The leukocidin pore: Evidence for an octamer with four LukF subunits and four LukS subunits alternating around a central axis

Protein Science

Volumn 14, Issue 10, 2005, Pages 2550-2561

  Jayasinghe, Lakmal ^a   Bayley, Hagan ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

barrel; Chemical cross linking; Concatameric subunits; Leukocidin; Pore forming toxin; Staphylococcal hemolysin; Subunit arrangement; Subunit stoichiometry

Indexed keywords

LEUKOCIDIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN SUBUNIT;

ARTICLE; BETA CHAIN; CHANNEL GATING; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN ENGINEERING; PROTEIN FAMILY; PROTEIN STRUCTURE; STOICHIOMETRY; STRUCTURE ANALYSIS;

BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL MEMBRANE; HEMOLYSIN PROTEINS; LEUKOCIDINS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN ENGINEERING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; RECOMBINANT FUSION PROTEINS; STAPHYLOCOCCUS AUREUS;

EID: 25844526536     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.051648505     Document Type: Article

References (64)

1. Alouf, J.E. and Freer, J.H. 1999. The comprehensive sourcebook of bacterial protein toxins. Academic Press, New York.
2. Baida, G., Budarina, Z.I., Kuzmin, N.P., and Solonin, A.S. 1999. Complete nucleotide sequence and molecular characterization of hemolysin II gene from Bacillus cereus. FEMS Microbiol. Lett. 180: 7-14.
3. Bayley, H. and Cremer, P.S. 2001. Stochastic sensors inspired by biology. Nature 413: 226-230.
4. Bayley, H. and Jayasinghe, L. 2004. Functional engineered channels and pores. Mol. Membrane Biol. 21: 209-220.
5. Betanzos, M., Chiang, C.-S., Guy, H.R., and Sukharev, S. 2002. A large iris-like expansion of a mechanosensitive channel protein induced by membrane tension. Nature Struct. Biol. 9: 704-710.
6. Bhakdi, S., Walev, I., Palmer, M., and Valeva, A. 2000. Staphylococcal a toxin. In Bacterial protein toxins (eds. K. Aktories and I. Just), pp. 509-527. Springer, Berlin.
7. Bhattacharjee, H. and Rosen, B.P. 1996. Spatial proximity of Cys113, Cys172, and Cys422 in the metalloactivation domain of the ArsA ATPase. J.Biol.Chem. 271: 24465-24470.
8. Braha, O., Walker, B., Cheley, S., Kasianowicz, J.J., Song, L., Gouaux, J.E., and Bayley, H. 1997. Designed protein pores as components for biosensors. Chem. Biol. 4: 497-505.
9. Cheley, S., Malghani, M.S., Song, L., Hobaugh, M., Gouaux, J.E., Yang, J., and Bayley, H. 1997. Spontaneous oligomerization of a staphylococcal α-hemolysin conformationally constrained by removal of residues that form the transmembrane β barrel. Protein Eng. 10: 1433-1443.
10. Cheley, S., Braha, O., Lu, X., Conlan, S., and Bayley, H. 1999. A functional protein pore with a "retro" transmembrane domain. Protein Sci. 8: 1257-1267.
11. Cline, D.J., Thorpe, C., and Schneider, J.P. 2003. Effects of As(III) binding on α-helical structure. J. Am. Chem. Soc. 125: 2923-2929.
12. Cooney, J., Mulvey, M., Arbuthnott, J., and Foster, T. 1988. Molecular cloning and genetic analysis of the determinant for γ-lysin, a two component toxin of Staphylococcal aureus. J. Gen. Microbiol. 134: 2179-2188.
13. Cooney, J., Kienle, Z., Foster, T.J., and O'Toole, P.W. 1993. The γ-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.
14. Corrie, J.E.T., Craik, J.S., and Munasinghe, V.R.N. 1998. A homobifunctional rhodamine for labeling proteins with defined orientations of a fluorophore. Bioconjugate Chem. 9: 160-167.
15. Czajkowsky, D.M., Sheng, S., and Shao, Z. 1998. Staphylococcal α-hemolysin can form hexamers in phospholipid bilayers. J. Mol. Biol. 276: 325-330.
16. Donoghue, N., Yam, P.T.W., Jiang, X.-M., and Hogg, P.J. 2000. Presence of closely spaced protein thiols on the surface of mammalian cells. Protein Sci. 9: 2436-2445.
17. Dorigo, B., Schalch, T., Kulangara, A., Duda, S., Schroeder, R.R., and Richmond, T.J. 2004. Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science 306: 1571-1573.
18. Fang, Y., Cheley, S., Bayley, H., and Yang, J. 1997. The heptameric prepore of a staphylococcal α-hemolysin mutant in lipid bilayers imaged by atomic force microscopy. Biochemistry 36: 9518-9522.
19. Ferreras, M., Höper, F., Dalla Serra, M., Colin, D.A., Prévost, 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.
