Exotoxins ofStaphylococcus aureus

Clinical Microbiology Reviews - Tập 13 Số 1 - Trang 16-34 - 2000
Martin M. Dinges1, Paul M. Orwin1, Patrick M. Schlievert1
1Department of Microbiology, University of Minnesota School of Medicine, Minneapolis, Minnesota 55455

Tóm tắt

SUMMARYThis article reviews the literature regarding the structure and function of two types of exotoxins expressed by Staphylococcus aureus, pyrogenic toxin superantigens (PTSAgs) and hemolysins. The molecular basis of PTSAg toxicity is presented in the context of two diseases known to be caused by these exotoxins: toxic shock syndrome and staphylococcal food poisoning. The family of staphylococcal PTSAgs presently includes toxic shock syndrome toxin-1 (TSST-1) and most of the staphylococcal enterotoxins (SEs) (SEA, SEB, SEC, SED, SEE, SEG, and SEH). As the name implies, the PTSAgs are multifunctional proteins that invariably exhibit lethal activity, pyrogenicity, superantigenicity, and the capacity to induce lethal hypersensitivity to endotoxin. Other properties exhibited by one or more staphylococcal PTSAgs include emetic activity (SEs) and penetration across mucosal barriers (TSST-1). A detailed review of the molecular mechanisms underlying the toxicity of the staphylococcal hemolysins is also presented.

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10.1038/367094a0

Alber G. Hammer D. Fleischer B. Relationship between enterotoxic- and T lymphocyte-stimulating activity of staphylococcal enterotoxin B. J. Immunol. 144 1990 4501 4506

Alber G. Scheuber P. H. Reck B. Sailer-Kramer B. Hartmann A. Hammer D. K. Role of substance P in immediate-type skin reactions induced by staphylococcal enterotoxin B in unsensitized monkeys. J. Allergy Clin. Immunol. 84 1989 880 885

Altemeier W. A. Lewis S. A. Schlievert P. M. Bergdoll M. S. Bjornson H. J. Staneck J. L. Crass B. A. Staphylococcus aureus associated with toxic shock syndrome: phage typing and toxin capability tested. Ann. Intern. Med. 96 1982 978 982

10.1159/000235535

Arvidson S. Janzon L. Lofdahl S. The role of the δ-hemolysin gene ( hld ) in the agr -dependent regulation of exoprotein synthesis in Staphylococcus aureus Molecular biology of the staphylococci. Novick R. P. 1990 419 431 VCH Publishers Inc. New York N.Y

Beery J. T. Taylor S. Schlunz L. R. Freed R. C. Bergdoll M. S. Effects of staphylococcal enterotoxin A on the rat gastrointestinal tract. Infect. Immun. 44 1994 234 240

Beisel W. R. Pathophysiology of staphylococcal enterotoxin, type B, (SEB) toxemia after intravenous administration to monkeys. Toxicon 10 1972 433 440

Belmonte G. Cescatti L. Ferrari B. Nicolussi T. Ropele M. Menestrina G. Pore-formation by Staphylococcus aureus alpha-toxin in lipid bilayers: temperature and toxin concentration dependence. Eur. J. Biophys. 14 1987 349 358

Bergdoll M. S. Enterotoxins Staphylococci and staphylococcal infections. Easmon C. S. F. Adlam C. 1983 559 598 Academic Press Ltd. London United Kingdom

10.1016/S0140-6736(81)92186-3

Bergdoll M. S. Robbins R. N. Weiss K. Borja C. R. Huang I. Y. Chu F. S. The staphylococcal enterotoxins: similarities. Contrib. Microbiol. Immunol. 1 1973 390 396

Bergdoll M. S. Schlievert P. M. Toxic-shock syndrome toxin. Lancet ii 1984 691

Bernheimer A. W. Avigad L. S. Kim K. S. Staphylococcal sphingomyelinase (beta hemolysin). Ann. N. Y. Acad. Sci. 236 1974 292 306

10.1099/00221287-30-3-455

10.1128/iai.46.2.318-323.1984

10.1084/jem.168.2.527

10.1128/mr.55.4.733-751.1991

Birbeck T. H. Freer J. H. Purification and assay of staphylococcal δ-lysin. Methods Enzymol. 165 1988 16 22

10.1128/iai.58.9.3020-3028.1990

10.1016/S0021-9258(18)66787-0

Blomster-Hautamaa D. A. Kreiswirth B. N. Novick R. P. Schlievert P. M. The resolution of highly purified toxic-shock syndrome toxin-1 (TSST-1) into two distinct proteins by isoelectric focusing. Biochemistry 25 1986 54 59

10.1016/S0076-6879(88)65009-9

10.3109/10408419009105728

Bohach G. A. Jablonski L. M. Deobald C. F. Chi Y. I. Stauffacher C. V. Functional domains of staphylococcal enterotoxins Molecular approaches to food safety: issues involving toxic microorganisms. Ecklund M. Richard J. L. Mise K. 1995 339 356 Alaken Inc. Fort Collins Colo

Bohach G. A. Dinges M. M. Mitchell D. T. Ohlendorf D. H. Schlievert P. M. Exotoxins The staphylococci in human disease. Crossley K. B. Archer G. L. 1997 83 111 Churchill Livingstone Inc. New York N.Y

Bohach G. A. Jablonski L. Roggiani M. Sadler I. Schlievert P. M. Mitchell D. Ohlendorf D. Biological activity of pyrogenic toxins delivered at the mucosal surface European Conference on Toxic Shock Syndrome. International Congress and Symposium Series 229. Arbuthnott J. Furman B. 1998 170 172 Royal Society of Medicine Press Ltd New York N.Y

10.1128/iai.61.3.793-799.1993

10.1128/iai.63.2.509-515.1995

Campbell W. N. Fitzpatrick M. Ding X. Jett M. Liemski P. Goldblum S. E. SEB is cytotoxic and alters EC barrier function through protein tyrosine phosphorylation in vitro. Am. J. Physiol. 273 1997 L31 L39

Canonico P. G. Van Zweiten M. J. Swelling of mitochondria from rabbit liver induced by staphylococcal enterotoxin B. J. Infect. Dis. 124 1971 372 378

Centers for Disease Control and Prevention Case definitions for infectious conditions under public health surveillance. Morbid. Mortal. Weekly Rep. 46 RR-10 1997 1 55

Chesney P. J. Clinical aspects and spectrum of illness of toxic shock syndrome: overview. Rev. Infect. Dis. 11 1989 S1 S7

Chesney P. J. Toxic shock syndrome The staphylococci in human disease. Crossley K. B. Archer G. L. 1997 509 525 Churchill Livingstone Inc. New York N.Y

Chesney R. W. Chesney P. J. Davis J. P. Segar W. E. Renal manifestations of the staphylococcal toxic-shock syndrome. Am. J. Med. 71 1981 583 588

Chesney R. W. McCarron D. M. Haddad J. G. Hawker C. D. DiBella F. P. Chesney P. J. Davis J. P. Pathogenic mechanisms of the hypocalcemia of the staphylococcal toxic-shock syndrome. J. Lab. Clin. Med. 101 1983 576 585

10.1073/pnas.89.14.6462

Choi Y. Lafferty J. A. Clements J. R. Todd J. K. Gelfand E. W. Kappler J. Marrack P. Kotzin B. L. Selective expansion of T cells expressing Vβ2 in toxic shock syndrome. J. Exp. Med. 172 1990 981 984

Coleman D. C. Arbuthnott J. P. Pomeroy H. M. Birbeck H. Cloning and expression in Escherichia coli and Staphylococcus aureus of the beta-lysin determinant from Staphylococcus aureus: evidence that bacteriophage conversion of beta-lysin activity is caused by insertional inactivation of the beta-lysin determinant. Microb. Pathog. 1 1986 549 564

10.1128/iai.62.8.3184-3188.1994

Cone L. A. Woodard D. R. Byrd R. G. Schulz K. Kopp S. M. Schlievert P. M. A recalcitrant, erythematous, desquamating disorder associated with toxin-producing staphylococci in patients with AIDS. J. Infect. Dis. 165 1991 638 643

10.1128/jb.170.7.2954-2960.1988

10.1056/NEJM198012183032501

Deresiewicz R. L. Staphylococcal toxic shock syndrome Superantigens: molecular biology immunology and relevance to human disease. Leung D. Y. M. Huber B. T. Schlievert P. M. 1996 435 479 Marcel Dekker Inc. New York N.Y

Dhople V. M. Nagaraj R. δ-toxin, unlike melittin, has only hemolytic activity and no antimicrobial activity: rationalization of this specific biological activity. Biosci. Rep. 13 1993 245 250

Reference deleted.

Dinges M. Jessurun J. Schlievert P. Comparisons of mouse and rabbit models of toxic shock syndrome European Conference on Toxic Shock Syndrome. International Congress and Symposium Series 229. Arbuthnott J. Furman B. 1998 167 168 Royal Society of Medicine Press Ltd New York N.Y

Doery H. M. Magnuson B. J. Cheyne I. M. Galasekharam J. A phospholipase in staphylococcal toxin which hydrolizes sphingomyelin. Nature (London) 198 1963 1091 1093

Doery H. M. Magnuson B. J. Galasekharam J. Pearson J. E. The properties of phospholipase enzymes in staphylococcal toxins. J. Gen. Microbiol. 40 1965 283 296

Driessen C. Hirv K. Kircherner H. Rink L. Zinc regulates cytokine induction by superantigens and lipopolysaccharide. Immunology 84 1995 272 277

Earhart C. A. Prasad G. S. Murray D. L. Novick R. P. Schlievert P. M. Ohlendorf D. H. Growth and analysis of crystal forms of toxic shock syndrome toxin-1. Proteins 17 1993 329 334

Earhart C. A. Mitchell D. T. Murray D. L. Pinheiro D. M. Matsumara M. Schlievert P. M. Ohlendorf D. H. Structures of five mutants of toxic shock syndrome toxin-1 with reduced biological activity. Biochemistry 37 1998 7194 7202

10.1128/iai.57.7.2230-2236.1989

10.1038/384188a0

10.1084/jem.167.5.1697

Fraser J. D. Lowe S. Irwin M. J. Gascoigne N. R. J. Hudson K. R. Structural model of staphylococcal enterotoxin A interaction with MHC class II antigens Superantigens: a pathogen's view of the immune system. Huber B. T. Palmer E. 1993 7 29 Cold Spring Harbor Laboratory Press Plainview N.Y

10.1016/0163-7258(82)90042-0

Freer J. H. Birbeck T. H. Possible conformation of delta-lysin, a membrane-damaging peptide of Staphylococcus aureus. J. Theor. Biol. 94 1982 535 540

Fujikawa H. Igarashi H. Usami H. Tanaka S. Tamura H. Clearance of endotoxin from blood of rabbits injected with staphylococcal toxic shock syndrome toxin-1. Infect. Immun. 52 1986 134 137

Glenny A. T. Stevens N. F. Staphylococcal toxins and antitoxins. J. Pathol. Bacteriol. 40 1935 201 210

Gottfried A. Scheuber P. H. Reck B. Sailer-Kramer B. Hartmann A. Hammer D. K. Role of substance P in immediate-type skin reactions induced by staphylococcal enterotoxin B in unsensitized monkeys. J. Allergy Clin. Immunol. 84 1989 880 885

Gouaux E. α-Hemolysin from Staphylococcus aureus: an archetype of β-barrel, channel forming toxins. J. Struct. Biol. 121 1998 110 122

Gouaux J. E. Braha O. Hobaugh M. R. Song L. Cheley S. Shustak C. Bayley H. Subunit stoichiometry of staphylococcal alpha-hemolysin in crystals and on membranes: a heptameric transmembrane pore. Proc. Natl. Acad. Sci. USA 91 1994 12828 12831

10.1016/S0016-5085(81)80120-5

10.1128/iai.46.2.615-618.1984

Hamad A. R. Marrack P. Kappler J. W. Transcytosis of staphylococcal superantigen toxins. J. Exp. Med. 185 1997 1447 1454

10.1128/iai.61.8.3175-3183.1993

Harshman S. Sugg N. Cassiday P. Preparation and purification of staphylococcal alpha toxin. Methods Enzymol. 165 1988 3 7

10.1016/S0021-9258(19)47358-4

10.1128/iai.62.8.3396-3407.1994

Holmberg S. D. Blake P. A. Staphylococcal food poisoning in the United States. JAMA 251 1984 487 489

