Chapter 21 : Virulence Plasmids of Nonsporulating Gram-Positive Pathogens

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Virulence Plasmids of Nonsporulating Gram-Positive Pathogens, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817732/9781555812652_Chap21-1.gif /docserver/preview/fulltext/10.1128/9781555817732/9781555812652_Chap21-2.gif


Gram-positive bacteria are leading causes of many types of human infection, including pneumonia; skin and nasopharyngeal infections; and, among hospitalized patients, bloodstream, urinary tract, and surgical wound infections. As variable traits of the species, many of these virulence properties are encoded by mobile genetic elements, such as virulence plasmids and pathogenicity islands. This chapter reviews virulence plasmids in nonsporulating gram-positive bacteria and examines their contribution to the pathogenesis of disease. More recent studies have determined the nature of the bacteriocin activity linked with exfoliative toxin B (ETB) virulence plasmids. Some strains produce a cytolysin with both bactericidal and toxin activity against eukaryotic cells. The cytolysin operon occurs along with aggregation substance on pheromone-responsive plasmids and within the recently described 150-kb pathogenicity island on which enterococcal surface protein (Esp) and aggregation substance are found. Aggregation substance expression has also been shown to correlate with an enhanced uptake of enterococci by intestinal epithelial cells. However, this increase in uptake did not result in an increase in translocation across intestinal epithelium in vitro. Virulence plasmids may then represent "selfish DNA" of limited benefit to the bacterium that takes advantage of an otherwise stable, intimate association to ensure its perpetuation, with selection limiting its presence to a small proportion of the population so as not to jeopardize the commensal existence of the vast majority.

Citation: Pillar C, Gilmore M. 2004. Virulence Plasmids of Nonsporulating Gram-Positive Pathogens, p 439-454. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch21

Key Concept Ranking

Mobile Genetic Elements
Toxic Shock Syndrome
Urinary Tract Infections
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Restriction map of pIB485 encoding SED and SEJ. Genes encoding cadmium resistance (cad) and resistance to beta-lactams (bla) are also indicated. Plasmid diagram contributed by J. J. landolo, Oklahoma University Health Sciences Center (OUHSC), Oklahoma City, Okla.

Citation: Pillar C, Gilmore M. 2004. Virulence Plasmids of Nonsporulating Gram-Positive Pathogens, p 439-454. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch21
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Plasmid map of a representative ETB-expressing plasmid, pETB. ORFs encoding ETB, cadmium resistance (cad), an operon responsible for production of staphylococcin c55 (bacteriocin operon), and the virulence factor EDIN-C are depicted (accession no. NC_003265) (174).

Citation: Pillar C, Gilmore M. 2004. Virulence Plasmids of Nonsporulating Gram-Positive Pathogens, p 439-454. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch21
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

(A) Plasmid map of pADl depicting UV-resistance genes (uvr), the cytolysin operon, and genes involved in plasmid maintenance/transmission ( ). (B) Depiction of genes involved in plasmid transfer and pheromone-sensing (adapted from reference ). (C) Regulation of pheromone-response-mediated plasmid transfer; transcripts are depicted by arrows (adapted from reference ).

Citation: Pillar C, Gilmore M. 2004. Virulence Plasmids of Nonsporulating Gram-Positive Pathogens, p 439-454. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch21
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

(A) Detailed schematic of cytolysin operon (contributed by W. Haas, OUHSC, Oklahoma City, Okla.). (B) Schematic of cytolysin expression and posttranslational modification. ( ) CyIL and CylL, are synthesized, ( ) arc intracellulary modified by CylM to create CylL * and CylL,* ( ) arc secreted and further modified by CylB, resulting in CyIL′ and CylL ′ and ( ) are cleaved extracellularly by CylA to form the active cytolysin components CylL″ and CylL″. CylL″ and CylL″ are capable of forming aggregates ( ) but are prevented from lysing cytolysin expressing cells via Cyl ( ) (contributed by W. Haas, OUHSC, Oklahoma City, Okla.).

Citation: Pillar C, Gilmore M. 2004. Virulence Plasmids of Nonsporulating Gram-Positive Pathogens, p 439-454. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch21
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Plasmid map of virulence plasmid p33701 of R. equi. ORFs believed to be involved in plasmid maintenance and conjugation are depicted in gray, ORFs encoding Vaps are depicted in black, and putative ORFs within the proposed pathogenicity island are depicted in white ( ).

Citation: Pillar C, Gilmore M. 2004. Virulence Plasmids of Nonsporulating Gram-Positive Pathogens, p 439-454. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch21
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Adesiyun, A. A.,, W. Lenz,, and K. P. Schaal. 1991. Exfoliative toxin production by Staphylococcus aureus strains isolated from animals and human beings in Nigeria. Microbiologica 14: 357 362.
2. Aktories, K. 1997. Rho proteins: targets for bacterial toxins. Trends Microbiol. 5: 282 288.
3. Altboum, Z.,, I. Hertman,, and S. Sarid. 1985. Penicillinase plasmid-linked genetic determinants for enterotoxins B and CI production in Staphylococcus aureus. Infect. Immun. 47: 514 521.
4. Amagai, M.,, N. Matsuyoshi,, Z. H. Wang,, C. Andl,, and J. R. Stanley. 2000. Toxin in bullous impetigo and staphylococcal scalded-skin syndrome targets desmoglein 1. Nat. Med. 6: 1275 1277.
5. An, F. Y.,, and D. B. Clewell. 1994. Characterization of the determinant (traB) encoding sex pheromone shutdown by the hemolysin/bacteriocin plasmid pAD1 in Enterococcus faecalis. Plasmid 31: 215 221.
6. Arbuthnott, J. P.,, J. Kent,, A. Lyell, and C G. Gemmell. 1971. Toxic epidermal necrolysis produced by an extracellular product of Staphylococcus aureus. Br. J. Dermatol. 85: 145 149.
7. Balaban, N.,, and A. Rasooly. 2000. Staphylococcal enterotoxins. Int. J. Food Microbiol. 61: 1 10.
8. Banerjee, S.,, and J. N. Hansen. 1988. Structure and expression of a gene encoding the precursor of subtilin, a small protein antibiotic. J. Biol. Chem. 263: 9508 9514.