20. Firsov, D., Gautschi, I., Merillat, A.M., Rossier, B.C., and Schild, L. 1998. The heterotetrameric architecture of the epithelial sodium channel (ENaC). EMBO J. 17: 344-352.
21. Gouaux, J.E., Braha, O., Hobaugh, M.R., Song, L., Cheley, S., Shustak, C., and Bayley, H. 1994. Subunit stoichiometry of staphylococcal ahemolysin in crystals and on membranes: A heptameric transmembrane pore. Proc. Natl. Acad. Sci. 91: 12828-12831.
22. Gouaux, E., Hobaugh, M., and Song, L. 1997. α-Hemolysin, γ-hemolysin and leukocidin from Staphylococcus aureus: Distant in sequence but similar in structure. Protein Sci. 6: 2631-2635.
23. Groot-Kormelink, P.J., Broadbent, S.D., Boorman, J.P., and Sivilotti, L.G. 2004. Incomplete incorporation of tandem subunits in recombinant neuronal nicotinic receptors. J. Gen. Physiol. 123: 697-708.
24. Guillet, V., Roblin, P., Werner, S., Coriaola, M., Menestrina, G., Monteil, H., Prévost, G., and Mourey, L. 2004. Crystal structure of leucocidin S component. New insight into the staphylococcal β-barrel pore-forming toxins. J. Biol. Chem. 279: 41028-41037.
25. Hamdan, F.F., Ward, S.D., Siddiqui, N.A., Bloodworth, L.M., and Wess, J. 2002. Use of an in situ disulfide cross-linking strategy to map proximities between amino acid residues in transmembrane domains I and VII of the M3 muscarinic acetylcholine receptor. Biochemistry 41: 7647-7658.
26. Hildebrand, A., Pohl, M., and Bhakdi, S. 1991. Staphylococcus aureus atoxin. Dual mechanism of binding to target cells. J. Biol. Chem. 266: 17195-17200.
27. Howorka, S. and Bayley, H. 1998. Improved protocol for high-throughput cysteine scanning mutagenesis. Biotechniques 25: 766-772.
28. Jiang, W., Hermolin, J., and Fillingame, R.H. 2001. The preferred stoichiometry of c subunits in the rotary motor section of Escherichia coli ATP synthase is 10. Proc. Natl. Acad. Sci. 98: 4966-4971.
29. Jones, D.H. 1995. PCR mutagenesis and recombination in vivo. In PCR primer: A laboratory manual (eds. Dieffenbach C.W. and Dveksler G.S.), pp. 591-601. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. O ATP synthase. J. Biol. Chem. 273: 17178-17185.
31. Kaneko, J. and Kamio, Y. 2004. Bacterial two-component and heteroheptameric pore-forming cytolytic toxins: Structures, pore-forming mechanism, and organization of the genes. Biosci. Biotechnol. Biochem. 68: 981-1003.
32. Kaneko, J., Ozawa, T., Tomita, T., and Kamio, Y. 1997. Sequential binding of staphylococcal γ-hemolysin to human erythrocytes and complex formation of hemolysin on the cell surface. Biosci. Biotech. Biochem. 61: 846-851.
33. Karlin, A. 1993. Structure of nicotinic acetylcholine receptors. Curr. Opinion Neurobiol. 3: 299-309.
34. Kawate, T. and Gouaux, E. 2003. Arresting and releasing staphylococcal α-hemolysin at intermediate stages of pore formation by engineered protein disulfide bonds. Protein Sci. 12: 997-1006.
35. König, B., Prévost, G., and König, W. 1997. Composition of staphylococcal bi-component toxins determines pathophysiological reactions. J. Med. Microbiol. 46: 479-485.
36. Krasilnikov, O.V., Merzlyak, P.G., Yuldasheva, L.N., Rodrigues, C.G., Bhakdi, S., and Valeva, A. 2000. Electrophysiological evidence for heptameric stoichiometry of ion channels formed by Staphylococcus aureus α-toxin in planar lipid bilayers. Mol. Microbiol. 37: 1372-1378.
37. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
38. Lee, G.F., Burrows, G.G., Lebert, M.R., Dutton, D.P., and Hazelbauer, G.L. 1994. Deducing the organization of a transmembrane domain by disulfide crosslinking: The bacterial chemoreceptor Trg. J. Biol. Chem. 269: 29920-29927.
39. Maurer, J.A., Elmore, D.E., Lester, H.A., and Dougherty, D.A. 2000. Comparing and contrasting Escherichia coli and Mycobacterium tuberculosis mechanosensitive channels (MscL). J. Biol. Chem. 275: 22238-22244.
40. Menestrina, G., Dalla Serra, M., and Prévost, G. 2001. Mode of action of β barrel pore-forming toxins of the staphylococcal α-hemolysin family. Toxicon 39: 1661-1672.
41. Miles, G., Cheley, S., Braha, O., and Bayley, H. 2001. The staphylococcal leukocidin bicomponent toxin forms large ionic channels. Biochemistry 40: 8514-8522.
42. Miles, G., Bayley, H., and Cheley, S. 2002a. Properties of Bacillus cereus hemolysin II: A heptameric transmembrane pore. Protein Sci. 11: 1813-1824.
