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Microbiol Rev. Jun 1993; 57(2): 347–366.
PMCID: PMC372913

Bacterial phospholipases C.

Abstract

A variety of pathogenic bacteria produce phospholipases C, and since the discovery in 1944 that a bacterial toxin (Clostridium perfringens alpha-toxin) possessed an enzymatic activity, there has been considerable interest in this class of proteins. Initial speculation that all phospholipases C would have lethal properties has not been substantiated. Most of the characterized enzymes fall into one of four groups of structurally related proteins: the zinc-metallophospholipases C, the sphingomyelinases, the phosphatidylinositol-hydrolyzing enzymes, and the pseudomonad phospholipases C. The zinc-metallophospholipases C have been most intensively studied, and lethal toxins within this group possess an additional domain. The toxic phospholipases C can interact with eukaryotic cell membranes and hydrolyze phosphatidylcholine and sphingomyelin, leading to cell lysis. However, measurement of the cytolytic potential or lethality of phospholipases C may not accurately indicate their roles in the pathogenesis of disease. Subcytolytic concentrations of phospholipase C can perturb host cells by activating the arachidonic acid cascade or protein kinase C. Nonlethal phospholipases C, such as the Listeria monocytogenes PLC-A, appear to enhance the release of the organism from the host cell phagosome. Since some phospholipases C play important roles in the pathogenesis of disease, they could form components of vaccines. A greater understanding of the modes of action and structure-function relationships of phospholipases C will facilitate the interpretation of studies in which these enzymes are used as membrane probes and will enhance the use of these proteins as models for eukaryotic phospholipases C.

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  • Allan D, Thomas P, Michell RH. Rapid transbilayer diffusion of 1,2-diacylglycerol and its relevance to control of membrane curvature. Nature. 1978 Nov 16;276(5685):289–290. [PubMed]
  • Altenbern RA. Formation of hemolysin by strains of Pseudomonas aeruginosa. Can J Microbiol. 1966 Apr;12(2):231–241. [PubMed]
  • Anba J, Bidaud M, Vasil ML, Lazdunski A. Nucleotide sequence of the Pseudomonas aeruginosa phoB gene, the regulatory gene for the phosphate regulon. J Bacteriol. 1990 Aug;172(8):4685–4689. [PMC free article] [PubMed]
  • Aurebekk B, Little C. Phospholipase C from Bacillus cereus. Evidence for essential lysine residues. Biochem J. 1977 Jan 1;161(1):159–165. [PMC free article] [PubMed]
  • Badwey JA, Karnovsky ML. Production of superoxide by phagocytic leukocytes: a paradigm for stimulus-response phenomena. Curr Top Cell Regul. 1986;28:183–208. [PubMed]
  • Baine WB. Cytolytic and phospholipase C activity in Legionella species. J Gen Microbiol. 1985 Jun;131(6):1383–1391. [PubMed]
  • Baine WB. A phospholipase C from the Dallas 1E strain of Legionella pneumophila serogroup 5: purification and characterization of conditions for optimal activity with an artificial substrate. J Gen Microbiol. 1988 Feb;134(2):489–498. [PubMed]
  • Baine WB, Rasheed JK, Mackel DC, Bopp CA, Wells JG, Kaufmann AF. Exotoxin activity associated with the Legionnaires disease bacterium. J Clin Microbiol. 1979 Mar;9(3):453–456. [PMC free article] [PubMed]
  • BANGHAM AD, DAWSON RM. Electrokinetic requirements for the reaction between Cl. perfringens alpha-toxin (phospholipase C) and phospholipid substrates. Biochim Biophys Acta. 1962 May 7;59:103–115. [PubMed]
  • Berka RM, Gray GL, Vasil ML. Studies of phospholipase C (heat-labile hemolysin) in Pseudomonas aeruginosa. Infect Immun. 1981 Dec;34(3):1071–1074. [PMC free article] [PubMed]
  • Bernheimer AW, Avigad LS, Kim KS. Staphylococcal sphingomyelinase (beta-hemolysin). Ann N Y Acad Sci. 1974 Jul 31;236(0):292–306. [PubMed]
  • Bernheimer AW, Bey RF. Copurification of Leptospira interrogans serovar pomona hemolysin and sphingomyelinase C. Infect Immun. 1986 Oct;54(1):262–264. [PMC free article] [PubMed]
