Identification of three novel superantigen-encoding genes in Streptococcus equi subsp. zooepidemicus, szeF, szeN, and szeP

Infection and Immunity

Volumn 78, Issue 11, 2010, Pages 4817-4827

  Paillot, Romain ^a   Darby, Alistair C ^b   Robinson, Carl ^a   Wright, Nicola L ^a   Steward, Karen F ^a   Anderson, Emma ^a,f   Webb, Katy ^a   Holden, Matthew T G ^c   Efstratiou, Androulla ^d   Broughton, Karen ^d   Jolley, Keith A ^e   Priestnall, Simon L ^f   Campi, Maria C Marotti ^g   Hughes, Margaret A ^b   Radford, Alan ^b   Erles, Kerstin ^f   Waller, Andrew S ^a  

^a ANIMAL HEALTH TRUST   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d PUBLIC HEALTH ENGLAND   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f ROYAL VETERINARY COLLEGE   (United Kingdom)

^g Al Khaledia Equine Hospital   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; SUPERANTIGEN; SZEF; SZEN; SZEP; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE; GENE IDENTIFICATION; GENETIC CODE; HORSE; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOGENICITY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROPHAGE; SEQUENCE ANALYSIS; STREPTOCOCCUS EQUI ZOOEPIDEMICUS;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; DNA, BACTERIAL; DOG DISEASES; DOGS; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; HORSE DISEASES; HORSES; HUMANS; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS EQUI; SUPERANTIGENS;

EID: 78049420145     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00751-10     Document Type: Article

References (51)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Anzai, T., A. S. Sheoran, Y. Kuwamoto, T. Kondo, R. Wada, T. Inoue, and J. F. Timoney. 1999. Streptococcus equi but not Streptococcus zooepidemicus produces potent mitogenic responses from equine peripheral blood mononuclear cells. Vet. Immunol. Immunopathol. 67:235-246.
3. Arad, G., D. Hillman, R. Levy, and R. Kaempfer. 2001. Superantigen antagonist blocks Th1 cytokine gene induction and lethal shock. J. Leukoc. Biol. 69:921-927.
4. Artiushin, S. C., J. F. Timoney, A. S. Sheoran, and S. K. Muthupalani. 2002. Characterization and immunogenicity of pyrogenic mitogens SePE-H and SePE-I of Streptococcus equi. Microb. Pathog. 32:71-85.
5. Banks, D. J., B. Lei, and J. M. Musser. 2003. Prophage induction and expression of prophage-encoded virulence factors in group A Streptococcus serotype M3 strain MGAS315. Infect. Immun. 71:7079-7086.
6. Beres, S. B., R. Sesso, S. W. Pinto, N. P. Hoe, S. F. Porcella, F. R. Deleo, and J. M. Musser. 2008. Genome sequence of a Lancefield group C Streptococcus zooepidemicus strain causing epidemic nephritis: new information about an old disease. PLoS One 3:e3026.
7. Bradley, S. F., J. J. Gordon, D. D. Baumgartner, W. A. Marasco, and C. A. Kauffman. 1991. Group C streptococcal bacteremia: analysis of 88 cases. Rev. Infect. Dis. 13:270-280.
8. Brooks, D. E., S. E. Andrew, D. J. Biros, H. M. Denis, T. J. Cutler, D. T. Strubbe, and K. N. Gelatt. 2000. Ulcerative keratitis caused by beta-hemolytic Streptococcus equi in 11 horses. Vet. Ophthalmol. 3:121-125.
9. Brosnahan, A. J., M. M. Schaefers, W. H. Amundson, M. J. Mantz, C. A. Squier, M. L. Peterson, and P. M. Schlievert. 2008. Novel toxic shock syndrome toxin-1 amino acids required for biological activity. Biochemistry 47:12995-13003.
10. Brouillard, J. N., S. Gunther, A. K. Varma, I. Gryski, C. A. Herfst, A. K. Rahman, D. Y. Leung, P. M. Schlievert, J. Madrenas, E. J. Sundberg, and J. K. McCormick. 2007. Crystal structure of the streptococcal superantigen SpeI and functional role of a novel loop domain in T cell activation by group V superantigens. J. Mol. Biol. 367:925-934.
11. Carver, T. J., K. M. Rutherford, M. Berriman, M. A. Rajandream, B. G. Barrell, and J. Parkhill. 2005. ACT: the Artemis Comparison Tool. Bioinformatics 21:3422-3423.
12. Chalker, V. J., H. W. Brooks, and J. Brownlie. 2003. The association of Streptococcus equi subsp. zooepidemicus with canine infectious respiratory disease. Vet. Microbiol. 95:149-156.
13. Cunningham, M. W. 2000. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13:470-511.
14. Delcher, A. L., D. Harmon, S. Kasif, O. White, and S. L. Salzberg. 1999. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27:4636-4641.
15. Dellabona, P., J. Peccoud, J. Kappler, P. Marrack, C. Benoist, and D. Mathis. 1990. Superantigens interact with MHC class II molecules outside of the antigen groove. Cell 62:1115-1121. (Pubitemid 20333771)
16. Didelot, X., and D. Falush. 2007. Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251-1266. (Pubitemid 46798228)
17. Downar, J., B. M. Willey, J. W. Sutherland, K. Mathew, and D. E. Low. 2001. Streptococcal meningitis resulting from contact with an infected horse. J. Clin. Microbiol. 39:2358-2359.
18. Fraser, J. D., and T. Proft. 2008. The bacterial superantigen and superantigen-like proteins. Immunol. Rev. 225:226-243.
19. Hashikawa, S., Y. Iinuma, M. Furushita, T. Ohkura, T. Nada, K. Torii, T. Hasegawa, and M. Ohta. 2004. Characterization of group C and G streptococcal strains that cause streptococcal toxic shock syndrome. J. Clin. Microbiol. 42:186-192.
20. Holden, M. T., Z. Heather, R. Paillot, K. F. Steward, K. Webb, F. Ainslie, T. Jourdan, N. C. Bason, N. E. Holroyd, K. Mungall, M. A. Quail, M. Sanders, M. Simmonds, D. Willey, K. Brooks, D. M. Aanensen, B. G. Spratt, K. A. Jolley, M. C. Maiden, M. Kehoe, N. Chanter, S. D. Bentley, C. Robinson, D. J. Maskell, J. Parkhill, and A. S. Waller. 2009. Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathog. 5:e1000346.
21. Hong, C. B., J. M. Donahue, R. C. Giles, Jr., M. B. Petrites-Murphy, K. B. Poonacha, A. W. Roberts, B. J. Smith, R. R. Tramontin, P. A. Tuttle, and T. W. Swerczek. 1993. Etiology and pathology of equine placentitis. J. Vet. Diagn. Invest. 5:56-63.
22. Ikebe, T., A. Wada, Y. Inagaki, K. Sugama, R. Suzuki, D. Tanaka, A. Tamaru, Y. Fujinaga, Y. Abe, Y. Shimizu, and H. Watanabe. 2002. Dissemination of the phage-associated novel superantigen gene speL in recent invasive and noninvasive Streptococcus pyogenes M3/T3 isolates in Japan. Infect. Immun. 70:3227-3233.
23. Jorm, L. R., D. N. Love, G. D. Bailey, G. M. McKay, and D. A. Briscoe. 1994. Genetic structure of populations of beta-haemolytic Lancefield group C streptococci from horses and their association with disease. Res. Vet. Sci. 57:292-299.
24. Kurtz, S., A. Phillippy, A. L. Delcher, M. Smoot, M. Shumway, C. Antonescu, and S. L. Salzberg. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5:R12.