43. Miles, G., Movileanu, L., and Bayley, H. 2002b. Subunit composition of a bicomponent toxin: Staphylococcal leukocidin forms an octameric transmembrane pore. Protein Sci. 11: 894-902.
44. Minier, F. and Sigel, E. 2004. Techniques: Use of concatenated subunits for the study of ligand-gated ion channels. Trends Pharmacol. Sci. 25: 499-503.
45. Montoya, M. and Gouaux, E. 2003. β-Barrel membrane protein folding and structure viewed through the lens of α-hemolysin. Biochim. Biophys. Acta 1609: 19-27.
46. Nguyen, V.T., Kamio, Y., and Higuchi, H. 2003. Single-molecule imaging of cooperative assembly of γ-hemolysin on erythrocyte membranes. EMBO J. 19: 4968-4979.
47. 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. Nat. Struct. Biol. 6: 134-140.
48. Oneto, J.F. 1938. Sulfophenylarsonic acids and certain of their derivatives. I. p-sulfophenylarsonic acid. J. Am. Chem. Soc. 60: 2058-2059.
49. Ozawa, T., Kaneko, J., and Kamio, Y. 1995. Essential binding of LukF of staphylococcal -hemolysin followed by the binding of HII for the hemolysis of human erythrocytes. Biosci. Biotech. Biochem. 59: 1181-1183.
50. Pakula, A.A. and Simon, M.I. 1992. Determination of transmembrane protein structure by disulfide cross-linking: The Escherichia coli Tar receptor. Proc. Natl. Acad. Sci. 89: 4144-4148.
51. Pany, S., Vijayvargia, R., and Krishnasastry, M.V. 2004. Caveolin-1 binding motif of α-hemolysin: Its role in stability and pore formation. Biochem. Biophys. Res. Commun. 322: 29-36.
52. Pédelacq, J.-D., Maveyraud, L., Prévost, G., Baba-Moussa, L., González, A., Courcelle, E., Shepard, W., Monteil, H., Samama, J.-P., and Mourey, L. 1999. The structure of Staphylococcus aureus leukocidin component (LukF-PV) reveals the fold of the water-soluble species of a family of transmembrane pore-forming toxins. Structure 7: 277-288.
53. Prévost, G., Colin, D.A., Mourey, L., and Menestrina, G. 2001. Staphylococcal pore-forming toxins. Curr. Top. Microbiol. Immunol. 257: 53-83.
54. Prévost, G., Menestrina, G., Colin, D.A., Werner, S., Bronner, S., Dalla Serra, M., Baba Moussa, L., Coraiola, M., Gravet, A., and Monteil, H. 2003. Staphylococcal bicomponent leucotoxins, mechanism of action, impact on cells and contribution to virulence. In Pore-forming peptides and protein toxins (eds. G. Menestrina et al.), 3-26. Taylor and Francis, London.
55. Shin, S.-H., Luchian, T., Cheley, S., Braha, O., and Bayley, H. 2002. Kinetics of a reversible covalent-bond forming reaction observed at the single molecule level. Angew. Chem. Int. Ed. 41: 3707-3709.
56. 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: 1859-1865.
57. Sugawara, N., Tomita, T., and 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.
58. Sugawara, N., Tomita, T., Sato, T., and Kamio, Y. 1999. Assembly of Staphylococcus aureus leukocidin into a pore-forming ring-shaped oligomer on human polymorphonuclear leukocytes and rabbit erythrocytes. Biosci. Biotech. Biochem. 63: 884-891.
59. Sugawara-Tomita, N., Tomita, T., and Kamio, Y. 2002. Stochastic assembly of two-component staphylococcal γ-hemolysin into heteroheptameric transmembrane pores with alternate subunit arrangements in ratios of 3:4 and 4:3. J. Bacteriol. 184: 4747-4756.
60. Vijayavargia, R., Kauer, S., Sangha, N., Sahasrabuddhe, A.A., Surolia, I., Shouche, Y., and Krishnasastry, M.V. 2004a. Assembly of a-hemolysin on A431 cells leads to clustering of caveolin-1. Biochem. Biophys. Res. Commun. 324: 1124-1129.
61. Vijayavargia, R., Suresh, C.G., and Krishnasastry, M.V. 2004b. Functional form of caveolin-1 is necessary for the assembly of a-hemolysin. Biochem. Biophys. Res. Commun. 324: 1130-1136.
62. Walker, B. and Bayley, H. 1995. Key residues for membrane binding, oligomerization, and pore-forming activity of staphylococcal a-hemolysin identified by cysteine scanning mutagenesis and targeted chemical modification. J. Biol. Chem. 270: 23065-23071.
63. Walker, B.J., Krishnasastry, M., Zorn, L., and Bayley, H. 1992. Assembly of the oligomeric membrane pore formed by staphylococcal a-hemolysin examined by truncation mutagenesis. J. Biol. Chem. 267: 21782-21786.
64. Walker, B., Braha, O., Cheley, S., and Bayley, H. 1995. An intermediate in the assembly of a pore-forming protein trapped with a geneticallyengineered switch. Chem. Biol. 2: 99-105.