  • Berridge MJ. Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem. 1987;56:159–193. [PubMed]
  • Bianco ID, Fidelio GD, Maggio B. Effect of sulfatide and gangliosides on phospholipase C and phospholipase A2 activity. A monolayer study. Biochim Biophys Acta. 1990 Jul 24;1026(2):179–185. [PubMed]
  • Blow D. Enzymology. Lipases reach the surface. Nature. 1991 Jun 6;351(6326):444–445. [PubMed]
  • Boëthius J, Rydqvist B, Möllby R, Wadström T. Effect of a highly purified phospholipase C on some electrophysiological properties of the frog muscle fibre membrane. Life Sci. 1973 Jul 16;13(2):171–176. [PubMed]
  • Boyd NA, Thomson RO, Walker PD. The prevention of experimental Clostridium novyi and Cl. perfringens gas gangrene in high-velocity missile wounds by active immunisation. J Med Microbiol. 1972 Nov;5(4):467–472. [PubMed]
  • Bramley AJ, Patel AH, O'Reilly M, Foster R, Foster TJ. Roles of alpha-toxin and beta-toxin in virulence of Staphylococcus aureus for the mouse mammary gland. Infect Immun. 1989 Aug;57(8):2489–2494. [PMC free article] [PubMed]
  • Brzozowski AM, Derewenda U, Derewenda ZS, Dodson GG, Lawson DM, Turkenburg JP, Bjorkling F, Huge-Jensen B, Patkar SA, Thim L. A model for interfacial activation in lipases from the structure of a fungal lipase-inhibitor complex. Nature. 1991 Jun 6;351(6326):491–494. [PubMed]
  • Camilli A, Goldfine H, Portnoy DA. Listeria monocytogenes mutants lacking phosphatidylinositol-specific phospholipase C are avirulent. J Exp Med. 1991 Mar 1;173(3):751–754. [PMC free article] [PubMed]
  • Canard B, Cole ST. Genome organization of the anaerobic pathogen Clostridium perfringens. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6676–6680. [PMC free article] [PubMed]
  • Chin JC, Watts JE. Biological properties of phospholipase C purified from a fleecerot isolate of Pseudomonas aeruginosa. J Gen Microbiol. 1988 Sep;134(9):2567–2575. [PubMed]
  • Chovnick A, Schneider WP, Tso JY, Queen C, Chang CN. A recombinant, membrane-acting immunotoxin. Cancer Res. 1991 Jan 15;51(2):465–467. [PubMed]
  • Christiansson A, Kuypers FA, Roelofsen B, Op den Kamp JA, van Deenen LL. Lipid molecular shape affects erythrocyte morphology: a study involving replacement of native phosphatidylcholine with different species followed by treatment of cells with sphingomyelinase C or phospholipase A2. J Cell Biol. 1985 Oct;101(4):1455–1462. [PMC free article] [PubMed]
  • Clark JD, Lin LL, Kriz RW, Ramesha CS, Sultzman LA, Lin AY, Milona N, Knopf JL. A novel arachidonic acid-selective cytosolic PLA2 contains a Ca(2+)-dependent translocation domain with homology to PKC and GAP. Cell. 1991 Jun 14;65(6):1043–1051. [PubMed]
  • Clark MA, Shorr RG, Bomalaski JS. Antibodies prepared to Bacillus cereus phospholipase C crossreact with a phosphatidylcholine preferring phospholipase C in mammalian cells. Biochem Biophys Res Commun. 1986 Oct 15;140(1):114–119. [PubMed]
  • Coleman K, Dougan G, Arbuthnott JP. Cloning, and expression in Escherichia coli K-12, of the chromosomal hemolysin (phospholipase C) determinant of Pseudomonas aeruginosa. J Bacteriol. 1983 Feb;153(2):909–915. [PMC free article] [PubMed]
  • Coleman R, Finean JB, Knutton S, Limbrick AR. A structural study of the modification of erythrocyte ghosts by phospholipase C. Biochim Biophys Acta. 1970;219(1):81–92. [PubMed]
  • Colley CM, Zwaal RF, Roelofsen B, van Deenen LL. Lytic and non-lytic degradation of phospholipids in mammalian erythrocytes by pure phospholipases. Biochim Biophys Acta. 1973 Apr 25;307(1):74–82. [PubMed]
  • Conlan JW, North RJ. Roles of Listeria monocytogenes virulence factors in survival: virulence factors distinct from listeriolysin are needed for the organism to survive an early neutrophil-mediated host defense mechanism. Infect Immun. 1992 Mar;60(3):951–957. [PMC free article] [PubMed]
  • COSTLOW RD. Lecithinase from Bacillus anthracis. J Bacteriol. 1958 Sep;76(3):317–325. [PMC free article] [PubMed]
  • Coutinho IR, Berk RS, Mammen E. Platelet aggregation by a phospholipase C from Pseudomonas aeruginosa. Thromb Res. 1988 Sep 1;51(5):495–505. [PubMed]