9. Bayles, K. W.,, and J. J. landolo. 1989. Genetic and molecular analyses of the gene encoding staphylococcal enterotoxin D. J. Bacteriol. 171: 4799 4806.
10. Bensing, B. A.,, and G. M. Dunny. 1993. Cloning and molecular analysis of genes affecting expression of binding substance, the recipient-encoded receptor(s) mediating mating aggregate formation in Enterococcus faecalis. J. Bacteriol. 175: 7421 7429.
11. Bergdoll, M. S.,, J . K. Czop,, and S. S. Gould. 1974. Enterotoxin synthesis by the staphylococci. Ann. N. Y. Acad. Sci. 236: 307 316.
12. Berti, M.,, G. Candiani,, A. Kaufhold,, A. Muscholl,, and R. Wirth. 1998. Docs aggregation substance of Enterococcus faecalis contribute to development of endocarditis? Infection 26: 48 53.
13. Bohach, G. A.,, and P. M. Sclilievert. 1987. Expression of staphylococcal enterotoxin C1 in Escherichia coli. Infect. Immun. 55: 428 432.
14. Booth, M. CM C. P. Bogie, H. G. Sahl, R. J. Siezen, K. L. Hatter, and M. S. Gilmore. 1996. Structural analysis and proteolytic activation of Enterococcus faecalis cytolysin, a novel lantibiotic. Mol. Microbiol. 21: 1175 1184.
15. Booth, M. C., L. M. Pence,, P. Mahasreshti,, M. C. Callegan,, and M. S. Gilmore. 2001. Clonal associations among Staphylococcus aureus isolates from various sites of infection. Infect. Immun. 69: 345 352.
16. Brock, T.,, B. Peachcr,, and D. Pierson. 1963. Survey of the bacteriocines of enterococci. J. Bacteriol. 86: 702 707.
17. Byrne, B. A.,, J. F. Prescott,, G. H. Palmer,, S. Takai,, V. M. Nicholson,, D. C. Alperin,, and S. A. Hines. 2001. Virulence plasmid of Rhodococcus equi contains inducible gene family encoding secreted proteins. Infect. Immun. 69: 650 656.
18. Casman, E. P. 1965. Staphylococcal enterotoxin. Ann. N. V. Acad. Sci. 128: 124 131.
19. Chintagumpala, M. M.,, J. A. Mollick,, and R. R. Rich. 1991. Staphylococcal toxins bind to different sites on HLA-DR. J. Immunol. 147: 3876 3881.
20. Choi, Y. W.,, A. Herman,, D. DiGiusto,, T. Wade,, P. Marrack,, and J. Kapplcr. 1990. Residues of the variable region of the T-cell-receptor beta-chain that interact with S. aureus toxin superantigens. Nature 346: 471 473.
21. Chow, J. W.,, L. A. Thai,, M. B. Perri,, J. A. Vazquez,, S. M. Donabedian,, D. B. Clewell, and M, J. Zervos. 1993. Plasmid-associated hemolysin and aggregation substance production contribute to virulence in experimental enterococcal endocarditis. Antimicrob. Agents Cbemother. 37: 2474 247.
22. Clewell, D., 1999. Sex pheromone systems in enterococci, p. 47 65. In G. Dunny, and S. Winans (ed.), Cell-Cell Signaling in Bacteria. American Society for Microbiology, Washington, D.C..
23. Clewell, D.,, Y. Yagi,, Y. Ike,, R. Craig,, B. Brown,, and F. An,. 1982. S ex pheromones in Streptococcus faecalis: multiple pheromone systems in strain DS5, similarities of pAD1 and pAMdl,and mutants of pAD1 altered in conjugative properties, p. 97 100. In D. Schlessinger (ed.), Microbiology—1982. American Society for Microbiology, Washington, D.C..
24. Clewell, D. B. 1993. Bacterial sex pheromone-induced plasmid transfer. Cell 73: 9 12.
25. Clewell, D. B. 1981. Plasmids, drug resistance, and gene transfer in the genus Streptococcus. Microbiol. Rev. 45: 409 436.
26. Clewell, D. B.,, P. K. Tomich,, M. C Gawron-Burke,, A. E. Franke,, Y. Yagi,, and F. Y. An. 1982. Mapping of Streptococcus faecalis plasmids pADl and pAD2 and studies relating to transposition of Tn 917 J . Bacteriol. 152: 1220 1230.
27. Coburn, P. S.,, L. E. Hancock,, M. C. Booth,, and M. S. Gilmore. 1999. A novel means of self-protection, unrelated to toxin activation, confers immunity to the bactericidal effects of the Enterococcus faecalis cytolysin. Infect. Immun. 67: 3339 3347.
28. Colmar, I.,, and T. Horaud. 1987. Enterococcus faecalis hemolysin-bacteriocin plasmids belong to the same incompatibility group. Appl. Environ. Microbiol. 53: 567 570.
29. Crupper, S. S.,, A. J. Gies,, and J. J. landolo. 1997. Purification and characterization of staphylococcin BacR1, a broad-spectrum bacteriocin. Appl. Environ. Microbiol. 63: 4185 4190.
30. Dajani, A. S. 1972. The scalded-skin syndrome: relation to phage-group II staphylococci. J. Infect. Dis. 125: 548 551.
31. Dancer, S. J.,, R. Garratt,, J. Saldanha,, H. Jhoti,, and R. Evans. 1990. The epidermolytic toxins are serine proteases. EEBS Lett. 268: 129 132.
32. Dancer, S. J.,, and W. C Noble. 1991. Nasal, axillary, and perineal carriage of Staphylococcus aureus among women: identification of strains producing epidermolytic toxin, J. Clin. Pathol. 44: 681 684.
33. Davies, J.. 1994. Inactivation of antibiotics and the dissemination of resistance genes. Science 264: 375 382.
34. de Azavedo, J.,, and J. P. Arbuthnott. 1981. Prevalence of epidermolytic toxin in clinical isolates of Staphylococcus aureus .J. Med. Microbiol. 14: 341 344.
35. Doolittle, W. F.,, and C. Sapienza. 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601 603.
36. Dorman, C. J.,, and M. E. Porter. 1998. The Shigella virulence gene regulatory cascade: a paradigm of bacterial gene control mechanisms. Mol. Microbiol. 29: 677 684.
37. Dunny, G. M.,, and D. B. Clewell. 1975. Transmissible toxin (hemolysin) plasmid in Streptococcus faecalis and its mobilization of a noninfectious drug resistance plasmid. J. Bacteriol. 124: 784 790.
38. Dunny, G.,, M. R. A. Craig,, R. L. Carron,, and D. B. Clewell. 1979. Plasmid transfer in Streptococcus faecalis: production of multiple sex pheromones by recipients. Plasmid 2: 454 465.
39. Dunny, G. M.,, B. A. Leonard,, and P. J. Hedberg. 1995. Pheromone-inducible conjugation in Enterococcus faecalis: interbacterial and host-parasite chemical communication. J. Bacteriol. 177: 871 876.
40. Dupont, H.,, P. Montravers,, J. Mohler,, and C. Carbon. 1998. Disparate findings on the role of virulence factors of Enterococcus faecalis in mouse and rat models of peritonitis. Infect. Immun. 66: 2570 2575.
41. Ehrenfeld, E. E.,, R. E. Kesslcr,, and D. B. Clewell. 1986. Identification of pheromone-induced surface proteins in Streptococcus faecalis and evidence of a role for lipoteichoic acid in formation of mating aggregates. J. Bacteriol. 168: 6 12.
42. Elias, P. M.,, P. Fritsch,, G. Tappeiner,, H. Mittermayer,, and K. Wolff. 1974. Experimental staphylococcal toxic epidermal necrolysis (TEN) in adult humans and mice. J. Lab. Clin. Med. 84: 414 424.
43. Flahaut, S.,, J. Frere,, P. Boutibonnes,, and Y. Auffray. 1996. Comparison of the bile salts and sodium dodecyl sulfate stress responses in Enterococcus faecalis. Appl. Environ. Microbiol. 62: 2416 2420.
44. Flahaut, S.,, A. Hartke,, J. C. Giard,, and Y. Auffray. 1997. Alkaline stress response in Enterococcus faecalis: adaptation, cross-protection, and changes in protein synthesis. Appl. Environ. Microbiol. 63: 812 814.
45. Flahaut, S.,, A. Hartke,, J. C. Giard,, A. Benachour,, P. Boutibonnes,, and Y. Auffray. 1996. Relationship between stress response toward bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiol. Lett. 138: 49 54.
46. Francia, M. V.,, W. Haas,, R. Wirth,, E. Samberger,, A. Muscholl-Silberhorn,, M. S. Gilmore,, Y. Ike,, K. E. Weaver,, F. Y. An,, and D. B. Clewell. 2001. Completion of the nucleotide sequence of the Enterococcus faecalis conjugative virulence plasmid pAD1 and identification of a second transfer origin. Plasmid 46: 117 127.
47. Galli, D.,, F. Lottspeich,, and R. Wirth. 1990. Sequence analysis of Enterococcus faecalis aggregation substance encoded by the sex pheromone plasmid pAD1 Mol. Microbiol. 4: 895 904.
48. Galli, D.,, R. Wirth,, and G. Wanner. 1989. Identification of aggregation substances of Enterococcus faecalis cells after induction by sex pheromones. An immunological and ultra-structural investigation. Arch. Microbiol. 151: 486 490.
49. Garsin, D. A.,, C. D. Sifri,, E. Mylonakis,, X. Qin,, K. V. Singh,, B. E. Murray,, S. B. Calderwood,, and F. M. Ausubel. 2001. A simple model host for identifying gram-positive virulence factors. Proc. Natl. Acad. Sci. USA 98: 10892 10897.
50. Giguere, S.,, M. K. Hondalus,, J. A. Yager,, P. Darrah,, D. M. Mosser,, and J. F. Prescott. 1999. Role of the 85-kilobase plasmid and plasmid-encoded virulence-associated protein A in intracellular survival and virulence of Rhodococcus equi. Infect. Immun. 67: 3548 3557.
51. Gilmore, M. S.,, P. S. Coburn,, S. R. Nallapareddy,, and B. E. Murray,. 2002. Enterococcal virulence, p. 301 354. In M. S. Gilmore (ed.), The Enterococci. Pathogenesis, Molecular Biology, and Antimicrobial Resistance. American Society for Microbiology, Washington, D.C..
52. Gilmore, M. S.,, R. A. Segarra,, and M. C. Booth. 1990. An HlyB-type function is required for expression of the Enterococcus faecalis hemolysin/bacteriocin. Infect. Immun. 58: 3914 3923.
53. Gilmore, M. S.,, R. A. Segarra,, M. C, Booth, C. P. Bogie, L. R. Hall, and D. B. Clewell. 1994. Genetic structure of the Enterococcus faecalis plasmid pAD1-encoded cytolytic toxin system and its relationship to lantibiotic determinants. J. Bacteriol. 176: 7335 7344.
54. Gomez-Lus, R. 1998. Evolution of bacterial resistance to antibiotics during the last three decades. Int. Microbiol 1: 279 284.
55. Gutschik, E.,, S. Moller,, and N. Christensen. 1979. Experimental endocarditis in rabbits. 3. Significance of the proteolytic capacity of the infecting strains of Streptococcus faecalis. Acta Pathol. Microbiol. Scand. Sect. B 87: 353 362.
56. Haas, W.,, and M. S. Gilmore. 1999. Molecular nature of a novel bacterial toxin; the cytolysin of Enterococcus faecalis. Med. Microbiol. Immunol. (Berlin) 187: 183 190.
57. Haas, W.,, B. D. Shepard,, and M. S. Gilmore. 2002. Two-component regulator of Enterococcus faecalis cytolysin responds to quorum-sensing autoinduction. Nature 415: 84 87.
58. Hancock, L. E.,, and M. S. Gilmore. 2002. The capsular polysaccharide of Enterococcus faecalis and its relationship to other polysaccharides in the cell wall. Proc. Natl. Acad. Sci. USA 99: 1574 1579.
59. Hancock, L., E. and M. S. Gilmore. 1999. Enterococcal pathogenicity, p. 251 258 . In V. Fischetti,, R. Novick,, J. Ferretti,, D. Portnoy,, and J. Rood (ed.), Gram-Positive Pathogens. American Society for Microbiology, Washington, D.C..
60. Hirt, H.,, P. M. Schlievert,, and G. M. Dunny. 2002. In vivo induction of virulence and antibiotic resistance transfer in Enterococcus faecalis mediated by the sex pheromone-sensing system of pCF10. Infect. Immun. 70: 716 723.
61. Hirt, H.,, R. Wirth,, and A. Muscholl. 1996. Comparative analysis of 18 sex pheromone plasmids from Enterococcus faecalis: detection of a new insertion element on pPD1 and implications for the evolution of this plasmid family. Mol Gen. Genet. 252: 640 647.
62. Holmberg, S. D.,, and P. A. Blake. 1984. Staphylococcal food poisoning in the United States. New facts and old misconceptions. JAMA 251: 487 489.
63. Huycke, M. M.,, V. Abrams,, and D. R. Moore. 2002. Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis 23: 529 536.
64. Huycke, M. M.,, and M. S. Gilmore. 1995. Frequency of aggregation substance and cytolysin genes among enterococcal endocarditis isolates. Plasmid 34: 152 156.
65. Huycke, M. M.,, M. S. Gilmore,, B. D. Jett,, and J. L. Booth. 1992. Transfer of pheromone-inducible plasmids between Enterococcus faecalis in the Syrian hamster gastrointestinal tract J. Infect. Dis. 166: 1188 1191.
66. Huycke, M. M.,, W. A. Joyce,, and M. S. Gilmore. 1995. Enterococcus faecalis cytolysin without effect on the intestinal growth of susceptible enterococci in mice.;. Infect. Dis. 172: 273 276.
67. Huycke, M. M. D. Moore, W. Joyce, P. Wise, L. Shepard, Y. Kotake, and M. S. Gilmore. 2001. Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol. Microbiol. 42: 729 740.
68. Huycke, M. M.,, D. F. Sahm,, and M. S. Gilmore. 1998. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg. Infect. Dis. 4: 239 249.
69. Huycke, M. M.,, C. A. Spiegel,, and M. S. Gilmore. 1991. Bacteremia caused by hemolytic, high-level gentamicin-resistant Enterococcus faecalis. Antimicrob. Agents Chemother. 35: 1626 1634.
70. Ike, Y.,, and D. B. Clewell. 1984. Genetic analysis of the pAD1 pheromone response in Streptococcus faecalis, using transposon Tn 917 as an insertional mutagen. J. Bacteriol 158: 777 783.
71. Ike, Y.,, D. B. Clewell,, R. A. Segarra,, and M. S. Gilmore. 1990. Genetic analysis of the pAD1 hemolysin/bacteriocin determinant in Enterococcus faecalis: Tn 917 insertional mutagenesis and cloning. J. Bacteriol. 172: 155 163.
72. Ike, Y.,, H. Hashimoto,, and D. B. Clewell. 1984. Hemolysin of Streptococcus faecalis subspecies zymogenes contributes to virulence in mice. Infect. Immun. 45: 528 530.
73. Ike, Y.,, H. Hashimoto,, and D. B. Clewell. 1987. High incidence of hemolysin production by Enterococcus (Streptococcus) faecalis strains associated with human parenteral infections. J. Clin. Microbiol 25: 1524 1528.
74. Inoue, S.,, M. Sugai,, Y. Murooka, S, Y. Paik, Y. M. Hong, H. Ohgai, and H. Suginaka. 1991. Molecular cloning and sequencing of the epidermal cell differentiation inhibitor gene from Staphylococcus aureus. Biochem. Biopbys. Res. Commun. 174: 459 464.
75. Jackson, M. P.,, and J. J. landolo. 1986. Cloning and expres sion of the exfoliative toxin B gene from Staphylococcus aureus. J. Bacteriol. 166: 5745 80.
76. Jackson, M. P.,, and J. J. landolo. 1986. Sequence of the exfoliative toxin B gene of Staphylococcus aureus. J. Bacteriol 167: 726 728.
77. Jacob, A. E.,, G. J. Douglas,, and S. J. Hobbs. 1975. Self-transferable plasmids determining the hemolysin and bacteriocin of Streptococcus faecalis var. zymogenes. J. Bacteriol 121: 863 872.
78. Jett, B. D. R. V. Atkuri, and M. S. Gilmore. 1998. Enterococcus faecalis localization in experimental endophthalmitis: role of plasmid-encoded aggregation substance. Infect Immun. 66: 843 848.
79. Jett, B. D.,, and M. S. Gilmore. 1990. The growth-inhibitory effect of the Enterococcus faecalis bacteriocin encoded by pAD1 extends to the oral streptococci. J. Dent. Res. 69: 1640 1645.
80. Jett, B. D.,, M. M. Huycke,, and M. S. Gilmore. 1994. Virulence of enterococci. Clin. Microbiol. Rev. 7: 462 478.
81. Jett, B. D.,, H. G. Jensen,, R. E. Nordquist,, and M. S. Gilmore. 1992. Contribution of the pAD1-encoded cytolysin to the severity of experimental F,nterococcus faecalis endophthalmitis. Infect. Immun. 60: 2445 2452.
82. Kaletta, C.,, and K. D. Entian. 1989. Nisin, a peptide antibiotic: cloning and sequencing of the nisA gene and posttranslational processing of its peptide product. J. Bacteriol 171: 1597 1601.
83. Kapral, F. A. 1974. Staphylococcus aureus: some host-parasite interactions, Ann. N. Y. Acad. Sci. 236: 267 276.
84. Kondo, I.,, S. Sakurai,, and Y. Sarai. 1973. Purification of exfoliatin produced by Staphylococcus aureus of bacterio-phage group 2 and its physicochemical properties. Infect. Immun. 8: 156 164.
85. Kondo, L.,, S. Sakurai,, Y. Sarai,, and S. Futaki. 1975. Two serotypes of exfoliatin and their distribution in staphylococcal strains isolated from patients with scalded skin syndrome. J. Clin. Microbiol. 1: 3974 400.
86. Kornblum, J.,, B. N. Krciswirth,, S. J. Projan,, H. Ross,, and R. P. Novick,, 1991. Agn A polycistronic locus regulating exoprotein synthesis in Staphylococcus aureus, p. 3734 02. In R. P. Novick (ed.), Molecular Biology of the Staphylococci. VCH Publishers, New York, N.Y..
87. Kreft, B.,, R. Marre,, U. Schramm,, and R. Wirth. 1992. Aggregation substance of Enterococcus faecalis mediates adhesion to cultured renal tubular cells. Infect. Immun. 60: 25 30.
88. Ladhani, S.,, C. L. Joannou,, D. P. Lochrie,, R. W. Evans,, and S. M. Poston, 1999. Clinical, microbial, and biochemical aspects of the exfoliative toxins causing staphylococcal scalded-skin syndrome. Clin. Microbiol. Rev. 12: 224 242.
89. Le Bouguenec, C.,, G. de Cespedes,, and T. Horaud. 1988. Molecular analysis of a composite chromosomal conjugative element (TnMOl) of Streptococcus pyogenes. J. Bacteriol 170: 3930 3936.
90. Lee, C. Y.,, J. J. Schmidt,, A. D. Johnson-Winegar,, L. Spero,, and J. J. landolo. 1987. Sequence determination and comparison of the exfoliative toxin A and toxin B genes from Staphylococcus aureus. J. Bacteriol. 169: 3904 3909.
91. Lindler, L. E.,, G. V. Piano,, V. Burland,, G. F. Mayhew,, and F. R. Blattner. 1998. Complete DNA sequence and detailed analysis of the Yersinia pestis KIM5 plasmid encoding murine toxin and capsular antigen. Infect. Immun. 66: 5731 5742.
92. Lowney, E. D.,, J. V. Baublis,, G. M. Kreye,, E. R. Harrell,, and A. R. McKenzie. 1967. The scalded skin syndrome in small children. Arch. Dermatol. 95: 359 369.
93. Mackawa, S.,, M. Yoshioka,,and Y. Kumamoto. 1992. Proposal of a new scheme for the serological typing of Enterococcus facialis strains. Microbiol. Immunol. 36: 671 681.
94. McLay, A. L.,, J. P. Arbuthnott,, and A. LyelL. 1975. Action of staphylococcal epidermolytic toxin on mouse skin: an electron microscopic study. J . Invest. Dermatol. 65: 423 428.
95. Melish, M. E.,, and L. A, Glasgow. 1971. Staphylococcal scalded skin syndrome: the expanded clinical syndrome. J. Pediatr. 78: 958 967.
96. Melish, M. E., and L. A. Glasgow. 1970. The staphylococcal scalded-skin syndrome. N. Engl. J. Med. 282: 1114 1119.
97. Melish, M. E.,, L. A. Glasgow,, and M. D. Turner. 1972. The staphylococcal scalded-skin syndrome: isolation and partial characterization of the exfoliative toxin. J. Infect. Dis. 125: 129 140.
98. Melish, M. E.,, L. A. Glasgow,, M. D. Turner,, and C. B. Lillibridge. 1974. The staphylococcal epidermolytic toxin: its isolation, characterization, and site of action. Ann. N. Y. Acad. Sci. 236: 317 342.
99. Miller, M. M.,, and F. A. Kapral. 1972. Neutralization of Staphylococcus aureus exfoliatin by antibody. Infect. Immun. 6: 561 563.
100. Moellering, R.,. 1995. Enterococcus species, Streptococcus bovis, and Leuconostac species, p. 1826 1835. In G. Mandell,, J. Bennett,, and R. Dolin (ed.), Principles and Practices of Infectious Diseases, 4th ed. Churchill Livingston, New York, N.Y..
101. Mollick, J. A.,, M. Chintagumpala,, R. G. Cook,, and R. R. Rich. 1991. Staphylococcal exotoxin activation of T cells. Role of exotoxin-MHC class II binding affinity and class II isotype. J. Immunol. 146: 463 468.
102. Monday, S. R.,, and G. A. Bohach,. 1999. Properties of Staphylococcus aureus enterotoxins and toxic shock syndrome toxin-1, p. 589 610. In J. Alouf, and J. Freer (ed.), The Comprehensive Sourcebook of Bacterial Protein Toxins. Academic Press, London, United Kingdom.
103. Mori, M.,, Y. Sakagami,, M. Narita,, A. Isogai,, M. Fujino,, C. Kitada,, R. A. Craig,, D. B. Clewell,, and A. Suzuki. 1984. Isolation and structure of the bacterial sex pheromone, cAD1, that induces plasmid transfer in Streptococcus faecalis. FEBS Lett. 178: 97 100.
104. Mori, M.,, H. Tanaka,, Y. Sakagami,, A. Isogai,, M. Fujino,, C. Kitada,, B. A. White,, F. Y. An,, D. B. Clewell,, and A. Suzuki. 1986. Isolation and structure of the Streptococcus faecalis sex pheromone, cAM373. FEBS Lett. 206: 69 72.
105. Mundy, L. M.,, D. F. Sahm,, and M. Gilmore. 2000. Relationships between enterococcal virulence and antimicrobial resistance. Clin. Microbiol. Rev. 13: 513 522.
106. Murono, K.,, K. Fujita,, and H. Yoshioka. 1988. Microbiologic characteristics of exfoliative toxin-producing Staphylococcus aureus. Pediatr. Infect. Dis. J. 7: 313 315.
107. Murray, B. E. 1990. The life and times of the Enterococcus. Clin. Microbiol. Rev. 3: 46 65.
108. Muscholl-Silberhorn, A. B. 2000. Pheromone-regulated expression of sex pheromone plasmid pAD1-encoded aggregation substance depends on at least six upstream genes and a Ws-acting, orientation-dependent factor. J. Bacteriol. 182: 3816 3825.
109. Nallapareddy, S. R.,, X. Qin,, G. M. Weinstock,, M. Hook,, and B. E. Murray. 2000. Enterococcus faecalis adhesin, ace, mediates attachment to extracellular matrix proteins collagen type IV and hi min in as well as collagen type I. Infect. Immun. 68: 5218 5224.
110. Nallapareddy, S. R.,, K. V. Singh,, R. W. Duh,, G. M. Weinstock,, and B. E, Murray. 2000. Diversity of ace, a gene encoding a microbial surface component recognizing adhesive matrix molecules, from different strains of Enterococcus faecalis and evidence for production of ace during human infections. Infect Immun. 68: 5210 5217.
111. Navaratna, M. A.,, H. G. Sahl,, and J. R. Tagg. 1999. Identification of genes encoding two-component lantibiotic production in Staphylococcus aureus CSS and other phage group II S. aureus strains and demonstration of an association with the exfoliative toxin B gene. Infect. Immun. 67: 4268 4271.
112. Neu, H. C. 1992. The crisis in antibiotic resistance. Science 257: 1064 1073.
113. Novick, R. P., 2000. Pathogenicity factors and their regulation, p. 392 407. In V. Fischetti,, R. Novick,, J. Ferretti,, D. Portnoy,, and J. Rood (ed.), Gram-Positive Pathogens. American Society for Microbiology, Washington, D.C..
114. Oliver, D. R., B. L. Brown,, and D. B. Clewell. 1977. Characterization of plasmids determining hemolysin and bacteriocin production in Streptococcus faecalis 5952. J. Bacteriol. 130: 948 950.
115. Olmsted, S. B., G. M. Dunny,, S. L. Erlandsen,, and C. L. Wells. 1994. A plasmid-encoded surface protein on Enterococcus faecalis augments its internalization by cultured intestinal epithelial cells. J. Infect Dis. 170: 1549 1556.
116. Perry, R. D.,, S. C. Straley,, J. D. Fetherston,, D. J. Rose,, J. Gregor,, and F. R. Blattner. 1998. DNA sequencing and analysis of the low-Ca2+-response plasmid pCD1 of Yersinia pestis KIM5. Infect Immun. 66: 4611 4623.
117. Piemont, Y., 1999. Staphylococcal epidermolytic toxins: structure, biological and pathophysiological properties, p. 657 668. In J. Alouf, and J. Freer (ed.), The Comprehensive Sourcebook of Bacterial Protein Toxins. Academic Press, London, United Kingdom.
118. Piemont, Y.,, D. Rasoamananjara,, J. M. Fouace,, and T. Bruce. 1984. Epidemiological investigation of exfoliative toxin-producing Staphylococcus aureus strains in hospitalized patients. J. Clin. Microbiol. 19: 417 420.
119. Projan, S. J.,, and R. P. Novick,. 1997. The molecular basis of virulence, p. 55 81. In G. Archer, and K. Crossley (ed.), Staphylococci in Human Disease. Churchill Livingstone, New York, N.Y..
120. Qin, X.,, K. V. Singh,, G. M. Weinstock, and B, E. Murray. 2000. Effects of Enterococctts faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect. Immun. 68: 2579 2586.
121. Rakita, R. M.,, N. N. Vanek,, K. Jacques-Palaz,, M. Mee,, M. M. Mariscalco,, G. M. Dunny,, M. Snuggs,, W. B. Van Winkle,, and S. I. Simon. 1999. Enterococcus faecalis bearing aggregation substance is resistant to killing by human neutrophils despite phagocytosis and neutrophil activation. Infect Immun. 67: 6067 6075.
122. Richards, M. J.,, J. R. Edwards,, D. H. Culver,, and R. P. Gaynes. 2000. Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect. Control Hosp. Epidemiol. 21: 510 515.
123. Richards, M. J.,, J. R. Edwards,, D. H. Culver,, and R. P. Gaynes. 1999. Nosocomial infections in medical intensive care units in the United States. National Nosocomial Infections Surveillance System. Crit. Care Med. 27: 887 892.
124. Rogolsky, M.,, R. Warren,, B. B. Wiley,, H. T. Nakamura,, and L. A. Glasgow. 1974. Nature of the genetic determinant controlling exfoliative toxin production in Staphylococcus aureus. J. Bacteriol. 117: 157 165.
125. Rogolsky, M.,, and B. B. Wiley. 1977. Production and properties of a staphylococci genetically controlled by the staphylococcal plasmid for exfoliative toxin synthesis. Infect. Immun. 15: 726 732.
126. Rowe-Magnus, D. A.,, and D. Mazel. 2001. Integrons: natural tools for bacterial genome evolution. Curr. Opin. Microbiol. 4: 565 569.
127. Sannomiya, P.,, R. A. Craig,, D. B. Clewell,, A. Suzuki,, M. Fujino,, G. O. Till,, and W. A. Marasco. 1990. Characterization of a class of nonformylated Enterococcus faecalisderived neutrophil chemotactic peptides: the sex pheromones. Proc. Natl. Acad. Sci. USA 87: 66 70.
128. Sato, H.,, Y. Matsumori, T, Tanabe, H. Saito, A. Shimizu, and J. Kawano. 1994. A new type of staphylococcal exfoliative toxin from a Staphylococcus aureus strain isolated from a horse with phlegmon. Infect Immun. 62: 3780 3785.
129. Sato, H.,, T. Tanabe,, M. Kuramoto,, K. Tanaka,, T. Hashimoto,, and H. Saito. 1991. Isolation of exfoliative toxin from Staphylococcus hyicus subsp. hyicus and its exfoliative activity in the piglet. Vet. Microbiol. 27: 263 275.
130. Sato, H.,, T. Watanabe,, Y. Murata,, A. Ohtake,, M. Nakamura,, C. Aizawa,, H. Saito,, and N. Machara. 1999. New exfoliative toxin produced by a plasmid-carrying strain of Staphylococcus hyicus. Infect. Immun. 67: 4014 4018.
131. Schlievert, P. M.,, P. J. Gahr,, A. P. Assimacopoulos,, M. M. Dinges,, J. A. Stoehr,, J. W. Harmala,, H. Hirt,, and G. M. Dunny. 1998. Aggregation and binding substances enhance pathogenicity in rabbit models of Enterococcus faecalis endocarditis. Infect. Immun. 66: 218 223.
132. Schnell, N.,, K. D. Entian,, U. Schneider,, F. Gotz,, H. Zahner,, R. Kellner,, and G. Jung. 1988. Prepeptide sequence of epidermin, a ribosomally synthesized antibiotic with four sulphide-rings. Nature 333: 276 278.
133. Segarra, R. A.,, M. C. Booth,, D. A. Morales,, M. M. Huyeke,, and M. S. Gilmore. 1991. Molecular characterization of the Enterococcus faecalis cytolysin activator. Infect. Immun. 59: 1239 1246.
134. Shafer, W. M.,, and J. J. landolo. 1978. Chromosomal locus for staphylococcal enterotoxin B. Infect. Immun. 20: 273 278.
135. Shankar, N.,, A. S. Baghdayan,, and M. S. Gilmore. 2002. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417: 746 750.
136. Shankar, N. C.,, V. Lockatell,, A. S. Baghdayan,, C. Drachenberg,, M. S. Gilmore,, and D. E. Johnson. 2001. Role of Enterococcus faecalis surface protein Esp in the pathogenesis of ascending urinary tract infection. Infect. Immun. 69: 4366 4372.
137. Sherwood, N.,, B. Russell,, A. Jay,, and K. Bowman. 1949. Studies on streptococci. III. New antibiotic substances produced by beta hemolytic streptococci. J. Infect. Dis. 84: 88 91.
138. Singh, K. V.,, X. Qin,, G. M. Weinstock,, and B. E. Murray. 1998. Generation and testing of mutants of Enterococcus faecalis in a mouse peritonitis model. J . Infect. Dis. 178: 1416 1420.
139. Skurray, R. A.,, and N. Firth, 1997. Molecular evolution of multiply-antibiotic-resistant staphylococci. Ciba Pound. Symp. 207: 167 183; discussion 183 191.
140. Stark, J. 1960. Antibiotic activity of haemolytic enterococci. Lancet i: 733 734.
141. Stevens, S. X.,, H. G. Jensen,, B. D. Jett,, and M. S. Gilmore. 1992. A hemolysin-encoding plasmid contributes to bacterial virulence in experimental Enterococcus faecalis endophthalmitis. Invest. Ophthalmol. Vis. Sci. 33: 1650 1656.
142. Su, Y. A.,, M. C. Sulavik,, P. He,, K. K. Makinen,, P. L. Makinen,, S. Fiedler,, R. Wirth,, and D. B. Clewell. 1991. Nucleotide sequence of the gelatinase gene (gelE) from Enterococcus faecalis subsp. liquefaciens. Infect. Immun. 59: 415 420.
143. Sugai, M.,, T. Enomoto,, K. Hashimoto,, K. Matsumoto,, Y. Matsuo,, H. Ohgai,, Y. M. Hong,, S. Inoue,, K. Yoshikawa,, and H. Suginaka. 1990. A novel epidermal cell differentiation inhibitor (EDIN): purification and characterization from Staphylococcus aureus. Biochem. Biopbys. Res. Commun. 173: 92 98.
144. Sussmuth, S. D.,, A. Muscholl-Silberhorn,, R. Wirth,, M. Susa,, R. Marre,, and E. Rozdzinski. 2000. Aggregation substance promotes adherence, phagocytosis, and intracellular survival of Enterococcus faecalis within human macrophages and suppresses respiratory burst. Infect. Immun. 68: 4900 4906.
145. Takai, S.,, N. Fukunaga,, K. Kamisawa,, Y. Imai,, Y. Sasaki,, and S. Tsubaki. 1996. Expression of virulence-associated antigens of Rhodococcus equi is regulated by temperature and pH. Microbiol. Immunol. 40: 591 594.
146. Takai, S.,, S. A. Hines,, T. Sekizaki,, V. M. Nicholson,, D. A. Alperin,, M. Osaki,, D. Takamatsu,, M. Nakamura,, K. Suzuki,, N. Ogino,, T. Kakuda,, H. Dan,, and J. F. Prescott. 2000. DNA sequence and comparison of virulence plasmids from Rhodococcus equi ATCC 33701 and 103. Infect. Immun. 68: 6840 6847.
147. Takai, S.,, M. lie,, Y. Watanabe,, S. Tsubaki,, and T. Sckizaki. 1992. Virulence-associated 15- to 17-kilodalton antigens in Rhodococcus equh temperature-dependent expression and location of the antigens. Infect. Immun. 60: 2995 2997.
148. Takai, S., Y, Imai, N. Fukunaga, Y. Uchida, K. Kamisawa, Y. Sasaki, S. Tsubaki, and T. Sckizaki. 1995. Identification of virulence-associated antigens and plasmids in Rhodococcus equi from patients with AIDS. J. Infect. Dis. 172: 1306 1311.
149. Takai, S.,, K. Koike,, S. Ohbushi,, C. Izumi,, and S. Tsubaki. 1991. Identification of 15- to 17-kilodalton antigens associated with virulent Rhodococcus equi. J. Clin. Microbiol. 29: 439 443.
150. Takai, S.,, T. Sckizaki,, T. Ozawa,, T. Sugawara,, Y. Watanabe,, and S. Tsubaki. 1991. Association between a large plasmid and 15- to 17-kilodalton antigens in virulent Rhodococcus equi. Infect. Immun. 59: 4056 4060.
151. Takai, S.,, Y. Watanabe,, T. Ikeda,, T. Ozawa,, S. Matsukura,, Y. Tamada,, S. Tsubaki,, and T. Sckizaki. 1993. Virulence-associated plasmids in Rhodococcus equi. J. Clin. Microbiol. 31: 1726 1729.
152. Tan, C.,, J. F. Prescott,, M. C. Patterson,, and V. M. Nicholson. 1995. Molecular characterization of a lipid-modified virulence-associated protein of Rhodococcus equi and its potential in protective immunity. Can. J. Vet. Res. 59: 51 59.
153. Tanimoto, K.,, F. Y. An,, and D. B. Clewell. 1993. Characterization of the traC determinant of the Enterococcus faecalis hemolysin-bactcriocin plasmid pADl: binding of sex pheromone. J. Bacteriol. 175: 5260 5264.
154. Tkachuk-Saad, O.,, and J . Prescott. 1991. Rhodococcus equi plasmids: isolation and partial characterization. J. Clin. Microbiol. 29: 2696 2700.
155. Todd, E. 1934. A comparative serological study of streptolysins derived from human and from animal infections, with notes on pneumococcal hacmolysin, tetanolysin and staphylococcus toxin. J. Pathol. Bacteriol 39: 299 321.
156. Todd, J. K. 1985. Staphylococcal toxin syndromes. Annu. Rev. Med. 36: 337 347.
157. Toledo-Arana, A.,, J. Valle,, C. Solano,, M. J. Arrizubieta,, C. Cucarella,, M. Lamata,, B. Amorena,, J. Leiva,, J. R. Penades,, and I. Lasa. 2001. The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl. Environ. Microbiol. 67: 4538 4545.
158. Tomich, P. K.,, F. Y. An,, S. P, Damle, and D. B. Clewell. 1979. Plasmid-related transmissibility and multiple drug resistance in Streptococcus faecalis subsp. zymogenes strain DS16, Antimicrob. Agents Chemother. 15: 828 830.
159. Vanek, N. N.,, S. I. Simon,, K. Jacques-Palaz,, M. M. Mariscalco,, G. M. Dunny,, and R. M. Rakita. 1999. Enterococcus faecalis aggregation substance promotes opsonin-independent binding to human neutrophils via a complement receptor type 3-mediated mechanism. FEMS Immunol. Med. Microbiol. 26: 49 60.
160. Warren, R.,, M. Rogolsky,, B. B. Wiley,, and L. A. Glasgow. 1974. Effect of ethidium bromide on elimination of exfoliative toxin and bacteriocin production in Staphylococcus aureus. J. Bacteriol. 118: 980 985.
161. Warren, R. L. 1980. Exfoliative toxin plasmids of bacterio-phage group 2 Staphylococcus aureus: sequence homology. Infect. Immun. 30: 601 606.
162. Weaver, K., 2000. Enterococcal genetics, p. 259 271. In V. Fischetti,, R. Novick,, J. Ferretti,, D. Portnoy,, and J. Rood (ed.), Gram-Positive Pathogens. American Society for Microbiology, Washington, D.C..
163. Weaver, K. E.,, and D. B. Clewell. 1989. Construction of Enterococcus faecalis pAD1 miniplasmids: identification of a minimal pheromone response regulatory region and evaluation of a novel pheromone-dependent growth inhibition. Plasmid 22: 106 119.
164. Weaver, K. E.,, D. B. Clewell,, and F. An. 1993. Identification, characterization, and nucleotide sequence of a region of Enterococcus faecalis pheromone-responsive plasmid pAD1 capable of autonomous replication. J. Bacteriol. 175: 1900 1909.
165. Weaver, K. E.,, K. D. Jensen,, A. Colwell,, and S. I. Sriram. 1996. Functional analysis of the Enterococcus faecalis plasmid pAD1-encoded stability determinant par. Mol. Microbiol. 20: 53 63.
166. Wells, C. L.,, R. P. Jechorek,, and S. L. Erlandsen. 1990. Evidence for the translocation of Enterococcus faecalis across the mouse intestinal tract. J Infect. Dis. 162: 82 90.
167. Wieneke, A. A.,, D. Roberts,, and R. J. Gilbert. 1993. Staphylococcal food poisoning in the United Kingdom, 1969-90. Epidemiol. Infect. 110: 519 531.
168. Wiley, B. B.,, L. A. Glasgow,, and M. Rogolsky. 1976. Staphylococcal scalded-skin syndrome: development of a primary binding assay for human antibody to the exfoliative toxin. Infect. Immun. 13: 513 520.
169. Willems, R. J.,, W. Homan,, J. Top,, M. van Santen-Verheuvel,, D. Tribe,, X. Manzioros, C Gaillard, C. M. Vandenbroucke- Grauls, E. M. Mascini, E. van Kregten, J. D. van Embden, and M. J, Bonten. 2001. Variant esp gene as a marker of a distinct genetic lineage of vancomycin-resistant Enterococcus faecium spreading in hospitals. Lancet 357: 853 855.
170.Wirth, R, 1994. The sex pheromone system of Enterococcus faecalis. More than just a plasmid-collection mechanism? Eur.J. Biochem. 222: 235246.
171. Woodford, N. 2001. Epidemiology of the genetic elements responsible for acquired glycopeptide resistance in enterococci. Microb. Drug Resist. 7: 229 236.
172. Yager, J . A.,, C. A. Prescott,, D. P. Kramar,, H. Hannah,, G. A. Balson,, and B. A. Croy. 1991. The effect of experimental infection with Rhodococcus equi on immunodeficient mice. Vet. Microbiol. 28: 363 376.
173. Yamaguchi, T.,, T. Hayashi,, H. Takami,, K. Nakasone,, M. Ohnishi,, K. Nakayama,, S. Yamada,, H. Komatsuzawa,, and M. Sugai. 2000. Phage conversion of exfoliative toxin A production in Staphylococcus aureus. Mol Microbiol. 38: 694 705.
174. Yamaguchi, T.,, T. Hayashi,, H. Takami,, M. Ohnishi,, T. Murata,, K. Nakayama,, K. Asakawa,, M. Ohara,, H. Komatsuzawa,, and M. Sugai. 2001. Complete nucleotide sequence of a Staphylococcus aureus exfoliative toxin B plasmid and identification of a novel ADP-ribosykransfcrase, EDIN-C. Infect. Immun. 69: 7760 7771.
175. Zhang, S. J. J. landolo, and G. C. Stewart. 1998. The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS Microbiol. Lett. 168: 227 233.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error