Clostridium absonum α-toxin: New insights into clostridial phospholipase C substrate binding and specificity

Journal of Molecular Biology

Volumn 333, Issue 4, 2003, Pages 759-769

  Clark, Graeme C ^a   Briggs, David C ^a   Karasawa, Tadahiro ^b   Wang, Xingmin ^b   Cole, Ambrose R ^a   Maegawa, Tsuneo ^b   Jayasekera, Pramukh N ^c   Naylor, Claire E ^a   Miller, Julie ^c   Moss, David S ^a   Nakamura, Shinichi ^b   Basak, Ajit K ^a   Titball, Richard W ^c  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b KANAZAWA UNIVERSITY   (Japan)

^c DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

Author keywords

Characterisation; Clostridium absonum alpha toxin; Gas gangrene; Phospholipase C; X ray crystallography

Indexed keywords

BACTERIAL ENZYME; CLOSTRIDIUM TOXIN; PHOSPHOLIPASE C;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL VIRULENCE; CLOSTRIDIUM; CLOSTRIDIUM ABSONUM; CONFORMATION; CRYSTAL STRUCTURE; CYTOTOXICITY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; GAS GANGRENE; LETHAL DOSE; MEMBRANE BINDING; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TOXIN STRUCTURE;

CLOSTRIDIUM; CLOSTRIDIUM ABSONUM; CLOSTRIDIUM PERFRINGENS;

EID: 0142042864     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.07.016     Document Type: Article

References (57)

1. Awad M.M., Bryant A.E., Stevens D.L., Rood J.I. Virulence studies on chromosomal mutants constructed by allelic exchange provide genetic evidence for the essential role of α-toxin in Clostridium perfringens-mediated gas gangrene. Mol. Microbiol. 15:1995;191-202.
2. Krug E.L., Kent C. Phospholipase C from Clostridium perfringens: preparation and characterisation of homogeneous enzyme. Arch. Biochem. Biophys. 231:1984;400-410.
3. Sato H., Yamakawa Y., Ito A., Murata R. Effect of zinc and calcium ions on the production of alpha-toxin and proteases by Clostridium perfringens. Infect. Immun. 20:1978;325-333.
4. Kurioka S., Matsuda M. Phospholipase C assay using ρ -nitrophenylphosphorylcholine together with sorbitol and its application to studying the metal and detergent requirement of the enzyme. Anal. Biochem. 75:1976;281-289.
5. Moreau H., Pieroni G., Jolivet-Reynaud C., Alouf J.E., Verger R. A kinetic approach for studying phospholipase C (Clostridium perfringens alpha-toxin) activity on phospholipid monolayers. Biochemistry. 27:1988;2319-2323.
6. Titball R.W., Hunter S.E., Martin K., Morris K.L., Morris B., Shuttleworth A.D., et al. Molecular cloning and nucleotide sequence of the alpha-toxin (phospholipase C) of Clostridium perfringens. Infect. Immun. 57:1989;367-376.
7. Alape-Giron A., Flores-Diaz M., Guillouard I., Naylor C.E., Titball R.W., Rucavado A., et al. Identification of residues critical for toxicity in Clostridium perfringens phospholipase C, the key toxin in gas gangrene. Eur. J. Biochem. 267:2000;5191-5197.
8. Walker N., Holley J., Naylor C.E., Flores-Diaz M., Alape-Giron A., Carter G., et al. Identification of residues in the carboxy-terminal domain of Clostridium perfringens α-toxin (phospholipase C) which are required for its biological activities. Arch. Biochem. Biophys. 384:2000;24-30.
9. Leslie D., Fairweather N., Pickard D., Dougan G., Kehoe M. Phospholipase C and haemolytic activities of Clostridium perfringens alpha-toxin cloned in Escherichia coli: sequence and homology with a Baciluus cereus phospholipase C. Mol. Microbiol. 3:1989;383-392.
10. Naylor C.E., Eaton J.T., Howells A., Justin N., Moss D., Titball R.W., Basak A.K. Structure of the key toxin in gas gangrene. Nature Struct. Biol. 5:1998;738-746.
11. Nagahama M., Okagawa Y., Nakayama T., Nishioka E., Sakurai J. Site-directed mutagenesis of histidine residues in Clostridium perfringens alpha-toxin. J. Bacteriol. 177:1995;1179-1185.
12. Guillouard I., Garnier T., Cole S.T. Use of site-directed mutagenesis to probe structure-function relationships of alpha-toxin from Clostridium perfringens. Infect. Immun. 64:1996;2440-2444.
13. 2-like domain of the α-toxin from Clostridium perfringens mediates calcium-dependent membrane recognition. Mol. Microbiol. 26:1997;867-876.
14. Nagahama M., Nakayama T., Michiue K., Sakurai J. Site-specific mutagensis of Clostridium perfringens alpha-toxin: replacement of Asp-56. Asp-130, or Glu-152 causes loss of enzymatic and haemolytic activities. Infect. Immun. 65:1997;3489-3492.
15. Nagahama M., Mukai M., Ochi S., Sakurai J. Role of tryptophan-1 in haemolytic and phospholipase C activities of Clostridium perfringens alpha-toxin. Microbiol. Immunol. 44:2000;585-589.
16. Titball R.W., Leslie D.L., Harvey S., Kelly D.C. Hemolytic and sphingomyelinase activities of Clostridium perfringens alpha-toxin are dependent on a domain homologous to that of an enzyme from the human arachidonic acid pathway. Infect. Immun. 59:1991;1872-1874.
17. Titball R.W., Fearn A.M., Williamson E.D. Biochemical and immunological properties of the C-terminal domain of the alpha-toxin of Clostridium perfringens. FEMS Microbiol. Letters. 110:1993;45-50.
18. Jepson M., Bullifent H., Crane D., Flores-Diaz M., Alape-Giron A., Jayasekera P., et al. Tyrosine 331 and phenylalanine 334 in Clostridium perfringens α-toxin are essential for cytotoxic activity. FEBS Letters. 495:2001;172-177.
19. Nakamura S., Shimamura T., Hayase M., Nishida S. Numerical taxonomy of saccharolytic clostridia, particularly Clostridium perfringens-like strains: descriptions of Clostridium absonum sp. and Clostridium paraperfringens. Int. J. Syst. Bacteriol. 23:1973;419-429.
20. Miles E.M., Miles A.A. The lecithinase of Clostridium bifermentans and its relation to the α-toxin of Clostridium welchii. J. Gen. Microbiol. 1:1947;385-399.
21. Tso J., Siebel C. Cloning and expression of the phospholipase C gene from Clostridium perfringens and Clostridium bifermentans. Infect. Immun. 57:1989;468-476.
22. Jepson M., Howells A., Bullifent H., Bolgiano B., Crane D., Miller J., et al. Differences in the carboxy-terminal (putative phospholipid binding) domains of Clostridium perfringens and Clostridium bifermentans phospholipase C influence the haemolytic and lethal properties of these enzymes. Infect. Immun. 67:1999;3297-3301.
23. Masaki T., Umehashi H., Miyazaki H., Takano M., Yamakawa K., Nakamura S. Clostridium absonum from gas gangrene. Jpn. J. Med. Sci. Biol. 41:1988;27-30.