  • de GIER, VAN DEENEN L. Some lipid characteristics of red cell membranes of various animal species. Biochim Biophys Acta. 1961 May 13;49:286–296. [PubMed]
  • Demel RA, Geurts van Kessel WS, Zwaal RF, Roelofsen B, van Deenen LL. Relation between various phospholipase actions on human red cell membranes and the interfacial phospholipid pressure in monolayers. Biochim Biophys Acta. 1975 Sep 16;406(1):97–107. [PubMed]
  • De Silva NS, Quinn PA. Rapid screening assay for phospholipase C activity in mycoplasmas. J Clin Microbiol. 1987 Apr;25(4):729–731. [PMC free article] [PubMed]
  • Diaz-Laviada I, Larrodera P, Diaz-Meco MT, Cornet ME, Guddal PH, Johansen T, Moscat J. Evidence for a role of phosphatidylcholine-hydrolysing phospholipase C in the regulation of protein kinase C by ras and src oncogenes. EMBO J. 1990 Dec;9(12):3907–3912. [PMC free article] [PubMed]
  • Diener M, Eglème C, Rummel W. Phospholipase C-induced anion secretion and its interaction with carbachol in the rat colonic mucosa. Eur J Pharmacol. 1991 Aug 6;200(2-3):267–276. [PubMed]
  • Doery HM, Magnusson BJ, Gulasekharam J, Pearson JE. The properties of phospholipase enzymes in staphylococcal toxins. J Gen Microbiol. 1965 Aug;40(2):283–296. [PubMed]
  • Dowling JN, Saha AK, Glew RH. Virulence factors of the family Legionellaceae. Microbiol Rev. 1992 Mar;56(1):32–60. [PMC free article] [PubMed]
  • ELEK SD, LEVY E. The nature of discrepancies between haemolysins in culture filtrates and plate haemolysin patterns of staphylococci. J Pathol Bacteriol. 1954 Jul;68(1):31–40. [PubMed]
  • el-Sayed MY, DeBose CD, Coury LA, Roberts MF. Sensitivity of phospholipase C (Bacillus cereus) activity to phosphatidylcholine structural modifications. Biochim Biophys Acta. 1985 Dec 4;837(3):325–335. [PubMed]
  • el-Sayed MY, Roberts MF. Charged detergents enhance the activity of phospholipase C (Bacillus cereus) towards micellar short-chain phosphatidylcholine. Biochim Biophys Acta. 1985 Sep 20;831(1):133–141. [PubMed]
  • Exton JH. Signaling through phosphatidylcholine breakdown. J Biol Chem. 1990 Jan 5;265(1):1–4. [PubMed]
  • Fujii T, Tamura A. Asymmetric manipulation of the membrane lipid bilayer of intact human erythrocytes with phospholipase A, C, or D induces a change in cell shape. J Biochem. 1979 Nov;86(5):1345–1352. [PubMed]
  • Fujii Y, Nomura S, Oshita Y, Sakurai J. Excitatory effect of Clostridium perfringens alpha toxin on the rat isolated aorta. Br J Pharmacol. 1986 Jul;88(3):531–539. [PMC free article] [PubMed]
  • Fujii Y, Sakurai J. Contraction of the rat isolated aorta caused by Clostridium perfringens alpha toxin (phospholipase C): evidence for the involvement of arachidonic acid metabolism. Br J Pharmacol. 1989 May;97(1):119–124. [PMC free article] [PubMed]
  • Gaillard JL, Berche P, Mounier J, Richard S, Sansonetti P. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun. 1987 Nov;55(11):2822–2829. [PMC free article] [PubMed]
  • Gatt S, Dinur T, Barenholz Y. A spectrophotometric method for determination of sphingomyelinase. Biochim Biophys Acta. 1978 Sep 28;530(3):503–507. [PubMed]
  • Geoffroy C, Raveneau J, Beretti JL, Lecroisey A, Vazquez-Boland JA, Alouf JE, Berche P. Purification and characterization of an extracellular 29-kilodalton phospholipase C from Listeria monocytogenes. Infect Immun. 1991 Jul;59(7):2382–2388. [PMC free article] [PubMed]
  • Granström M, Ericsson A, Strandvik B, Wretlind B, Pavlovskis OR, Berka R, Vasil ML. Relation between antibody response to Pseudomonas aeruginosa exoproteins and colonization/infection in patients with cystic fibrosis. Acta Paediatr Scand. 1984 Nov;73(6):772–777. [PubMed]
  • Gray GL, Berka RM, Vasil ML. Phospholipase C regulatory mutation of Pseudomonas aeruginosa that results in constitutive synthesis of several phosphate-repressible proteins. J Bacteriol. 1982 Jun;150(3):1221–1226. [PMC free article] [PubMed]
  • Guddal PH, Johansen T, Schulstad K, Little C. Apparent phosphate retrieval system in Bacillus cereus. J Bacteriol. 1989 Oct;171(10):5702–5706. [PMC free article] [PubMed]