Hovde C. J. Marr J. C. Hoffmann M. L. Hackett S. P. Chi Y. I. Crum K. K. Stevens D. L. Stauffacher C. V. Bohach G. A. Investigation of the role of the disulfide bond in activity and structure of staphylococcal enterotoxin C1. Mol. Microbiol. 13 1994 897 909

Hurley J. M. Shimonkevitz R. Hanagan A. Enney K. Boen E. Mahmstrom S. Kotzin B. L. Matsumura M. Identification of class II major histocompatibility complex and T cell receptor binding sites in the superantigen toxic shock syndrome toxin 1. J. Exp. Med. 181 1995 2229 2235

10.1146/annurev.mi.43.100189.002111

Ikejima T. Okusawa S. van der Meer J. W. Dinarello C. A. Induction by toxic-shock-syndrome-toxin-1 of a circulating tumor necrosis factor-like substance in rabbits and of immunoreactive tumor necrosis factor and interleukin-1 from human mononuclear cells. J. Infect. Dis. 158 1988 1017 1025

Jardetzky T. S. Brown J. H. Gorga J. C. Stern L. J. Urban R. G. Chi Y. I. Stauffacher C. V. Strominger J. L. Wiley D. C. Three-dimensional structure of a human class II histocompatibility molecule complexed with superantigen. Nature (London) 368 1994 711 718

10.1128/iai.58.11.3494-3499.1990

10.1128/iai.62.4.1304-1312.1994

Kamio Y. Rahman A. Nariya H. Ozawa T. Izaki K. The two staphylococcal bi-component toxins, leukocidin and gamma-hemolysin, share one component in common. FEBS Lett. 321 1993 15 18

Kass E. H. Parsonnet J. Mills J. T. Role of magnesium ions in the pathogenesis of toxic shock syndrome. Trans. Assoc. Am. Physiol. 100 1987 158 163

Kass E. H. Schlievert P. M. Parsonnet J. Mills J. T. Effect of magnesium on production of toxic-shock syndrome toxin-1: a collaborative study. J. Infect. Dis. 158 1988 44 51

Keane W. F. Gekker G. Schlievert P. M. Peterson P. K. Enhancement of endotoxin-induced isolated renal tubular cell injury by toxic shock syndrome toxin 1. Am. J. Pathol. 122 1986 169 176

Kent T. H. Staphylococcal enterotoxin gastroenteritis in rhesus monkeys. Am. J. Pathol. 48 1966 387 407

10.1126/science.7997880

10.1128/iai.60.7.2969-2975.1992

Konig B. Prevost G. Konig W. Composition of staphylococcal bi-component toxins determines pathophysiological reactions. J. Med. Microbiol. 46 1997 479 485

10.1016/S0065-2776(08)60534-9

Krakauer T. Cell adhesion molecules are co-receptors for staphylococcal enterotoxin B-induced T-cell activation and cytokine production. Immunol. Lett. 39 1994 121 125

10.1128/iai.3.3.449-465.1971

Kushnaryov V. M. MacDonald H. S. Reiser R. F. Bergdoll M. S. Reaction of toxic shock syndrome toxin 1 with endothelium of human umbilical cord vein. Rev. Infect. Dis. 11 1989 S282 S288

10.1128/CMR.12.2.224

Larkin S. M. Williams D. N. Osterholm M. T. Tofte R. W. Posalaky Z. Toxic shock syndrome: clinical, laboratory, and pathologic findings in nine fatal cases. Ann. Intern. Med. 96 1982 858 864

Lee K. H. Fitton J. E. Wuthrich K. Nuclear magnetic resonance investigation of the conformation of δ-haemolysin bound to dodecylphosphocholine micelles. Biochim. Biophys. Acta 911 1987 144 153

10.1128/jcm.27.8.1890-1892.1989

10.1128/iai.59.3.879-884.1991

Lee P. K. Kreiswirth B. N. Deringer J. R. Projan S. J. Eisner W. Smith B. L. Carlson E. Novick R. P. Schlievert P. M. Nucleotide sequences and biological properties of toxic shock syndrome toxin-1 from ovine- and bovine-associated Staphylococcus aureus. J. Infect. Dis. 165 1992 1056 1063

