Superantigen genes encoded by the egc cluster and SaPlbov are predominant among Staphylococcus aureus isolates from cows, goats, sheep, rabbits and poultry

Journal of Medical Microbiology

Volumn 54, Issue 4, 2005, Pages 401-411

  Smyth, Davida S ^a   Hartigan, Patrick J ^a   Meaney, William J ^b   Fitzgerald, J Ross ^a   Deobald, Claudia F ^c   Bohach, Gregory A ^c   Smyth, Cyril J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b ANIMAL AND GRASSLAND RESEARCH AND INNOVATION CENTRE   (Ireland)

^c UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROTOXIN; SUPERANTIGEN; TOXIC SHOCK SYNDROME TOXIN 1;

ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIUM ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; COW; GENE CLUSTER; GENE FREQUENCY; GENE IDENTIFICATION; GENETIC SCREENING; GOAT; MITOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POULTRY; PRIORITY JOURNAL; RABBIT; SEA GENE; SEE GENE; SEG GENE; SEL GENE; SEM GENE; SEN GENE; SEO GENE; SEQ GENE; SHEEP; STAPHYLOCOCCUS AUREUS; STATISTICAL SIGNIFICANCE; T LYMPHOCYTE ACTIVATION; TST GENE;

ANIMALS; BACTERIAL TOXINS; BASE SEQUENCE; CATTLE; DNA PRIMERS; ENTEROTOXINS; GEOGRAPHY; GOATS; MULTIGENE FAMILY; POLYMERASE CHAIN REACTION; POULTRY; RABBITS; SHEEP; STAPHYLOCOCCUS AUREUS; SUPERANTIGENS;

EID: 16844371859     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.45863-0     Document Type: Article

References (76)

1. Akineden, Ö., Annemüller, C., Hassan, A. A., Lämmler, C., Wolter, W. & Zschöck, M. (2001). Toxin genes and other characteristics of Staphylococcus aureus isolates from milk of cows with mastitis. Clin Diagn Lab Immunol 8, 959-964.
2. Alouf, J. E. & Müller-Alouf, H. (2003). Staphylococcal and streptococcal superantigens: molecular, biological and clinical aspects. Int J Med Microbiol 292, 429-440.
3. Balaban, N. & Rasooly, A. (2000). Staphylococcal enterotoxins. Int J Food Microbiol 61, 1-10.
4. Bautista, L., Gaya, P., Medina, M. & Nuñez, M. (1988). A quantitative study of enterotoxin production by sheep milk staphylococci. Appl Environ Microbiol 54, 566-569.
5. Beck, H. S., Wise, W. S. & Dodd, F. H. (1992). Cost benefit analysis of bovine mastitis in the UK. J Dairy Res 59, 449-460.
6. Becker, K., Friedrich, A. W., Lubritz, G., Weilert, M., Peters, G. & von Eiff, C. (2003). Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J Clin Microbiol 41, 1434-1439.
7. Blaiotta, G., Ercolini, D., Pennacchia, C., Fusco, V., Casaburi, A., Pepe, O. & Villani, F. (2004). PCR detection of Staphylococcal enterotoxin genes in Staphylococcus spp. strains isolated from meat and dairy products. Evidence for new variants of seG and seI in S. aureus AB-8802. J Appl Microbiol 97, 719-730.
8. Cenci-Goga, B. T., Karama, M., Rossitto, P. V., Morgante, R. A. & Cullor, J. S. (2003). Enterotoxin production by Staphylococcus aureus isolated from mastitic cows. J Food Prof 66, 1693-1696.
9. Chen, T.-R., Chiou, C.-S. & Tsen, H.-Y. (2004). Use of novel PCR primers specific to the genes of Staphylococcal enterotoxin G, H, I for the survey of Staphylococcus aureus strains isolated from food-poisoning cases and food samples in Taiwan. Int J Food Microbiol 92, 189-197.
10. Dinges, M. M., Orwin, P. M. & Schlievert, P. M. (2000). Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13, 16-34.
11. Fitzgerald, J. R., Meaney, W. J., Hartigan, P. J., Smyth, C. J. & Kapur, V. (1997). Fine-structure molecular epidemiological analysis of Staphylococcus aureus recovered from cows. Epidemiol Infect 119, 261-269.
12. Fitzgerald, J. R., Hartigan, P. J., Meaney, W. J. & Smyth, C. J. (2000). Molecular population and virulence factor analysis of Staphylococcus aureus from bovine intramammary infection. J Appl Microbiol 88, 1028-1037.
13. Fitzgerald, J. R., Monday, S., Foster, T. J., Bohach, G. A., Hartigan, P. J., Meaney, W. J. & Smyth, C. J. (2001). Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol 183, 63-70.
14. Foschino, R., Invernizzi, A., Barucco, R. & Stradiotto, K. (2002). Microbial composition, including the incidence of pathogens, of goat milk from the bergamo region of Italy during a lactation year. J Dairy Sci 69, 213-225.
15. Gruet, P., Maincent, P., Berthelot, X. & Kaltsatos, V. (2001). Bovine mastitis and intramammary drug delivery: review and perspectives. Adv Drug Deliv Rev 50, 245-259.
16. Hazariwala, A., Sanders, CL, Hudson, C. R., Hofacre, C., Thayer, S. G. & Maurer, J. J. (2002). Distribution of Staphylococcal enterotoxin genes among Staphylococcus aureus isolates from poultry and humans with invasive Staphylococcal disease. Avian Dis 46, 132-136.
17. Hentschel, U. & Hacker, J. (2001). Pathogenicity islands: the tip of the iceberg. Microbes Infect 3, 545-548.
18. Herdt, P. (2000). Differentiation between high and low virulence Staphylococcus aureus strains from rabbits by randomly amplified polymorphic DNA (RAPD) analysis. Vet Microbiol 72, 311-319.
19. Hermans, K., Haesebrouck, F., Vaneechoutte, M., Devriese, L. A., Godard, C. & de Hermans, K., Devriese, L. A. & Haesebrouck, F. (2003). Rabbit staphylococcosis: difficult solutions for serious problems. Vet Microbiol 91, 57-64.
20. Ho, G., Campbell, W. H. & Carlson, E. (1989). Ovine-associated Staphylococcus aureus protein with immunochemical similarity to toxic shock syndrome toxin 1. J Clin Microbiol 72, 210-212.
21. Huff, G. R., Huff, W. E., Rath, N. C. & Balog, J. M. (2000). Turkey osteomyelitis complex. Poult Sci 79, 1050-1056.
22. Jablonski, L. M. & Bohach, G. A. (2001). Staphylococcus aureus. In Fundamentals of Food Microbiology, pp. 410-434. Edited by L. Beuchat, M. Doyle & T. Montville. Washington, DC: American Society for Microbiology.
23. Jarraud, S., Peyrat, M. A., Lim, A. & 7 other authors (2001). egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol 166, 669-677 (erratum in J Immunol 166, following 4259).
24. Jarraud, S., Peyrat, M. A., Lim, A. & 7 other authors (2001). egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol 166, 669-677 (erratum in J Immunol 166, following 4259).
25. Kenny, K., Reiser, R. F., Bastida-Corcuera, F. D. & Norcross, N. L. (1993). Production of enterotoxins and toxic shock syndrome toxin by bovine mammary isolates of Staphylococcus aureus. J Clin Microbiol 31, 706-707.
26. Kuroda, M., Ohta, T., Uchiyama, I. & 34 other authors (2001). Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357, 1225-1240.
27. Kuzma, K., Malinowski, E., Lassa, H. & Kłossowska, A. (2003). Detection of genes for enterotoxins and toxic shock syndrome toxin-1 in Staphylococcus aureus isolated from bovine mastitis. Bull Vet Inst Pulawy 47, 419-426.
28. Larsen, H. D., Huda, A., Eriksen, N. H. R. & Jensen, N. E. (2000). Differences between Danish bovine and human Staphylococcus aureus isolates in the possession of superantigens. Vet Microbiol 76, 153-162.
29. Larsen, H. D., Aarestrup, F. M. & Jensen, N. E. (2002). Geographical variation in the presence of genes encoding superantigenic exotoxins and β-hemolysin among Staphylococcus aureus isolated from bovine mastitis in Europe and USA. Vet Microbiol 85, 61-67.
30. Le Loir, Y., Baron, F. & Gautier, M. (2003). Staphylococcus aureus and food poisoning. Genet Mol Res 2, 7-28.
31. Letertre, C., Perelle, S., Dilasser, F. & Fach, P. (2003a). Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J Appl Microbiol 95, 38-43.
32. Letertre, C., Perelle, S., Dilasser, F. & Fach, P. (2003b). Detection and genotyping by real-time PCR of the staphylococcal enterotoxin genes sea to sej. Mol Cell Probes 17, 139-147.
33. Letertre, C., Perelle, S., Dilasser, F. & Fach, P. (2003c). A strategy based on 5′-nuclease multiplex PCR to detect enterotoxin genes sea to sej of Staphylococcus aureus. Mol Cell Probes 17, 227-235.
34. Linares, J. A. & Wigle, W. L. (2001). Staphylococcus aureus pneumonia in turkey poults with gross lesions resembling aspergillosis. Avian Dis 45, 1068-1072.
35. Lindsay, I. A., Ruzin, A., Ross, H. F., Kurepina, N. & Novick, R. P. (1998). The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol 29, 527-543.
36. Llewelyn, M. & Cohen, J. (2002). Superantigens: microbial agents that corrupt immunity. Lancet Infect Dis 2, 156-162.
37. Loncarevic, S. & Mathisen, T. (2004). Characterisation of Staphylococcus aureus enterotoxin type H from a food outbreak. In Proceedings of the 5th World Congress on Foodborne Infections and Intoxications, Berlin, Germany, June 2004, abstract no. P-A10, p. 118. Berlin: Berlin Federal Institute for Risk Assessement.
38. Marr, J. C., Lyon, J. D., Roberson, J. R., Lupher, M., Davis, W. C. & Bohach, G. A. (1993). Characterisation of novel type C staphylococcal enterotoxins: biological and evolutionary implications. Infect Immun 61, 4254-4262.
39. Martin, M. C., Fueyo, J. M., Gonzȧlez-Hevia, M. A. & Mendoza, M. C. (2004). Genetic procedures for identification of enterotoxigenic strains of Staphylococcus aureus from three food poisoning outbreaks. Int J Food Microbiol 94, 279-286.
40. Matsunaga, T., Kamata, S., Kakiichi, N. & Uchida, K. (1993). Characteristics of Staphylococcus aureus isolated from peracute, acute and chronic bovine mastitis. J Vet Med Sci 55, 297-300.
41. McCormick, J. K., Yarwood, J. M. & Schlievert, P. M. (2001). Toxic shock syndrome and bacterial superantigens: an update. Annu Rev Microbiol 55, 77-104.
42. McCullagh, J. J., McNamee, P. T., Smyth, J. A. & Ball, H. J. (1998). The use of pulsed field gel electrophoresis to investigate the epidemiology of Staphylococcus aureus infection in commercial broiler flocks. Vet Microbiol 63, 275-281.
43. McNamee, P. T., McCullagh, J. J., Thorp, B. H., Ball, H. J., Graham, D., McCullough, S. J., McConaghy, D. & Smyth, J. A. (1998). Study of leg weakness in two commercial broiler flocks. Vet Rec 143, 131-135.
44. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., Griffin, P. M. & Tauxe, R. V. (1999). Food-related illness and death in the United States. Emerg Infect Dis 5, 607-625.
45. Mehrotra, M., Wang, G. & Johnson, W. M. (2000). Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1 and methicillin resistance. J Clin Microbiol 38, 1032-1035.
46. Michie, C. A. & Cohen, J. (1998). The clinical significance of T-cell superantigens. Trends Microbiol 6, 61-65.
47. Miles, H., Lesser, W. & Sears, P. (1992). The economic implications of bioengineered mastitis control. J Dairy Sci 75, 596-605.
48. Monday, S. R. & Bohach, G. A. (1999). Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J Clin Microbiol 37, 3411-3414.
49. Nashev, D., Toshkova, K., Salasia, S. I. O., Hassan, A. A., Lämmler, C. & Zschöck, M. (2004). Distribution of virulence genes of Staphylococcus aureus isolated from stable nasal carriers. FEMS Microbiol Lett 233, 45-52.
50. Novick, R. P. (2003). Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49, 93-105.
51. Novick, R. P., Schlievert, P. & Ruzin, A. (2001). Pathogenicity and resistance islands of staphyloccci. Microbes Infect 3, 585-594.
52. Omoe, K., Hu, D.-L., Takahashi-Omoe, H., Nakane, A. & Shinagawa, K. (2003). Identification and characterisation of a new staphylococcal enterotoxin-related putative toxin encoded by two kinds of plasmids. Infect Immun 71, 6088-6094.
53. Orden, J. A., Goyache, J., Hernández, J., Doménech, A., Suárez, G. & Gómez-Lucia, E (1992). Detection of enterotoxins and TSST-1 secreted by Staphylococcus aureus isolated from ruminant mastitis. Comparison of ELISA and immunoblot. J Appl Bacterial 72, 486-489.
54. Orwin, P. M., Leung, D. Y. M., Donahue, H. L., Novick, R. P. & Schlievert, P. M. (2001). Biochemical and biological properties of staphylococcal enterotoxin K. Infect Immun 69, 360-366.
55. Orwin, P. M., Leung, D. Y., Tripp, T. J., Bohach, G. A., Earhart, C. A., Ohlendorf, D. H. & Schlievert, P. M. (2002). Characterisation of a novel staphylococcal enterotoxin-like superantigen, a member of the group V subfamily of pyrogenic toxins. Biochemistry 41, 14033-14040.
56. Orwin, P. M., Fitzgerald, J. R., Leung, D. Y. M., Gutierrez, J. A., Bohach, G. A. & Schlievert, P. M. (2003). Characterization of Staphylococcus aureus enterotoxin L. Infect Immun 71, 2916-2919.
57. Peacock, S. J., Moore, C. E., Justice, A., Kantzanou, M., Story, L., Mackie, K. O'Neill, G. & Day, N. P. J. (2002). Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 70, 4987-4996.
58. Petersson, K., Forsberg, G. & Walse, B. (2004). Interplay between superantigens and immunoreceptors. Scand J Immunol 59, 345-355.
59. Poindexter, N. J. & Schlievert, P. M. (1985). Toxic-shock-syndrome toxin 1-induced proliferation of lymphocytes: comparison of the mitogenic response of human, murine, and rabbit lymphocytes. J Infect Dis 151, 65-72.
60. Proft, T. & Fraser, J. D. (2003). Bacterial superantigens. Clin Exp Immunol 133, 299-306.
61. Rodgers, J. D., McCullagh, J. J., McNamee, P. T., Smyth, J. A. & Ball, H. J. (1999). Comparison of Staphylococcus aureus recovered from personnel in a poultry hatchery and in broiler parent farms with those isolated from skeletal disease in broilers. Vet Microbiol 69, 189-198.
62. Rosec, J. P. & Gigaud, O. (2002). Staphylococcal enterotoxin genes of classical and new types detected by PCR in France. Int J Food Microbiol 77, 61-70.
63. Sambrook, J. & Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
64. Scherrer, D., Corti, S., Muehlherr, J. E., Zweifel, C. & Stephan, R. (2004). Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from raw bulk-tank milk samples of goats and sheep. Vet Microbiol 101, 101-107.
65. Schlievert, P. M., Jablonski, L. M., Roggiani, M., Sadler, I., Callantine, S., Mitchell, D. T., Ohlendorf, D. H. & Bohach, G. A. (2000). Pyrogenic toxin superantigen site specificity in toxic shock syndrome and food poisoning in animals. Infect Immun 68, 3630-3634.
66. Sergeev, N., Volokhov, D., Chizhikov, V. & Rasooly, A. (2004). Simultaneous analysis of multiple Staphylococcal enterotoxin genes by an oligonucleotide microarray assay. J Clin Microbiol 42, 2134-2143.
67. Shimizu, A., Fujita, M., Igarashi, H., Takagi, M., Nagase, N., Sasaki, A. & Kawano, J. (2000). Characterization of Staphylococcus aureus coagulase type VII isolates from Staphylococcal food poisoning outbreaks (1980-1995) in Tokyo, Japan, by pulsed-field gel electrophoresis. J Clin Microbiol 38, 3746-3749.
68. Stulberg, D. L., Penrod, M. A. & Blatny, R. A. (2002). Common bacterial skin infections. Am Fam Physician 66, 119-124.
69. Takeuchi, S., Matsunaga, K., Inubushi, S., Higuchi, H., Imaizumi, K. & Kaidoh, T. (2002). Structural gene and strain specificity of a novel cysteine protease produced by Staphylococcus aureus isolated from a diseased chicken. Vet Microbiol 89, 201-210.
70. Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
71. Webster, K. A. & Mitchell, G. B. (1989). Experimental production of tick pyaemia. Vet Parasitol 34, 129-133.
72. Wieneke, A. A., Roberts, D. & Gilbert, R. J. (1993). Staphylococcal food poisoning in the United Kingdom, 1969-90. Epidemiol Infect 110, 519-531.
73. Woteki, C. E. & Kineman, B. D. (2003). Challenges and approaches to reducing foodborne illness. Annu Rev Nutr 23, 315-344.
74. Yarwood, J. M., McCormick, J. K., Paustian, M. L., Orwin, P. M., Kapur, V. & Schlievert, P. M. (2002). Characterisation and expression analysis of Staphylococcus aureus pathogenicity island 3. J Biol Chem 277, 13138-13147.
75. Zhang, S., Iandolo, J. J. & Stewart, G. C. (1998). The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS Microbiol Lett 168, 227-233.
76. Zschöck, M., Riße, K. & Sommerhäuser, J. (2004). Occurrence and clonal relatedness of sec/tst-gene positive Staphylococcus aureus isolates of quartermilk samples of cows suffering with mastitis. Lett Appl Microbiol 38, 493-498.