24. Tsutsui K., Minami J., Matsushita O., Katayama S., Taniguchi Y., Nakamura S., et al. Phylogenetic analysis of phospholipase C genes from Clostridium perfringens types A to E and Clostridium novyi. J. Bacteriol. 177:1995;7164-7170.
25. Justin N., Walker N., Bullifent H.L., Songer G., Bueschel D.M., Jost H., et al. The first strain of Clostridium perfringens isolated from an avian source has an alpha-toxin with divergent structural and kinetic properties. Biochemistry. 41:2002;6253-6262.
26. Naylor C.E., Jepson M., Crane D.T., Titball R.W., Miller J., Basak A.K., Bolgiano B. Characterisation of the calcium-binding C-terminal domain of Clostridium perfringens alpha-toxin. J. Mol. Biol. 294:1999;757-770.
27. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
28. Eaton J.T., Naylor C.E., Howells A.M., Moss D.S., Titball R.W., Basak A.K. Crystal structure of the C. perfringens alpha-toxin with the active site closed by a flexible loop region. J. Mol. Biol. 319:2002;275-281.
29. Ostroff R.M., Vasil A., Vasil M.L. Molecular comparison of a non-hemolytic and haemolytic phospholipase C from Pseudomonas aeruginosa. J. Bacteriol. 172:1990;5915-5923.
30. Beecher D.J., Wong A.C. Cooperative, synergistic and antagonistic haemolytic interactions between haemolysin BL, phosphatidylcholine phospholipase C and sphingomyelinase from Bacillus cereus. Microbiology. 146:2000;3033-3039.
31. Hansen S., Hough E., Svensson L.A., Wong Y.-L., Martin S.F. Crystal structure of phospholipase C from Bacillus cereus complexes with a substrate analog. J. Mol. Biol. 234:1993;179-187.
32. Hergenrother P.J., Martin S.F. Determination of the kinetic parameters for phospholipase C (Bacillus cereus) on different phospholipid substrates using a chromogenic assay based on the quantitation of inorganic phosphate. Anal. Biochem. 251:1997;45-49.
33. Martin S.F., Hergenrother P.J. General base catalysis by the phosphatidylcholine-preferring phospholipase C from Bacillus cereus: the role of Glu4 and Asp55. Biochemistry. 37:1998;5755-5760.
34. Martin S.F., Hergenrother P.J. Catalytic cycle of the phosphatidylcholine-preferring phospholipase C from Bacillus cereus. Solvent viscosity, deuterium isotope effects and proton inventory studies. Biochemistry. 38:1999;4403-4408.
35. Ruiz-Arguello M., Veiga M.P., Arrondo J., Goni F.M., Alonso A. Sphingomyelinase cleavage of sphingomyelin in pure and mixed lipid membranes. Influence of the physical state of the sphingolipid. Chem. Phys. Lipids. 114:2002;11-20.
36. Gelb M.H., Min J.-H., Jain M.K. Do membrane-bound enzymes access their substrates from the membrane or aqueous phase: interfacial versus non-interfacial enzymes. Biochim. Biophys. Acta. 1488:2000;20-27.
37. Wang X., Maegawa T., Karasawa T., Kozaki S., Tsukamoto K., Gyobu Y., et al. Genetic analysis of type E botulinum toxin-producing Clostridium butyricum strains. Appl. Environ. Microbiol. 66:2000;4992-4997.
38. Sato H., Chiba J., Sato Y. Monoclonal antibodies against alpha-toxin of Clostridium perfringens. FEMS Microbiol. Letters. 59:1989;173-176.
39. Edman P., Begg G. A protein sequenator. Eur. J. Biochem. 1:1967;80-91.
40. Nagahama M., Michiue K., Sakurai J. Membrane-damaging action of Clostridium perfringens alpha-toxin on phospholipid liposomes. Biochim. Biophys. Acta. 1280:1996;120-126.
41. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
42. Evans P.R. Data reductions. Sawyer L., Isaacs N., Bailey. Proceedings of the CCP4 Study Weekend on Data Collection and Processing. 1993;114-122 Daresbury Laboratory, Warrington, UK.
43. The CCP4 suite: programs for the protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
44. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163.
45. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallog. 30:1997;1022-1025.
46. Tong L. Combined molecular replacement. Acta Crystallog. sect. A. 52:1996;782-784.
47. Kissinger C.R., Gehlhaar D.K., Fogel D.B. Rapid automated molecular replacement by evolutionary search. Acta Crystallog. sect. D. 55:1999;484-491.
48. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
49. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models into electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
50. Terwilliger T.C. Maximum likelihood density modification. Acta Crystallog. sect. D. 56:2000;965-972.
51. Terwilliger T.C. Map-likelihood phasing. Acta Crystallog. sect. D. 57:2001;1763-1775.
52. McRee D.M. Practical Protein Crystallography. 2nd edit. 1999;Academic Press, Dan Diego.
53. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D. 53:1997;240-255.
54. Perrakis A., Harkiolaki M., Wilson K.S., Lamzin V.S. ARP/wARP and molecular replacement. Acta Crystallog. sect. D. 57:2001;1445-1450.
55. Kabsch W. A solution for the best rotation to relate two sets of vectors. Acta Crystallog. sect. A. 32:1976;922-923.
56. Humphrey W., Dalke A., Schulten K. VMD - visual molecular dynamics. J. Mol. Graph. 14:1996;33-38.
57. Wallace A.C., Laskowski R.A., Thornton J.M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8:1995;127-134.