10.1093/infdis/164.4.711

Leist M. Gantner F. Bohlinger I. Germann P. G. Tiegs G. Wendel A. Murine hepatocyte apoptosis induced in vitro and in vivo by TNF-α requires transcriptional arrest. J. Immunol. 153 1994 1778 1788

10.1128/iai.60.9.3747-3755.1992

Leung D. Y. M. Meissner H. C. Fulton D. R. Murray D. L. Kotzin B. L. Schlievert P. M. Toxic shock syndrome toxin-secreting Staphylococcus aureus in Kawasaki syndrome. Lancet 342 1993 1385 1388

Li H. Llera A. Tsuchiya D. Leder L. Ysern X. Schlievert P. M. Karjalainen K. Mariuzza R. A. Three-dimensional structure of the complex between a T cell receptor beta chain and the superantigen staphylococcal enterotoxin B. Immunity 9 1998 807 816

10.1046/j.1365-2958.1998.00947.x

Low D. K. R. Freer J. H. The purification of β-lysin (sphingomyelinase C) from Staphylococcus aureus. FEMS Lett. 2 1977 139 143

10.1001/jama.1987.03390080043027

10.1126/science.2185544

10.1084/jem.171.2.455

Melish M. Fukunaga C. Murata S. TSST-1 dissemination in a vaginal model for TSS European Conference on Toxic Shock Syndrome. International Congress and Symposium Series 229. Arbuthnott J. Furman B. 1998 169 Royal Society of Medicine Press Ltd New York N.Y

Melish M. E. S. Murata C. Fukunaga K. Frogner S. Hirata and C. Wong. Endotoxin is not an essential mediator of toxic shock syndrome. Rev. Infect. Dis. 11: S219–S230.

Mellor I. R. Thomas D. H. Sansom M. S. P. Properties of ion channels formed by Staphylococcus aureus δ-toxin. Biochim. Biophys. Acta. 942 1988 280 294

Miethke T. Duschek K. Wahl C. Heeg K. Wagner H. Pathogenesis of toxic shock syndrome: T cell mediated lethal shock caused by the superantigen TSST-1. Eur. J. Immunol. 23 1993 1294 1500

10.1128/iai.64.1.371-374.1996

Murray D. L. Prasad G. S. Earhart C. A. Leonard B. A. B. Kreiswirth B. N. Novick R. P. Ohlendorf D. H. Schlievert P. M. Immunobiological and biochemical properties of mutants of toxic shock syndrome toxin-1. J. Immunol. 152 1994 87 95

10.1016/0016-5085(94)90604-1

10.1128/iai.64.8.3007-3015.1996

Newbould M. J. Malam J. McIllmurray J. M. Morris J. A. Telford D. R. Barson A. J. Immunohistological localization of staphylococcal toxic syndrome (TSST-1) antigen in sudden infant death syndrome. J. Clin. Pathol. 42 1989 935 939

Noda M. Kato I. Purification and crystallization of staphylococcal leukocidin. Methods Enzymol. 165 1988 22 32

Novick R. Lindsay J. Ruzin A. Ross H. Molecular genetics of the tst element a mobile pathogenicity island in Staphylococcus aureus . European Conference on Toxic Shock Syndrome. International Congress and Symposium Series 229. Arbuthnott J. Furman B. 1998 109 112 Royal Society of Medicine Press Ltd New York N.Y

10.1128/iai.65.9.3606-3614.1997

O'Reilly M. Kreiswirth B. N. Foster T. J. Molecular analysis of a nonexpressed α-toxin gene ( hla ) of clinical isolates of Staphylococcus aureus Molecular biology of the staphylococci. Novick R. P. 1990 439 443 VCH Publishers Inc New York N.Y

Osterholm M. T. Davis J. P. Gibson R. W. Mandel C. Rondeau J. Vergeront J. M. The Investigation Team Tri-state toxic-shock syndrome study. I. Epidemiologic findings. J. Infect. Dis. 145 1982 431 440

Paliard X. West S. G. Lafferty J. A. Clements J. R. Kappler J. W. Marrack P. Kotzin B. L. Evidence of the effects of a superantigen in rheumatoid arthritis. Science 253 1991 325 329

10.1016/S0969-2126(01)00212-X

Paris A. L. Herwaldt L. A. Blum D. Schmid G. P. Shands K. N. Broome C. V. Pathologic findings in twelve fatal cases of toxic shock syndrome. Ann. Intern. Med. 96 1982 852 857