25. Las Heras, A., A. I. Vela, E. Fernandez, E. Legaz, L. Dominguez, and J. F. Fernandez-Garayzabal. 2002. Unusual outbreak of clinical mastitis in dairy sheep caused by Streptococcus equi subsp. zooepidemicus. J. Clin. Microbiol. 40:1106-1108.
26. Li, L., C. J. Stoeckert, Jr., and D. S. Roos. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189.
27. Llewelyn, M., and J. Cohen. 2002. Superantigens: microbial agents that corrupt immunity. Lancet Infect. Dis. 2:156-162.
28. Lowe, T. M., and S. R. Eddy. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955-964.
29. Lukashin, A. V., and M. Borodovsky. 1998. GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26:1107-1115.
30. Marmur, J. 1961. A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J. Mol. Biol. 3:208-218.
31. Nooh, M. M., R. K. Aziz, M. Kotb, A. Eroshkin, W. J. Chuang, T. Proft, and R. Kansal. 2006. Streptococcal mitogenic exotoxin, SmeZ, is the most susceptible M1T1 streptococcal superantigen to degradation by the streptococcal cysteine protease, SpeB. J. Biol. Chem. 281:35281-35288.
32. Norrby-Teglund, A., M. Norgren, S. E. Holm, U. Andersson, and J. Andersson. 1994. Similar cytokine induction profiles of a novel streptococcal exotoxin, MF, and pyrogenic exotoxins A and B. Infect. Immun. 62:3731-3738.
33. Paillot, R., C. Robinson, K. Steward, N. Wright, T. Jourdan, N. Butcher, Z. Heather, and A. Waller. 2010. Contribution of each of four superantigens to Streptococcus equi-induced mitogenicity, IFN gamma synthesis and immunity. Infect. Immun. 78:1728-1739.
34. Pesavento, P. A., K. F. Hurley, M. J. Bannasch, S. Artiushin, and J. F. Timoney. 2008. A clonal outbreak of acute fatal hemorrhagic pneumonia in intensively housed (shelter) dogs caused by Streptococcus equi subsp. zooepidemicus. Vet. Pathol. 45:51-53.
35. Proft, T., and J. D. Fraser. 2003. Bacterial superantigens. Clin. Exp. Immunol. 133:299-306.
36. Proft, T., P. D. Webb, V. Handley, and J. D. Fraser. 2003. Two novel superantigens found in both group A and group C Streptococcus. Infect. Immun. 71:1361-1369.
37. Rutherford, K., J. Parkhill, J. Crook, T. Horsnell, P. Rice, M. A. Rajandream, and B. Barrell. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945.
38. Salasia, S. I., I. W. Wibawan, F. H. Pasaribu, A. Abdulmawjood, and C. Lammler. 2004. Persistent occurrence of a single Streptococcus equi subsp. zooepidemicus clone in the pig and monkey population in Indonesia. J. Vet. Sci. 5:263-265.
39. Sharp, M. W., M. J. Prince, and J. Gibbens. 1995. S. zooepidemicus infection and bovine mastitis. Vet. Rec. 137:128.
40. Shupp, J. W., M. Jett, and C. H. Pontzer. 2002. Identification of a transcytosis epitope on staphylococcal enterotoxins. Infect. Immun. 70:2178-2186.
41. Smith, K. C., A. S. Blunden, K. E. Whitwell, K. A. Dunn, and A. D. Wales. 2003. A survey of equine abortion, stillbirth and neonatal death in the UK from 1988 to 1997. Equine Vet. J. 35:496-501.
42. Soedarmanto, I., F. H. Pasaribu, I. W. Wibawan, and C. Lammler. 1996. Identification and molecular characterization of serological group C streptococci isolated from diseased pigs and monkeys in Indonesia. J. Clin. Microbiol. 34:2201-2204.
43. Sriskandan, S., L. Faulkner, and P. Hopkins. 2007. Streptococcus pyogenes: Insight into the function of the streptococcal superantigens. Int. J. Biochem. Cell Biol. 39:12-19.
44. Stevenson, R. G. 1974. Streptococcus zooepidemicus infection in sheep. Can. J. Comp. Med. 38:243-250.
45. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
46. Tettelin, H., V. Masignani, M. J. Cieslewicz, J. A. Eisen, S. Peterson, M. R. Wessels, I. T. Paulsen, K. E. Nelson, I. Margarit, T. D. Read, L. C. Madoff, A. M. Wolf, M. J. Beanan, L. M. Brinkac, S. C. Daugherty, R. T. DeBoy, A. S. Durkin, J. F. Kolonay, R. Madupu, M. R. Lewis, D. Radune, N. B. Fedorova, D. Scanlan, H. Khouri, S. Mulligan, H. A. Carty, R. T. Cline, S. E. Van Aken, J. Gill, M. Scarselli, M. Mora, E. T. Iacobini, C. Brettoni, G. Galli, M. Mariani, F. Vegni, D. Maione, D. Rinaudo, R. Rappuoli, J. L. Telford, D. L. Kasper, G. Grandi, and C. M. Fraser. 2002. Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc. Natl. Acad. Sci. U. S. A. 99:12391-12396.
47. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 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.
48. Tokura, Y., F. Furukawa, H. Wakita, H. Yagi, T. Ushijima, and M. Takigawa. 1997. T-cell proliferation to superantigen-releasing Staphylococcus aureus by MHC class II-bearing keratinocytes under protection from bacterial cytolysin. J. Invest. Dermatol. 108:488-494.
49. Webb, K., K. A. Jolley, Z. Mitchell, C. Robinson, J. R. Newton, M. C. Maiden, and A. Waller. 2008. Development of an unambiguous and discriminatory multilocus sequence typing scheme for the Streptococcus zooepidemicus group. Microbiology 154:3016-3024.
50. Wood, J. L., M. H. Burrell, C. A. Roberts, N. Chanter, and Y. Shaw. 1993. Streptococci and Pasteurella spp. associated with disease of the equine lower respiratory tract. Equine Vet. J. 25:314-318.
51. Wood, J. L., J. R. Newton, N. Chanter, and J. A. Mumford. 2005. Association between respiratory disease and bacterial and viral infections in British racehorses. J. Clin. Microbiol. 43:120-126.