  • Gustafson C, Sjödahl R, Tagesson C. Phospholipase activation and arachidonic acid release in intestinal epithelial cells from patients with Crohn's disease. Scand J Gastroenterol. 1990 Nov;25(11):1151–1160. [PubMed]
  • Gustafson C, Tagesson C. Phospholipase C from Clostridium perfringens stimulates phospholipase A2-mediated arachidonic acid release in cultured intestinal epithelial cells (INT 407). Scand J Gastroenterol. 1990 Apr;25(4):363–371. [PubMed]
  • Hanssens I, Van Cauwelaert FH. Shielding of phospholipid monolayers from phospholipase C hydrolysis by alpha-lactalbumin adsorption. Biochem Biophys Res Commun. 1978 Oct 30;84(4):1088–1096. [PubMed]
  • Henner DJ, Yang M, Chen E, Hellmiss R, Rodriguez H, Low MG. Sequence of the Bacillus thuringiensis phosphatidylinositol specific phospholipase C. Nucleic Acids Res. 1988 Nov 11;16(21):10383–10383. [PMC free article] [PubMed]
  • Hough E, Hansen LK, Birknes B, Jynge K, Hansen S, Hordvik A, Little C, Dodson E, Derewenda Z. High-resolution (1.5 A) crystal structure of phospholipase C from Bacillus cereus. Nature. 1989 Mar 23;338(6213):357–360. [PubMed]
  • Hummel R, Witte W, Kemmer G. Zur Frage der wechselseitigen Ubertragung von Staphylococcus aureus zwischen Mensch und Rind und der Milieuadaptation der Hämolysin- und Fibrinolysinbildung. Arch Exp Veterinarmed. 1978;32(2):287–298. [PubMed]
  • Ikezawa H, Matsushita M, Tomita M, Taguchi R. Effects of metal ions on sphingomyelinase activity of Bacillus cereus. Arch Biochem Biophys. 1986 Sep;249(2):588–595. [PubMed]
  • Ikezawa H, Nakabayashi T, Suzuki K, Nakajima M, Taguchi T, Taguchi R. Complete purification of phosphatidylinositol-specific phospholipase C from a strain of Bacillus thuringiensis. J Biochem. 1983 Jun;93(6):1717–1719. [PubMed]
  • Ikezawa H, Yamanegi M, Taguchi R, Miyashita T, Ohyabu T. Studies on phosphatidylinositol phosphodiesterase (phospholipase C type) of Bacillus cereus. I. purification, properties and phosphatase-releasing activity. Biochim Biophys Acta. 1976 Nov 19;450(2):154–164. [PubMed]
  • Johansen T, Holm T, Guddal PH, Sletten K, Haugli FB, Little C. Cloning and sequencing of the gene encoding the phosphatidylcholine-preferring phospholipase C of Bacillus cereus. Gene. 1988 May 30;65(2):293–304. [PubMed]
  • Kanfer JN, Spielvogel CH. Phospholipase C catalyzed formation of sphinogomyelin--14C from lecithin and N-(-14C)-oleoyl-sphingosine. Lipids. 1975 Jul;10(7):391–394. [PubMed]
  • Kameyama S, Sato H, Murata R. The role of alpha-toxin of Clostridium perfringens in experimental gas gangrene in guinea pigs. Jpn J Med Sci Biol. 1972 Jun;25(3):200–200. [PubMed]
  • Kent C, Evers A, Haun SS. Diacylglycerol metabolism in phospholipase C-treated mammalian cells. Arch Biochem Biophys. 1986 Nov 1;250(2):519–525. [PubMed]
  • Klein R, Miller N, Kemp P, Laser H. The activation of phospholipase C from Clostridium Welchii by quinine: an absolute requirement for calcium ions. Chem Phys Lipids. 1975 Sep;15(1):15–26. [PubMed]
  • Kominami T, Miki A, Ikehara Y. Electrophoretic characterization of hepatic alkaline phosphatase released by phosphatidylinositol-specific phospholipase C. A comparison with liver membrane and serum-soluble forms. Biochem J. 1985 Apr 1;227(1):183–189. [PMC free article] [PubMed]
  • Krug EL, Kent C. Phospholipase C from Clostridium perfringens: preparation and characterization of homogeneous enzyme. Arch Biochem Biophys. 1984 Jun;231(2):400–410. [PubMed]
  • Kuppe A, Evans LM, McMillen DA, Griffith OH. Phosphatidylinositol-specific phospholipase C of Bacillus cereus: cloning, sequencing, and relationship to other phospholipases. J Bacteriol. 1989 Nov;171(11):6077–6083. [PMC free article] [PubMed]
  • Kurioka S, Matsuda M. Phospholipase C assay using p-nitrophenylphosphoryl-choline together with sorbitol and its application to studying the metal and detergent requirement of the enzyme. Anal Biochem. 1976 Sep;75(1):281–289. [PubMed]
