Chapter 15 : Staphylococcal Phages

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The staphylococci are highly lysogenic; it is a rare strain that harbors no prophage. This chapter details the relationships between lysogeny and pathogenicity in the staphylococci. An infecting bacteriophage may either immediately replicate itself, causing lysis of the host bacterium, or integrate its DNA into the bacterial chromosome, leading to a state of lysogeny. Staphylokinase (SAK) is only one of several virulence factors that may be carried by beta-hemolysin-converting phages. Several prophages that are integrated into and carry different alleles of putative enterotoxin genes have been found in sequenced genomes. The positioning of enterotoxin genes on prophages may allow for the diversification of toxins that are capable of both attacking and evading the ever-evolving mammalian immune system. The very first reported association between lysogeny and toxigenicity in involved alpha-hemolysin, but it has not been confirmed, nor has conversion to delta-hemolysin production. Staphylococcal phages in other families exist, but none have been linked to virulence. Several broad generalizations can be made about the medically important staphylococcal phages. These generalizations will certainly be refuted as more staphylococcal phages are discovered, given the propensity of bacteriophages to recombine. A chromosomal gene that is adjacent to an integrated prophage can be mobilized by aberrant prophage excision. The simultaneous diversification and circulation of pathogenicity factors by prophages and other mobile elements contribute mightily to the pathogenic versatility of the staphylococci.

Citation: Matthews A, Novick R. 2005. Staphylococcal Phages, p 297-318. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch15

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Toxic Shock Syndrome Toxin 1
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Alignment of putative GEH catalytic domains, with key residues indicated with asterisks. The area corresponding to the 18-kb core site is shown in a box ( ). In strain COL, there is a prophage inserted in immediately downstream of this core.

Citation: Matthews A, Novick R. 2005. Staphylococcal Phages, p 297-318. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch15
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ϕETA. Bar, 100 nm. Reprinted from with permission of the publisher.

Citation: Matthews A, Novick R. 2005. Staphylococcal Phages, p 297-318. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch15
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ϕSTL. Bar, 100 nm. Reprinted from with permission of the publisher.