Parsonnet J. Case definition of staphylococcal TSS: A proposed revision incorporating laboratory findings European Conference on Toxic Shock Syndrome. International Congress and Symposium Series 229. Arbuthnott J. Furman B. 1998 15 Royal Society of Medicine Press Ltd New York N.Y

10.1128/iai.55.5.1070-1076.1987

Parsonnet J. Modern P. A. Giacobbe K. D. Effect of tampon composition on production of toxic shock syndrome toxin-1 by Staphylococcus aureus in vitro. J. Infect. Dis., 173 1996 98 103

10.1128/jb.170.9.4365-4372.1988

Plommet M. Preparation and purification of γ-hemolysin of staphylococci. Methods Enzymol. 165 1988 8 16

Poindexter N. J. Schlievert P. M. Toxic shock syndrome toxin-1-induced proliferation of lymphocytes: comparison of the mitogenic response of human, murine, and rabbit lymphocytes. J. Infect. Dis. 151 1985 65 72

Prasad G. S. Earhart C. A. Murray D. L. Novick R. P. Schlievert P. M. Ohlendorf D. H. Structure of toxic shock syndrome toxin-1. Biochemistry 32 1993 13761 13766

Prasad G. S. Radhakrishnan R. Mitchell D. T. Earhart C. A. Dinges M. M. Cook W. J. Schlievert P. M. Ohlendorf D. H. Refined structures of three crystal forms of toxic shock syndrome toxin-1 and of a tetramutant with reduced activity. Protein Sci. 6 1997 1220 1227

Prevost G. Couppie P. Prevost P. Gayet S. Petiau P. Cribier B. Monteil H. Piemont Y. Epidemiological data on Staphylococcus aureus strains producing synergohymenotropic toxins. J. Med. Microbiol. 42 1995 237 245

10.1128/iai.63.10.4121-4129.1995

Projan S. J. Kornblum J. Kreiswirth B. Moghazeh S. L. Eisner W. Novick R. P. Nucleotide sequence: the β-hemolysin gene of Staphylococcus aureus. Nucleic Acids Res. 17 1989 3305

Rago J. V. Schlievert P. M. Scalded skin syndrome. Rev. Med. Microbiol. 9 1998 9 15

Reck B. Scheuber P. H. Londong W. Sailer-Kramer B. Bartsch K. Hammer D. K. Protection against the staphylococcal enterotoxin-induced intestinal disorder in the monkey by anti-idiotypic antibodies. Proc. Natl. Acad. Sci. USA 85 1988 3170 3174

10.1007/BF00330517

Regelmann W. E. Gray E. D. Wannamaker L. W. Characterization of the human cellular immune response to purified group A streptococcal blastogen A. J. Immunol. 128 1982 1631 1636

Reingold A. L. Broome C. V. Gaventa S. Hightower A. W. Toxic Shock Study Group Risk factors for menstrual toxic shock syndrome: results of a multistate case-control study. Rev. Infect. Dis. 11 (Suppl. 1) 1989 S35 S41

Reingold A. L. Hargrett N. T. Dan B. B. Shands K. N. Strickland B. Y. Broome C. V. Nonmenstrual toxic shock syndrome: a review of 130 cases. Ann. Intern. Med. 96 1982 871 874

Sauter C. Wolfensberger C. Interferon in human serum after injection of endotoxin. Lancet ii 1980 852 853

10.1002/j.1460-2075.1995.tb07336.x

Scheuber P. H. Golecki J. R. Kickhofen B. Scheel D. Beck G. Hammer D. K. Cysteinyl leukotrienes as mediators of staphylococcal enterotoxin B in the monkey. Eur. J. Clin. Investig. 17 1987 455 459

Reference deleted.