  • Landfald B, Strøm AR. Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J Bacteriol. 1986 Mar;165(3):849–855. [PMC free article] [PubMed]
  • Larrodera P, Cornet ME, Diaz-Meco MT, Lopez-Barahona M, Diaz-Laviada I, Guddal PH, Johansen T, Moscat J. Phospholipase C-mediated hydrolysis of phosphatidylcholine is an important step in PDGF-stimulated DNA synthesis. Cell. 1990 Jun 15;61(6):1113–1120. [PubMed]
  • Lehmann V. Properties of purified phospholipase C from Acinetobacter calcoaceticus. Acta Pathol Microbiol Scand B Microbiol Immunol. 1972;80(6):827–834. [PubMed]
  • Lehmann V. Haemolytic activity of various strains of Acinetobacter. Acta Pathol Microbiol Scand B Microbiol Immunol. 1973 Aug;81(4):427–432. [PubMed]
  • Leimeister-Wächter M, Domann E, Chakraborty T. Detection of a gene encoding a phosphatidylinositol-specific phospholipase C that is co-ordinately expressed with listeriolysin in Listeria monocytogenes. Mol Microbiol. 1991 Feb;5(2):361–366. [PubMed]
  • 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 Bacillus cereus phospholipase C. Mol Microbiol. 1989 Mar;3(3):383–392. [PubMed]
  • Levine L, Xiao DM, Little C. Increased arachidonic acid metabolites from cells in culture after treatment with the phosphatidylcholine-hydrolyzing phospholipase C from Bacillus cereus. Prostaglandins. 1987 Nov;34(5):633–642. [PubMed]
  • Little C. The histidine residues of phospholipase C from Bacillus cereus. Biochem J. 1977 Nov 1;167(2):399–404. [PMC free article] [PubMed]
  • Little C, Aurebekk B. Inactivation of phospholipase C from Bacillus cereus by a carboxyl group modifying reagent. Acta Chem Scand B. 1977;31(4):273–277. [PubMed]
  • Little C, Aurebekk B, Otnaess AB. Purification by affinity chromatography of phospholipase C from Bacillus cereus. FEBS Lett. 1975 Apr 1;52(2):175–179. [PubMed]
  • Logan AJ, Williamson ED, Titball RW, Percival DA, Shuttleworth AD, Conlan JW, Kelly DC. Epitope mapping of the alpha-toxin of Clostridium perfringens. Infect Immun. 1991 Dec;59(12):4338–4342. [PMC free article] [PubMed]
  • Lory S, Tai PC. Characterization of the phospholipase C gene of Pseudomonas aeruginosa cloned in Escherichia coli. Gene. 1983 Apr;22(1):95–101. [PubMed]
  • Low DK, Freer JH, Arbuthnott JP, Möllby R, Wadström T. Consequences of spingomyelin degradation in erythrocyte ghost membranes by staphylococcal beta-toxin (sphingomyelinase C). Toxicon. 1974 May;12(3):279–285. [PubMed]
  • Low MG, Finean JB. The action of phosphatidylinositol-specific phospholipases C on membranes. Biochem J. 1976 Jan 15;154(1):203–208. [PMC free article] [PubMed]
  • Macfarlane MG, Knight BC. The biochemistry of bacterial toxins: The lecithinase activity of Cl. welchii toxins. Biochem J. 1941 Sep;35(8-9):884–902. [PMC free article] [PubMed]
  • MACKANESS GB. Cellular resistance to infection. J Exp Med. 1962 Sep 1;116:381–406. [PMC free article] [PubMed]
  • Mengaud J, Braun-Breton C, Cossart P. Identification of phosphatidylinositol-specific phospholipase C activity in Listeria monocytogenes: a novel type of virulence factor? Mol Microbiol. 1991 Feb;5(2):367–372. [PubMed]
  • Meyers DJ, Berk RS. Characterization of phospholipase C from Pseudomonas aeruginosa as a potent inflammatory agent. Infect Immun. 1990 Mar;58(3):659–666. [PMC free article] [PubMed]
  • Meyers DJ, Palmer KC, Bale LA, Kernacki K, Preston M, Brown T, Berk RS. In vivo and in vitro toxicity of phospholipase C from Pseudomonas aeruginosa. Toxicon. 1992 Feb;30(2):161–169. [PubMed]
  • Mitsu K, Mitsui N, Hase J. Clostridium perfringens exotoxins. I. Purification and properties of -toxin. Jpn J Exp Med. 1973 Apr;43(2):65–80. [PubMed]
  • Möllby R, Holme T, Nord CE, Smyth CJ, Wadström T. Production of phospholipase C (alpha-toxin), haemolysins and lethal toxins by Clostridium perfringens types A to D. J Gen Microbiol. 1976 Sep;96(1):137–144. [PubMed]
  • Möllby R, Thelestam M, Wadström T. Effect of Clostridium perfringens phospholipase C(alpha-toxin) on the human diploid fibroblast membrane. J Membr Biol. 1974;16(4):313–330. [PubMed]