Citation: Matthews A, Novick R. 2005. Staphylococcal Phages, p 297-318. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch15
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1. Aarestrup, F. M.,, and H. C. Wegener. 1997. Association between production of fibrinolysin and virulence of Staphylococcus hyicus in relation to exudative epidermitis in pigs. Acta Vet. Scand. 38: 295 297.
2. Abramson, C., 1972. Staphylococcal enzymes, p. 187 248. In J. O. Cohen (ed.), The Staphylococci. Wiley-Interscience, New York,N.Y.
3. Ackerman, H.-W.,, and S. T. Abedon. 2000. Bacteriophage names 2000. [Online.] www.phage. org/names.htm.
4. Alouf, J. E.,, and H. Muller-Alouf. 2003. Staphylococcal and streptococcal superantigens: molecular, biological and clinical aspects. Int. J. Med. Microbiol. 292: 429 440.
5. Altura, B. M.,, A. Gebrewold,, T. Zheng,, and B.T. Altura. 2002. Sphingomyelinase and ceramide analogs induce vasoconstriction and leukocyte-endothelial interactions in cerebral venules in the intact rat brain: insight into mechanisms and possible relation to brain injury and stroke. Brain Res. Bull. 58: 271 278.
6. 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.
7. Arbuthnott, J. P., 1982. Bacterial cytolysins (membrane-damaging toxins), p. 107 129. In P. C. A. S.V. Heyningen (ed.), Molecular Action of Toxins and Viruses. Elsevier Biomedical Press, Amsterdam, The Netherlands.
8. Arvidson, S., 1983. Extracellular enzymes from Staphylococcus aureus, p. 745 808. In C. S. F. Eastmon, and C. Adlam (ed.), Staphylococci and Staphylococcal Infections, vol. 2. Academic Press, London, United Kingdom.
9. Baba, T.,, F. Takeuchi,, M. Kuroda,, H. Yuzawa,, K. Aoki,, A. Oguchi,, Y. Nagai,, N. Iwama,, K. Asano,, T. Naimi,, H. Kuroda,, L. Cui,, K. Yamamoto,, and K. Hiramatsu. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359: 1819 1827.
10. Becker, K.,, G. Haverkamper,, C. von Eiff,, R. Roth,, and G. Peters. 2001. Survey of staphylococcal enterotoxin genes, exfoliative toxin genes, and toxic shock syndrome toxin 1 gene in non-Staphylococcus aureus species. Eur. J. Clin. Microbiol. Infect. Dis. 20: 407 409.
11. Beecher, D. J.,, and A. C. Wong. 2000. Cooperative, synergistic and antagonistic haemolytic interactions between haemolysin BL, phosphatidylcholine phospholipase C and sphingomyelinase from Bacillus cereus. Microbiology 146: 3033 3039.
12. Bergdoll, M. S., 1983. Enterotoxins, p. 559 598. In C. S. F. Easmon, and C. Adlam (ed.), Staphylococci and Staphylococcal Infections, vol. 2. Academic Press, London, United Kingdom.
13. Bergdoll, M. S.,, B. A. Crass,, R. F. Reiser,, R. N. Robbins,, and J. P. Davis. 1981. A new staphylococcal enterotoxin, enterotoxin F, associated with toxic-shock-syndrome Staphylococcus aureus isolates. Lancet i: 1017 1021.
14. Bergdoll, M. S.,, B. A. Crass,, R. F. Reiser,, R. N. Robbins,, A. C. Lee,, P. J. Chesney,, J. P. Davis,, J. M. Vergeront,, and P. J. Wand. 1982. An enterotoxin-like protein in Staphylococcus aureus strains from patients with toxic shock syndrome. Ann. Intern. Med. 96: 969 971.
15. Betley, M. J.,, S. Lofdahl,, B. N. Kreiswirth,, M. S. Bergdoll,, and R. P. Novick. 1984. Staphylococcal enterotoxin A gene is associated with a variable genetic element. Proc. Natl.Acad. Sci.USA 81: 5179 5183.
16. Betley, M. J.,, and J. J. Mekalanos. 1985. Staphylococcal enterotoxin A is encoded by phage. Science 229: 185 187.
17. Betley, M. J.,, V. L. Miller,, and J. J. Mekalanos. 1986. Genetics of bacterial enterotoxins. Annu. Rev. Microbiol. 40: 577 605.
18. Betley, M. J.,, P.M. Schlievert,, M. S. Bergdoll,, G. A. Bohach,, J. J. Iandolo,, S. A. Khan,, P. A. Patee,, and R. F. Reiser. 1990. Staphylococcal gene nomenclature. ASM News 56: 182.
19. Birmingham, V. A.,, and P. A. Pattee. 1981. Genetic transformation in Staphylococcus aureus: isolation and characterization of a competence-conferring factor from bacteriophage 80 alpha lysates. J. Bacteriol. 148: 301 307.
20. Blair, J. E.,, and M. Carr. 1961. Lysogeny in the staphylococci. J. Bacteriol. 82: 984 993.
21. Bohach, G. A., 1997. Staphylococcal enterotoxins B and C, p. 167 198. In D. Y. M. Leung,, B. T. Huber,, and P. M. Schlievert (ed.), Superantigens: Molecular Biology, Immunology, and Relevance to Human Disease. Marcel Dekker, New York, N.Y.
22. Bohach, G. A.,, and T. J. Foster,. 2000. Staphylococcus aureus exotoxins, p. 367 378. In V. A. Fischetti et al. (ed.), Gram-Positive Pathogens. American Society for Microbiology, Washington, D.C.
23. Bon, J.,, N. Mani,, and R. K. Jayaswal. 1997. Molecular analysis of lytic genes of bacteriophage 80 alpha of Staphylococcus aureus. Can. J. Microbiol. 43: 612 616.
24. Borst, D. W.,, and M. J. Betley. 1993. Mutations in the promoter spacer region and early transcribed region increase expression of staphylococcal enterotoxin A. Infect. Immun. 61: 5421 5425.
25. Borst, D. W.,, and M. J. Betley. 1994. Phageassociated differences in staphylococcal enterotoxin A gene ( sea) expression correlate with sea allele class. Infect. Immun. 62: 113 118.
26. Borst, D. W.,, and M. J. Betley. 1994. Promoter analysis of the staphylococcal enterotoxin A gene. J. Biol. