Alpha-toxin of Staphylococcus aureus.

Alpha-toxin, the major cytotoxic agent elaborated by Staphylococcus aureus, was the first bacterial exotoxin to be identified as a pore former. The protein is secreted as a single-chain, water-soluble molecule of Mr 33,000. At low concentrations (less than 100 nM), the toxin binds to as yet unidentified, high-affinity acceptor sites that have been detected on a variety of cells including rabbit erythrocytes, human platelets, monocytes and endothelial cells. At high concentrations, the toxin additionally binds via nonspecific absorption to lipid bilayers; it can thus damage both cells lacking significant numbers of the acceptor and protein-free artificial lipid bilayers. Membrane damage occurs in both cases after membrane-bound toxin molecules collide via lateral diffusion to form ring-structured hexamers. The latter insert spontaneously into the lipid bilayer to form discrete transmembrane pores of effective diameter 1 to 2 nm. A hypothetical model is advanced in which the pore is lined by amphiphilic beta-sheets, one surface of which interacts with lipids whereas the other repels apolar membrane constitutents to force open an aqueous passage. The detrimental effects of alpha-toxin are due not only to the death of susceptible targets, but also to the presence of secondary cellular reactions that can be triggered via Ca2+ influx through the pores. Well-studied phenomena include the stimulation of arachidonic acid metabolism, triggering of granule exocytosis, and contractile dysfunction. Such processes cause profound long-range disturbances such as development of pulmonary edema and promotion of blood coagulation.(ABSTRACT TRUNCATED AT 250 WORDS)

[1]  I. Kato,et al.  Chemical studies on staphylococcal alpha-toxin and its fragments. , 1980, Toxicon : official journal of the International Society on Toxinology.

[2]  S B Hladky,et al.  Ion transport across thin lipid membranes: a critical discussion of mechanisms in selected systems , 1972, Quarterly Reviews of Biophysics.

[3]  M. Mayer Mechanism of cytolysis by complement. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[4]  N. Thielens,et al.  Human complement protein C9 is a calcium binding protein. Structural and functional implications. , 1988, The Journal of biological chemistry.

[5]  R. Welch,et al.  Domains of Escherichia coli hemolysin (HlyA) involved in binding of calcium and erythrocyte membranes , 1990, Infection and immunity.

[6]  T. Foster,et al.  Virulence of protein A-deficient and alpha-toxin-deficient mutants of Staphylococcus aureus isolated by allele replacement , 1987, Infection and immunity.

[7]  S. Bhakdi,et al.  Damage to cell membranes by pore-forming bacterial cytolysins. , 1988, Progress in allergy.

[8]  K. Downing,et al.  Structure of PhoE porin in projection at 3.5 A resolution. , 1990, Journal of structural biology.

[9]  K. F. Chan,et al.  Staphylococcus aureus alpha-toxin. 2. Reduction of epidermal growth factor receptor affinity in PC12 cells. , 1987, Toxicon : official journal of the International Society on Toxinology.

[10]  D. Aunis,et al.  Characterization of hormone and protein release from alpha-toxin-permeabilized chromaffin cells in primary culture. , 1986, The Journal of biological chemistry.

[11]  C. Pederzolli,et al.  Modification of lysine residues of Staphylococcus aureus alpha-toxin: effects on its channel-forming properties. , 1991, The Journal of membrane biology.

[12]  G. Ahnert-Hilger,et al.  Ca2+-stimulated catecholamine release from alpha-toxin-permeabilized PC12 cells: biochemical evidence for exocytosis and its modulation by protein kinase C and G proteins. , 1987, Biochemistry.

[13]  J. Freer,et al.  Interaction of staphylococcal alpha-toxin with artificial and natural membranes. , 1968, Journal of bacteriology.

[14]  P. Owen,et al.  Multiple forms of staphylococcal alpha-toxin. , 1972, Journal of medical microbiology.

[15]  M. Thelestam,et al.  Staphylococcal alpha toxin--recent advances. , 1988, Toxicon : official journal of the International Society on Toxinology.

[16]  G. Menestrina,et al.  Staphylococcal alpha-toxin increases the permeability of lipid vesicles by cholesterol- and pH-dependent assembly of oligomeric channels. , 1989, European journal of biochemistry.

[17]  N. Suttorp,et al.  Effect of staphylococcal alpha-toxin on intracellular Ca2+ in polymorphonuclear leukocytes , 1988, Infection and immunity.

[18]  F. Baleux,et al.  Reaction of staphylococcal alpha-toxin with peptide-induced antibodies , 1989, Infection and immunity.

[19]  G. Weissmann,et al.  Staphylococcal Alpha-Toxin: Effects on Artificial Lipid Spherules , 1966, Science.

[20]  F. Burnet The production of staphylococcal toxin , 1930 .

[21]  C. Esmon,et al.  On the mechanism by which complement proteins C5b-9 increase platelet prothrombinase activity. , 1986, The Journal of biological chemistry.

[22]  S. Szmigielski,et al.  Brain bioelectric activity in staphylococcal α-hemolysin intoxication , 1968 .

[23]  S. Harshman,et al.  Purification and properties of two forms of staphylococcal toxin. , 1973, Biochemistry.

[24]  S. Bhakdi,et al.  Staphylococcus aureus alpha-toxin. Dual mechanism of binding to target cells. , 1991, The Journal of biological chemistry.

[25]  J. Nishimura,et al.  Norepinephrine and GTP-gamma-S increase myofilament Ca2+ sensitivity in alpha-toxin permeabilized arterial smooth muscle. , 1988, Biochemical and biophysical research communications.

[26]  S. Bhakdi,et al.  Correlation between toxin binding and hemolytic activity in membrane damage by staphylococcal alpha-toxin , 1984, Infection and immunity.

[27]  R. Möllby,et al.  Survival of cultured cells after functional and structural disorganization of plasma membrane by bacterial haemolysins and phospholipases. , 1983, Toxicon : official journal of the International Society on Toxinology.

[28]  C. Haest,et al.  Bacterial cytotoxins, amphotericin B and local anesthetics enhance transbilayer mobility of phospholipids in erythrocyte membranes. Consequences for phospholipid asymmetry. , 1986, Biochimica et biophysica acta.

[29]  L. Cooper,et al.  Heat stability and species range of purified staphylococcal alpha-toxin. , 1966, Journal of Bacteriology.

[30]  M. Thelestam,et al.  Oligomerization of 3H-labelled staphylococcal alpha-toxin and fragments on adrenocortical Y1 tumour cells. , 1988, Microbial pathogenesis.

[31]  G. Wiseman The hemolysins of Staphylococcus aureus , 1975, Bacteriological reviews.

[32]  S. Bhakdi,et al.  Release of interleukin-1 beta associated with potent cytocidal action of staphylococcal alpha-toxin on human monocytes , 1989, Infection and immunity.

[33]  S. Bhakdi,et al.  Mechanism of complement cytolysis and the concept of channel-forming proteins. , 1984, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  S. Arvidson,et al.  MUTANTS OF STAPHYLOCOCCUS AUREUS AFFECTED IN THE REGULATION OF EXOPROTEIN SYNTHESIS , 1980 .

[35]  N. Blanckaert,et al.  Endogenous esterification of bilirubin by liver microsomes. Evidence for an intramicrosomal pool of UDP-glucose and lumenal orientation of bilirubin UDP-glycosyltransferase. , 1987, The Journal of biological chemistry.

[36]  K. Kim,et al.  Factors Affecting Interaction of Staphylococcal Alpha Toxin with Membranes , 1972, Infection and immunity.

[37]  J. Freer,et al.  Binding of 125I-alpha toxin of Staphylococcus aureus to erythrocytes. , 1984, Journal of medical microbiology.

[38]  H. B. Fackrell,et al.  Inhibition of staphylococcal alpha-toxin by covalent modification of an arginine residue. , 1987, Biochimica et biophysica acta.

[39]  P. Sims,et al.  Complement C5b-9-stimulated platelet secretion is associated with a Ca2+-initiated activation of cellular protein kinases. , 1987, The Journal of biological chemistry.

[40]  S Bhakdi,et al.  Staphylococcal alpha-toxin: oligomerization of hydrophilic monomers to form amphiphilic hexamers induced through contact with deoxycholate detergent micelles. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[41]  H. Schrezenmeier,et al.  Inactivation of a T cell receptor-associated GTP-binding protein by antibody-induced modulation of the T cell receptor/CD3 complex , 1988, The Journal of experimental medicine.

[42]  W. Seeger,et al.  Staphylococcal alpha-toxin-induced vascular leakage in isolated perfused rabbit lungs. , 1990, Laboratory investigation; a journal of technical methods and pathology.

[43]  N. Fairweather,et al.  Cloning, expression, and mapping of the Staphylococcus aureus alpha-hemolysin determinant in Escherichia coli K-12 , 1983, Infection and immunity.

[44]  K. Preissner,et al.  Staphylococcus aureus alpha-toxin attack on human platelets promotes assembly of the prothrombinase complex. , 1990, The Journal of biological chemistry.

[45]  W. Seeger,et al.  Bacterial exotoxins and endothelial permeability for water and albumin in vitro. , 1988, The American journal of physiology.

[46]  Yoshie Suzuki,et al.  Effects of Lectins on the Hemolysis of Rabbit Erythrocytes by Staphylococcal Alpha Toxin , 1977, Microbiology and immunology.

[47]  C. Adlam,et al.  A histopathological study of the effects of highly purified staphlococcal alpha and beta toxins on the lactating mammary gland and skin of the rabbit. , 1979, Journal of comparative pathology.

[48]  I. Kato Inhibitory effect of a lethal toxic fragment of staphylococcal alpha-toxin on cyclic AMP-dependent protein kinase activity. , 1979, Biochimica et biophysica acta.

[49]  I. Kato,et al.  Purification and some properties of a lethal toxic fragment of staphylococcal alpha-toxin by tryptic digestion. , 1978, Biochimica et biophysica acta.

[50]  S. Szmigielski,et al.  Distribution of 131-I-labelled staphylococcal alpha-hemolysin in the rabbit. , 1969, Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. 1. Abt. Medizinisch-hygienische Bakteriologie, Virusforschung und Parasitologie. Originale.

[51]  I. Kato,et al.  Inhibitory effect of flavin mononucleotide on the hemolysis of rabbit erythrocytes by staphylococcal alpha-toxin , 1975, Infection and immunity.

[52]  M. O'Reilly,et al.  Roles of alpha-toxin and beta-toxin in virulence of Staphylococcus aureus for the mouse mammary gland , 1989, Infection and immunity.

[53]  S. Szmigielski,et al.  Histochemical demonstration of changes in enzymatic activity of KB cells produced by staphylococcal alpha and beta hemolysins. , 1965, The Journal of infectious diseases.

[54]  E. Carlson,et al.  Production of gamma-hemolysin and lack of production of alpha-hemolysin by Staphylococcus aureus strains associated with toxic shock syndrome , 1988, Journal of clinical microbiology.

[55]  M. Rogolsky Nonenteric Toxins of Staphylococcus aureus , 1979, Microbiological reviews.

[56]  R. Möllby,et al.  Sensitive assay for detection of toxin-induced damage to the cytoplasmic membrane of human diploid fibroblasts , 1975, Infection and immunity.

[57]  S. Harshman,et al.  Physical and chemical studies on staphylococcal -toxins A and B . , 1973, Biochemistry.

[58]  M. Bondurant,et al.  Susceptibility to staphylococcal alpha-toxin of Friend virus-infected murine erythroblasts during differentiation , 1985, Infection and immunity.

[59]  M. Thelestam,et al.  Early events in the action of staphylococcal alpha-toxin on the plasma membrane of adrenocortical Y1 tumor cells , 1986, Infection and immunity.

[60]  J. Freer,et al.  Physical states of staphylococcal alpha-toxin. , 1967, Journal of bacteriology.

[61]  M. O'Reilly,et al.  Cryptic alpha-toxin gene in toxic shock syndrome and septicaemia strains of Staphylococcus aureus. , 1990, Molecular microbiology.

[62]  J. C. M. van der Vijver,et al.  A study of virulence factors with induced mutants of Staphylococcus aureus. , 1975, Journal of medical microbiology.

[63]  F. Koo,et al.  Staphylococcal toxins: screening of burn wound isolates and evidence for alpha-haemolysin production in the burn wound. , 1987, Burns, including thermal injury.

[64]  R. Harrison,et al.  Staphylococcal α-toxin: A structure-function study using a monoclonal antibody , 1986 .

[65]  L. L. Schwartz,et al.  Isolation and composition of staphylococcal alpha toxin. , 1963, Journal of general microbiology.

[66]  S. Kinsky Antibiotic interaction with model membranes. , 1970, Annual review of pharmacology.

[67]  M. Watanabe,et al.  Membrane-damaging action of staphylococcal alpha-toxin on phospholipid-cholesterol liposomes. , 1987, Biochimica et biophysica acta.

[68]  N. Sugg,et al.  Effect of calcium ions on staphylococcal alpha-toxin-induced hemolysis of rabbit erythrocytes , 1985, Infection and immunity.

[69]  M. Lindberg,et al.  Virulence of Staphylococcus aureus in a mouse mastitis model: studies of alpha hemolysin, coagulase, and protein A as possible virulence determinants with protoplast fusion and gene cloning , 1985, Infection and immunity.

[70]  F. Kapral,et al.  Formation of intraperitoneal abscesses by Staphylococcus aureus , 1980, Infection and immunity.

[71]  E. Duflot,et al.  Staphylococcal alpha-toxin: a study of membrane penetration and pore formation. , 1989, The Journal of biological chemistry.

[72]  S. Bhakdi,et al.  Human hyperimmune globulin protects against the cytotoxic action of staphylococcal alpha-toxin in vitro and in vivo , 1989, Infection and immunity.

[73]  S. Szmigielski,et al.  Injury of myelin sheaths in isolated rabbit vagus nerves by α-toxin of Staphylococcus aureus , 1979 .

[74]  R. Möllby,et al.  Effects of Staphylococcal Alpha-, Beta-, Delta-, and Gamma-Hemolysins on Human Diploid Fibroblasts and HeLa Cells: Evaluation of a New Quantitative Assay for Measuring Cell Damage , 1973, Infection and immunity.

[75]  S. Bhakdi,et al.  Minimal requirements for exocytosis. A study using PC 12 cells permeabilized with staphylococcal alpha-toxin. , 1985, The Journal of biological chemistry.

[76]  M. Raff,et al.  Detoxification of staphylococcal alpha toxin by hydrocortisone and methylprednisolone. , 1978, Journal of medical microbiology.

[77]  S. Cohen,et al.  ACTION OF STAPHYLOCOCCAL TOXIN ON HUMAN PLATELETS. , 1964, The Journal of infectious diseases.

[78]  B. Petrini,et al.  Activation of human lymphocytes in vitro by membrane-damaging toxins from Staphylococcus aureus , 1981, Infection and immunity.

[79]  M. Thelestam,et al.  Crystalline layers and three-dimensional structure ofStaphylococcus aureus α-toxin , 1990 .

[80]  G. Gray,et al.  Primary sequence of the alpha-toxin gene from Staphylococcus aureus wood 46 , 1984, Infection and immunity.

[81]  E. Chiancone,et al.  Ultracentrifugal Analysis of Staphylococcal Alpha Toxin , 1971, Journal of bacteriology.

[82]  H. Jörnvall,et al.  Characterization of domain borders and of a naturally occurring major fragment of staphylococcal α‐toxin , 1987, FEBS letters.

[83]  G. Menestrina,et al.  Membrane damage by hemolytic viruses, toxins, complement, and other cytotoxic agents. A common mechanism blocked by divalent cations. , 1986, The Journal of biological chemistry.

[84]  E. Podack,et al.  Cytolysis by Ca-permeable transmembrane channels. Pore formation causes extensive DNA degradation and cell lysis , 1989, The Journal of experimental medicine.

[85]  A. W. Bernheimer Interactions between membranes and cytolytic bacterial toxins , 1974 .

[86]  F. Burnet The exotoxins of Staphylococcus pyogenes aureus , 1929 .

[87]  P. Cassidy,et al.  Iodination of a tyrosyl residue in staphylococcal alpha-toxin. , 1976, Biochemistry.

[88]  I. Kato,et al.  Inhibition of adenosine 3',5'-monophosphate-dependent protein kinase by staphylococcal alpha-toxin , 1979, Infection and immunity.

[89]  J. Freer,et al.  Effects of staphylococcal -toxin on the structure of erythrocyte membranes: a biochemical and freeze-etching study. , 1973, Journal of general microbiology.

[90]  M. Manohar,et al.  Platelet Damaging Factor, a Fifth Activity of Staphylococcal α-Toxin , 1967 .

[91]  P. Cassidy,et al.  Characterization of detergent-solubilized iodine-125-labeled alpha-toxin bound to rabbit erythrocytes and mouse diaphragm muscle. , 1979, Biochemistry.

[92]  S. Bhakdi,et al.  Damage to mammalian cells by proteins that form transmembrane pores. , 1987, Reviews of physiology, biochemistry and pharmacology.

[93]  M. Yoshikawa,et al.  Pleiotropic Alteration of Activities of Several Toxins and Enzymes in Mutants of Staphylococcus aureus , 1974, Journal of bacteriology.

[94]  I. Maharaj,et al.  Rabbit erythrocyte band 3: a receptor for staphylococcal alpha toxin. , 1980, Canadian journal of microbiology.

[95]  M. Naiki,et al.  Ganglioside and rabbit erythrocyte membrane receptor for staphylococcal alpha-toxin , 1976, Infection and immunity.

[96]  S. Orrenius,et al.  Cellular signalling in programmed cell death (apoptosis). , 1990, Immunology today.

[97]  R. Tweten,et al.  Transport and processing of staphylococcal alpha-toxin , 1983, Journal of bacteriology.

[98]  J. Arbuthnott,et al.  Purification of staphylococcus alpha‐toxin , 1963 .

[99]  J. Freer,et al.  Toxins of Staphylococcus aureus. , 1982, Pharmacology & therapeutics.

[100]  S. Mudd,et al.  ROLE OF ALPHA-TOXIN IN LESION FORMATION BY STAPHYLOCOCCUS AUREUS ON SUTURES SUBCUTANEOUSLY IMPLANTED IN MICE , 1963, Journal of bacteriology.

[101]  G. Coleman Pleiotropic compensation in the regulation of extracellular protein formation by a low alpha-toxin-producing variant of Staphylococcus aureus (Wood 46). , 1981, Journal of general microbiology.

[102]  E. Leake,et al.  Toxicity of staphylococcal alpha toxin for rabbit alveolar macrophages , 1983, Infection and immunity.

[103]  M. O'Reilly,et al.  Inactivation of the alpha-haemolysin gene of Staphylococcus aureus 8325-4 by site-directed mutagenesis and studies on the expression of its haemolysins. , 1986, Microbial pathogenesis.

[104]  A. J. Kenyon,et al.  THE CHARACTERIZATION OF STAPHYLOCOCCAL TOXINS : II. THE ISOLATION AND CHARACTERIZATION OF A HOMOGENEOUS STAPHYLOCOCCAL PROTEIN POSSESSING ALPHA HEMOLYTIC, DERMONECROTIC, LETHAL, AND LEUCOCIDAL ACTIVITIES. , 1962 .

[105]  G. Colacicco,et al.  Lipid monolayers. Interactions with staphylococcal alpha-toxin. , 1971, Biochimica et biophysica acta.

[106]  S. Bhakdi,et al.  Staphylococcal α toxin promotes blood coagulation via attack on human platelets , 1988, The Journal of experimental medicine.

[107]  S. Bhakdi,et al.  Quantitation of monomeric and oligomeric forms of membrane-bound staphylococcal alpha-toxin by enzyme-linked immunosorbent assay with a neutralizing monoclonal antibody , 1987, Infection and immunity.

[108]  B. Strandvik,et al.  Antibodies to Staphylococcal Teichoic Acid and Alpha Toxin in Patients with Cystic Fibrosis , 1986, Acta paediatrica Scandinavica.

[109]  S. Bhakdi,et al.  Potent leukocidal action of Escherichia coli hemolysin mediated by permeabilization of target cell membranes , 1989, The Journal of experimental medicine.

[110]  G. Wiseman,et al.  Further observations on the mode of action of the alpha toxin of Staphylococcus aureus "Wood-46". , 1972, Canadian journal of microbiology.

[111]  H. Bayley,et al.  Secondary structure and assembly mechanism of an oligomeric channel protein. , 1985, Biochemistry.

[112]  G. Wiseman,et al.  Trypsin-mediated activation of the alpha-haemolysin of Staphylococcus aureus. , 1975, Journal of medical microbiology.

[113]  S. Bhakdi,et al.  Quantitative analysis of the binding and oligomerization of staphylococcal alpha-toxin in target erythrocyte membranes , 1987, Infection and immunity.

[114]  J. Alouf,et al.  Photolabeling of staphylococcal α-toxin from within rabbit erythrocyte membranes , 1983 .

[115]  G. Coleman,et al.  Comparison of the patterns of increased in alpha-toxin and total extracellular protein by Staphylococcus aureus (Wood 46) grown in media supporting widely differing growth characteristics , 1977, Infection and immunity.

[116]  P. A. van der Merwe,et al.  Mechanisms of luteinizing-hormone exocytosis in Staphylococcus aureus-alpha-toxin-permeabilized sheep gonadotropes. , 1989, The Biochemical journal.

[117]  P. Pattee Chromosomal map location of the alpha-hemolysin structural gene in Staphylococcus aureus NCTC 8325 , 1986, Infection and immunity.

[118]  L. Cooper,et al.  HEMOLYSIS OF RABBIT ERYTHROCYTES BY PURIFIED STAPHYLOCOCCAL ALPHA-TOXIN I , 1964, Journal of bacteriology.

[119]  M. Blankenship,et al.  Disruption of myelin sheaths in mouse brain in vitro and in vivo by staphylococcal α-toxin , 1985 .

[120]  P. Pattee,et al.  Identification of a chromosomal determinant of alpha-toxin production in Staphylococcus aureus , 1980, Infection and immunity.

[121]  T. Birkbeck,et al.  Effect of phenethyl alcohol on Staphylococcus aureus alpha-lysin production , 1985, Infection and immunity.

[122]  L. L. Schwartz,et al.  EFFECT OF STAPHYLOCOCCAL AND OTHER BACTERIAL TOXINS ON PLATELETS IN VITRO. , 1965, The Journal of pathology and bacteriology.

[123]  P. Peterson,et al.  Biological effects of the interaction of staphylococcal alpha-toxin with human serum , 1982, Infection and immunity.

[124]  M. Kazatchkine,et al.  Relative inefficiency of terminal complement activation. , 1988, Journal of immunology.

[125]  B. McEwen,et al.  Permeabilization of rat hepatocytes with Staphylococcus aureus alpha- toxin , 1985, The Journal of cell biology.

[126]  C. Adlam,et al.  Effect immunization with highly purified alpha- and beta-toxins on staphylococcal mastitis in rabbits , 1977, Infection and immunity.

[127]  W. Seeger,et al.  Mechanism of leukotriene generation in polymorphonuclear leukocytes by staphylococcal alpha-toxin , 1987, Infection and immunity.

[128]  M. Thelestam,et al.  Distribution of 3H-labeled staphylococcal alpha-toxin and a toxin fragment in mice , 1987, Infection and immunity.