodt, A., Monteil, H. & Colin, D.A. (1995). Application of flow cytometry in toxinology: Pathophysiology of human polymorphonuclear leukocytes damaged by a pore-forming toxin from staphylococcus aureus. Cytometry 21, 241-247.
20. König, B., Prévost, G., Piémont, Y. & König, W. (1995). Effects of Staphylococcus aureus leukocidins on inflammatory mediator release from human granulocytes. J. Infect. Dis. 171, 607-613.
21. 2+ channels in the membrane of human polymorphonuclear neutrophils. J. Membr. Biol. 162, 209-216.
22. Ferreras, M., Höper, F., Serra, M.D., Colin, D.A., Prévost, G. & 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.
23. Song, L., Hobaugh, M.R., Shustak, C., Cheley, S., Bayley, H. & Gouaux, J.E. (1996). Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1866.
24. Füssle, R., Bhakdi, S., Sziegoleit, A., Tranum-Jensen, J., Kranz, T. & Wellensiek, H.J. (1981). On the mechanism of membrane damage by Staphylococcus aureus α-toxin. J. Cell Biol. 91, 83-94.
25. Gouaux, J.E., & Bayley, H., Et Al (1994). Subunit stoichiometry of staphylococcal α-hemolysin in crystals and on membranes: A heptameric transmembrane pore. Proc. Natl Acad. Sci. USA 91, 12828-12831.
26. Gouaux, E., Hobaugh, M. & Song, L. (1997). α-hemolysin, γ-hemolysin, and leukocidin from Staphylococcus aureus: Distant in sequence but similar in structure. Protein Sci. 12, 2631-2635.
27. Richardson, J.S. (1981). The anatomy and taxonomy of protein structure. Adv. Protein Chem. 34, 167-339.
28. Ward, R.J., Palmer, M., Leonard, K. & Bhakdi, S. (1994). Identification of a putative membrane-inserted segment in the α-toxin of staphylococcus aureus. Biochemistry 33, 7477-7484.
29. Valeva, A., Palmer, M., Hilgert, K., Kehoe, M. & 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.
30. Walker, B., Krishnasastry, M., Zorn, L. & Bayley, H. (1992). Assembly of the oligomeric membrane pore formed by staphylococcal α-hemolysin examined by truncation mutagenesis. J. Biol. Chem. 267, 21782-21786.
31. Valeva, A., Palmer, M. & Bhakdi, S. (1997). Staphylococcal α-toxin: Formation of the heptameric pore is partially cooperative and proceeds through multiple intermediate stages. Biochemistry 36, 13298-13304.
32. Vécsey-Semjén, B., Lesieur, C., Möllby, R. & van Der Goot, F.G. (1997). Conformational changes due to membrane binding and channel formation by staphylococcal α-toxin. J. Biol. Chem 272, 5709-5717.
33. Holm, L. & Sander, C. (1993). Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
34. Kleywegt, G.J. & Jones, T.A. (1994). Halloween. . . Masks and bones. In model (Bailey, S., Hubbard, R. & Waller, D., eds), pp. 59-66, SERC, Daresbury Laboratory, Warrington, UK.
35. Corfield, P.W., Lee, T.J. & Low, B.W. (1989). The crystal structure of erabutoxin a at 2.0-å resolution. J. Biol. Chem. 264, 9239-9242.
36. Bilwes, A., Rees, B., Moras, D., Ménez, R. & Ménez, A. (1994). X-ray structure at 1.55 Å of toxin γ, a cardiotoxin from Naja nigricollis venom. Crystal packing reveals a model for insertion into membranes. J. Mol. Biol. 239, 122-136.
37. Rees, B. & Bilwes, A. (1993). Three-dimensional structures of neurotoxins and cardiotoxins. Chem. Res. Toxicol. 6, 385-406.
38. Gouaux, E. (1998). α-Hemolysin from Staphylococcus aureus: An archetype of β-barrel, channel-forming toxins. J. Struct. Biol. 121, 110-122.
39. Cheley, S., & Bayley, H., Et Al. (1997). Spontaneous oligomerization of a staphylococcal α-hemolysin conformationally constrained by remova of residues that form the transmembrane β-barrel. Protein Eng. 10, 1433-1443.
40. Murzin, A.G., Lesk, A.M. & Chothia, C. (1994). Principles determining the structure of β-sheet barrels in proteins. I. A theoretical analysis. J. Mol. Biol. 236, 1369-1381.
41. Sansom, M.S. & Kerr, I.D. (1995). Transbilayer pores formed by β- Barrels: Molecular modeling of pore structures and properties. Biophys. J. 69, 1334-1343.
42. Colin, D.A., Meunier, O., Staali, L., Prévost, G. & Monteil, H. (1997). Bi-component leukotoxins from Staphylococcus aureus. In Cold Spring Harbor Laboratory on Microbial Pathogenesis and Host Response. (Maloy, S., Taylor, R.K. & Magee, P.T., eds), pp. 150, Cold Spring Harbor, New York.
43. Czajkowsky, D.M., Sheng, S. & Shao, Z. (1998). Staphylococcal α-hemolysin can form hexamers in phospholipid bilayers. J. Mol. Biol. 276, 325-330.
44. Otwinowski, Z. (1993). Oscillation data reduction program. In processing. (Sawyer, L., Isaccs, N. & Bailey, S., eds), pp. 56-62, SERC, Daresbury Laboratory, Warrington, UK.
45. Collaborative Computational Project No. 4. (1994). The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D 50, 760-763.
46. de La Fortelle, É. & Bricogne, G. (1997). Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472-494.
47. 1 ATPase. Acta Crystallogr. D 52, 30-42.
48. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240-255.
49. Brünger, A.T. (1992). X-PLOR Version 3.1. A System for X-ray Crystallography and NMR. Yale University Press, New Haven, CT.
50. Roussel, A. & Cambillau, C. (1989). TURBO-FRODO. In Silicon Graphics Geometry Partner Directory, Pp. 71-78, Silicon Graphics, Mountain View, CA.
51. Brünger, A.T. (1992). The free R value: A novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475.
52. Kraulis, P.J. (1991). MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
53. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637.