10.1128/iai.36.1.123-128.1982

Schlievert P. M. Alteration of immune function by staphylococcal pyrogenic exotoxin type C: possible role in toxic-shock syndrome. J. Infect. Dis. 147 1983 391 398

10.1016/S0140-6736(86)91859-3

Schlievert P. M. Comparison of cotton and cotton/rayon tampons for effect on production of toxic shock syndrome toxin. J. Infect. Dis. 172 1995 1112 1114

Schlievert P. M. Role of superantigens in human diseases. Curr. Opin. Infect. Dis. 8 1995 170 174

Schlievert P. M. Incidence studies of toxic shock syndrome European Conference on Toxic Shock Syndrome. International Congress and Symposium Series 229. Arbuthnott J. Furman B. 1998 34 36 Royal Society of Medicine Press Ltd. New York N.Y

10.1128/iai.27.2.542-548.1980

10.1093/infdis/147.2.236

10.1007/BF01540887

10.1093/infdis/143.4.509

Schwab J. H. Brown R. R. Anderle S. K. Schlievert P. M. Superantigen can reactivate bacterial cell wall-induced arthritis. J. Immunol. 150 1993 4151 4159

Schwab J. H. Watson D. W. Cromartie J. Further studies of group A streptococcal factors with lethal and cardiotoxic properties. J. Infect. Dis. 96 1955 14 18

Seeger W. Bauer M. Bhakdi S. Staphylococcal alpha-toxin induced vascular leakage in isolated perfused rabbit lungs. Lab. Investig. 63 1990 341 349

10.1056/NEJM198012183032502

Siqueira J. A. Speeg-Schatz C. Frehas F. I. S. Sahel J. Monteil H. Prevost G. Channel-forming leucotoxins from Staphylococcus aureus cause severe inflammatory reactions in a rabbit eye model. J. Med. Microbiol. 46 1997 486 494

10.1021/bi00738a019

Smith M. L. Price S. A. Staphylococcus γ-haemolysin. J. Pathol. Bacteriol. 47 1938 379 393

Spero L. Morlock B. A. Metzger J. F. On the cross-reactivity of staphylococcal enterotoxins A, B, C1. J. Immunol. 120 1978 86 89

Stolz S. J. Davis J. P. Vergeront J. M. Crass B. A. Chesney P. J. Wand P. J. Bergdoll M. S. Development of serum antibody to toxic shock syndrome toxin among individuals with toxic shock syndrome in Wisconsin. J. Infect. Dis. 151 1985 883 889

10.1093/infdis/155.4.682

Sugiyama H. Hayama T. Abdominal viscera as site of emetic action for staphylococcal enterotoxin in the monkey. J. Infect. Dis. 115 1965 330 336

10.1128/iai.61.2.580-587.1993

10.1152/ajpcell.1985.248.1.C127

Swaminathan S. Furey W. Pletcher J. Sax M. Crystal structure of staphylococcal enterotoxin B, a superantigen. Nature (London) 359 1992 801 806

10.1128/iai.11.4.640-648.1975

Tierno P. M. Hanna B. A. Propensity of tampons and barrier contraceptives to amplify Staphylococcus aureus toxic shock syndrome toxin-1. Infect. Dis. Obstet. Gynecol. 2 1994 140 145

10.1016/S0140-6736(78)92274-2

Todd J. K. Todd B. H. Franco-Buff A. Smith C. M. Lawellin D. W. Influence of focal growth conditions of the pathogenesis of toxic shock syndrome. J. Infect. Dis. 155 1987 673 681

10.1111/j.1365-2249.1992.tb02995.x

Valeva A. Palmer M. Bhakdi S. Staphylococcal exotoxin: formation of the heptameric pore is cooperative and proceeds through multiple intermediate stages. Biochemistry 36 1997 13298 13304

Vandana S. Raje M. Krishnasastry M. V. The role of the amino terminus in the kinetics and assembly of α hemolysin of Staphylococcus aureus. J. Biol. Chem. 272 1997 24858 24863

10.1093/infdis/148.4.692

10.1128/iai.61.12.4972-4979.1993

Wagner G. Bohr L. Wagner P. Perterson L. N. Tampon-induced changes in vaginal oxygen and carbon dioxide tension. Am. J. Obstet. Gynecol. 148 1984 147 150

Woodin A. M. Fractionation of the two components of leukocidin from Staphylococcus aureus. Biochem. J. 73 1959 225 237

Woodin A. M. Purification of the two components of leukocidin from Staphylococcus aureus. Biochem. J. 75 1960 158 165

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 subtilis. Eur. J. Biochem. 175 1988 213 220

10.1111/j.1574-6968.1998.tb13278.x