  • Moolten FL, Schreiber BM, Zajdel SH. Antibodies conjugated to potent cytotoxins as specific antitumor agents. Immunol Rev. 1982;62:47–73. [PubMed]
  • Moreau H, Pieroni G, Jolivet-Reynaud C, Alouf JE, Verger R. A new kinetic approach for studying phospholipase C (Clostridium perfringens alpha toxin) activity on phospholipid monolayers. Biochemistry. 1988 Apr 5;27(7):2319–2323. [PubMed]
  • Nelson GJ. Lipid composition of erythrocytes in various mammalian species. Biochim Biophys Acta. 1967 Oct 2;144(2):221–232. [PubMed]
  • Ohsaka A, Tsuchiya M, Oshio C, Miyairi M, Suzuki K, Yamakawa Y. Aggregation of platelets in the mesenteric microcirculation of the rat induced by alpha-toxin (phospholipase C) of Clostridium perfringens. Toxicon. 1978;16(4):333–341. [PubMed]
  • Okabe A, Shimizu T, Hayashi H. Cloning and sequencing of a phospholipase C gene of Clostridium perfringens. Biochem Biophys Res Commun. 1989 Apr 14;160(1):33–39. [PubMed]
  • Okawa Y, Yamaguchi T. Studies on phospholipases from Streptomyces. III. Purification and properties of Streptomyces hachijoensis phospholipase C. J Biochem. 1975 Sep;78(3):537–545. [PubMed]
  • Ostroff RM, Vasil AI, Vasil ML. Molecular comparison of a nonhemolytic and a hemolytic phospholipase C from Pseudomonas aeruginosa. J Bacteriol. 1990 Oct;172(10):5915–5923. [PMC free article] [PubMed]
  • Ostroff RM, Vasil ML. Identification of a new phospholipase C activity by analysis of an insertional mutation in the hemolytic phospholipase C structural gene of Pseudomonas aeruginosa. J Bacteriol. 1987 Oct;169(10):4597–4601. [PMC free article] [PubMed]
  • Ostroff RM, Wretlind B, Vasil ML. Mutations in the hemolytic-phospholipase C operon result in decreased virulence of Pseudomonas aeruginosa PAO1 grown under phosphate-limiting conditions. Infect Immun. 1989 May;57(5):1369–1373. [PMC free article] [PubMed]
  • Otnaess AB. The hydrolysis of sphingomyelin by phospholipase C from Bacillus cereus. FEBS Lett. 1980 Jun 2;114(2):202–204. [PubMed]
  • Otnaess AB, Giercksky KE, Prydz H. Parenteral administration of phospholipase C in the rat. Distribution, elimination, and lethal doses. Scand J Clin Lab Invest. 1976 Oct;36(6):553–559. [PubMed]
  • Otnaess AB, Little C, Sletten K, Wallin R, Johnsen S, Flengsrud R, Prydz H. Some characteristics of phospholipase C from Bacillus cereus. Eur J Biochem. 1977 Oct 3;79(2):459–468. [PubMed]
  • Parkinson EK. Phospholipase C mimics the differential effects of phorbol-12-myristate-13-acetate on the colony formation and cornification of cultured normal and transformed human keratinocytes. Carcinogenesis. 1987 Jun;8(6):857–860. [PubMed]
  • Pörn MI, Slotte JP. Reversible effects of sphingomyelin degradation on cholesterol distribution and metabolism in fibroblasts and transformed neuroblastoma cells. Biochem J. 1990 Oct 1;271(1):121–126. [PMC free article] [PubMed]
  • Portnoy DA, Jacks PS, Hinrichs DJ. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med. 1988 Apr 1;167(4):1459–1471. [PMC free article] [PubMed]
  • Pritchard AE, Vasil ML. Nucleotide sequence and expression of a phosphate-regulated gene encoding a secreted hemolysin of Pseudomonas aeruginosa. J Bacteriol. 1986 Jul;167(1):291–298. [PMC free article] [PubMed]
  • Projan SJ, Kornblum J, Kreiswirth B, Moghazeh SL, Eisner W, Novick RP. Nucleotide sequence: the beta-hemolysin gene of Staphylococcus aureus. Nucleic Acids Res. 1989 Apr 25;17(8):3305–3305. [PMC free article] [PubMed]
  • Rácz P, Tenner K, Mérö E. Experimental Listeria enteritis. I. An electron microscopic study of the epithelial phase in experimental listeria infection. Lab Invest. 1972 Jun;26(6):694–700. [PubMed]
  • Rácz P, Tenner K, Szivessy K. Electron microscopic studies in experimental keratoconjunctivitis listeriosa. I. Penetration of Listeria monocytogenes into corneal epithelial cells. Acta Microbiol Acad Sci Hung. 1970;17(3):221–236. [PubMed]
  • Renetseder R, Brunie S, Dijkstra BW, Drenth J, Sigler PB. A comparison of the crystal structures of phospholipase A2 from bovine pancreas and Crotalus atrox venom. J Biol Chem. 1985 Sep 25;260(21):11627–11634. [PubMed]
  • Rogolsky M. Nonenteric toxins of Staphylococcus aureus. Microbiol Rev. 1979 Sep;43(3):320–360. [PMC free article] [PubMed]
  • Rood JI, Cole ST. Molecular genetics and pathogenesis of Clostridium perfringens. Microbiol Rev. 1991 Dec;55(4):621–648. [PMC free article] [PubMed]
  • Rosenthal AF, Pousada M. Inhibition of phospholipase C by phosphonate analogs of glycerophosphatides. Biochim Biophys Acta. 1968 Oct 22;164(2):226–237. [PubMed]
  • Saint-Joanis B, Garnier T, Cole ST. Gene cloning shows the alpha-toxin of Clostridium perfringens to contain both sphingomyelinase and lecithinase activities. Mol Gen Genet. 1989 Nov;219(3):453–460. [PubMed]
  • Sakurai J, Fujii Y, Torii K, Kobayashi K. Dissociation of various biological activities of Clostridium perfringens alpha toxin by chemical modification. Toxicon. 1989;27(3):317–323. [PubMed]
  • Samuelsson B. Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation. Science. 1983 May 6;220(4597):568–575. [PubMed]
  • Sato H, Chiba J, Sato Y. Monoclonal antibodies against alpha toxin of Clostridium perfringens. FEMS Microbiol Lett. 1989 May;50(1-2):173–176. [PubMed]
  • 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. 1978 May;20(2):325–333. [PMC free article] [PubMed]
  • Shen BF, Tai PC, Pritchard AE, Vasil ML. Nucleotide sequences and expression in Escherichia coli of the in-phase overlapping Pseudomonas aeruginosa plcR genes. J Bacteriol. 1987 Oct;169(10):4602–4607. [PMC free article] [PubMed]
  • Shortridge VD, Lazdunski A, Vasil ML. Osmoprotectants and phosphate regulate expression of phospholipase C in Pseudomonas aeruginosa. Mol Microbiol. 1992 Apr;6(7):863–871. [PubMed]
  • Slein MW, Logan GF. MECHANISM OF ACTION OF THE TOXIN OF BACILLUS ANTHRACIS II. : Alkaline Phosphatasemia Produced by Culture Filtrates of Various Bacilli. J Bacteriol. 1962 Feb;83(2):359–369. [PMC free article] [PubMed]
  • Smyth CJ, Arbuthnott JP. Properties of Clostridium perfringens (welchii) type-A alpha-toxin (phospholipase C) purified by electrofocusing. J Med Microbiol. 1974 Feb;7(1):41–66. [PubMed]
  • Snyder WR. A continuous spectrophotometric assay for the Bacillus cereus phospholipase C using a thiophosphate substrate analog: evaluation of assay conditions and chromogenic agents. Anal Biochem. 1987 Jul;164(1):199–206. [PubMed]
  • Soucková A, Soucek A. Inhibition of the hemolytic action of and lysins of Staphylococcus pyogenes by Corynebacterium hemolyticum, C. ovis and C. ulcerans. Toxicon. 1972 Aug;10(5):501–509. [PubMed]
  • Southern PM, Jr, Mays BB, Pierce AK, Sanford JP. Pulmonary clearance of Pseudomonas aeruginosa. J Lab Clin Med. 1970 Oct;76(4):548–559. [PubMed]
  • Sowadski JM, Handschumacher MD, Murthy HM, Foster BA, Wyckoff HW. Refined structure of alkaline phosphatase from Escherichia coli at 2.8 A resolution. J Mol Biol. 1985 Nov 20;186(2):417–433. [PubMed]
  • Stevens DL, Mitten J, Henry C. Effects of alpha and theta toxins from Clostridium perfringens on human polymorphonuclear leukocytes. J Infect Dis. 1987 Aug;156(2):324–333. [PubMed]
  • Styrt B, Walker RD, White JC. Neutrophil oxidative metabolism after exposure to bacterial phospholipase C. J Lab Clin Med. 1989 Jul;114(1):51–57. [PubMed]
  • Sugahara T, Osaka A. Two molecular forms of Clostridium perfringens alpha-toxin associated with lethal, hemolytic and enzymatic activities. Jpn J Med Sci Biol. 1970 Feb;23(1):61–66. [PubMed]
  • Sugahara T, Takahashi T, Yamaya S, Ohsaka A. In vitro aggregation of platelets induced by alpha-toxin (phospholipase C) of Clostridium perfringens. Jpn J Med Sci Biol. 1976 Oct;29(5):255–263. [PubMed]
  • Sugahara T, Takahashi T, Yamaya S, Ohsaka A. Vascular permeability increase by alpha-toxin (phospholipase C) of Clostridium perfringens. Toxicon. 1977;15(1):81–87. [PubMed]
  • Taguchi R, Asahi Y, Ikezawa H. Purification and properties of phosphatidylinositol-specific phospholipase C of Bacillus thuringiensis. Biochim Biophys Acta. 1980 Jul 14;619(1):48–57. [PubMed]
  • Taguchi R, Ikezawa H. Phospholipase C from Clostridium novyi type A. I. Biochim Biophys Acta. 1975 Oct 21;409(1):75–85. [PubMed]
  • Taguchi R, Ikezawa H. Phosphatidyl inositol-specific phospholipase C from Clostridium novyi type A. Arch Biochem Biophys. 1978 Feb;186(1):196–201. [PubMed]
  • Takahashi T, Sugahara T, Ohsaka A. Phospholipase C from Clostridium perfringens. Methods Enzymol. 1981;71(Pt 100):710–725. [PubMed]
  • Thelestam M, Möllby R. Sensitive assay for detection of toxin-induced damage to the cytoplasmic membrane of human diploid fibroblasts. Infect Immun. 1975 Aug;12(2):225–232. [PMC free article] [PubMed]
  • Thuren T, Kinnunen PK. A continuous fluorometric assay for phospholipase C from Clostridium perfringens. Chem Phys Lipids. 1991 Aug;59(1):69–74. [PubMed]
  • Titball RW, Hunter SE, Martin KL, Morris BC, Shuttleworth AD, Rubidge T, Anderson DW, Kelly DC. Molecular cloning and nucleotide sequence of the alpha-toxin (phospholipase C) of Clostridium perfringens. Infect Immun. 1989 Feb;57(2):367–376. [PMC free article] [PubMed]
  • Titball RW, Leslie DL, Harvey S, Kelly D. 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. 1991 May;59(5):1872–1874. [PMC free article] [PubMed]
  • Titball RW, Rubidge T. The role of histidine residues in the alpha toxin of Clostridium perfringens. FEMS Microbiol Lett. 1990 Mar 15;56(3):261–265. [PubMed]
  • Tomita M, Nakai K, Yamada A, Taguchi R, Ikezawa H. Secondary structure of sphingomyelinase from Bacillus cereus. J Biochem. 1990 Nov;108(5):811–815. [PubMed]
  • Tomita M, Taguchi R, Ikezawa H. Molecular properties and kinetic studies on sphingomyelinase of Bacillus cereus. Biochim Biophys Acta. 1982 May 21;704(1):90–99. [PubMed]
  • Toyonaga T, Matsushita O, Katayama S, Minami J, Okabe A. Role of the upstream region containing an intrinsic DNA curvature in the negative regulation of the phospholipase C gene of Clostridium perfringens. Microbiol Immunol. 1992;36(6):603–613. [PubMed]
  • Tso JY, Siebel C. Cloning and expression of the phospholipase C gene from Clostridium perfringens and Clostridium bifermentans. Infect Immun. 1989 Feb;57(2):468–476. [PMC free article] [PubMed]
  • Vasil ML, Berka RM, Gray GL, Nakai H. Cloning of a phosphate-regulated hemolysin gene (phospholipase C) from Pseudomonas aeruginosa. J Bacteriol. 1982 Oct;152(1):431–440. [PMC free article] [PubMed]
  • Vasil ML, Krieg DP, Kuhns JS, Ogle JW, Shortridge VD, Ostroff RM, Vasil AI. Molecular analysis of hemolytic and phospholipase C activities of Pseudomonas cepacia. Infect Immun. 1990 Dec;58(12):4020–4029. [PMC free article] [PubMed]
  • Verkleij AJ, Zwaal RF, Roelofsen B, Comfurius P, Kastelijn D, van Deenen LL. The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochim Biophys Acta. 1973 Oct 11;323(2):178–193. [PubMed]
  • Wadström T, Möllby R. Studies on extracellular proteins from Staphylococcus aureus. VII. Studies on -haemolysin. Biochim Biophys Acta. 1971 Jul 21;242(1):308–320. [PubMed]
  • Wadström T, Möllby R. Some biological properties of purified staphylococcal haemolysins. Toxicon. 1972 Aug;10(5):511–519. [PubMed]
  • Weinberg ED. Iron and susceptibility to infectious disease. Science. 1974 May 31;184(4140):952–956. [PubMed]
  • Wiseman GM. The hemolysins of Staphylococcus aureus. Bacteriol Rev. 1975 Dec;39(4):317–344. [PMC free article] [PubMed]
  • Yamada A, Tsukagoshi N, Udaka S, Sasaki T, Makino S, Nakamura S, Little C, Tomita M, Ikezawa H. Nucleotide sequence and expression in Escherichia coli of the gene coding for sphingomyelinase of Bacillus cereus. Eur J Biochem. 1988 Aug 1;175(2):213–220. [PubMed]
  • Young PR, Snyder WR, McMahon RF. Inhibition of the Clostridium perfringens phospholipase C hydrolysis of a thiophosphate analog of lysophosphatidylcholine by micelle-bound ammonium and sulfonium cations. Lipids. 1991 Nov;26(11):957–959. [PubMed]
  • Young PR, Snyder WR, McMahon RF. Kinetic mechanism of Clostridium perfringens phospholipase C. Hydrolysis of a thiophosphate analogue of lysophosphatidylcholine. Biochem J. 1991 Dec 1;280(Pt 2):407–410. [PMC free article] [PubMed]

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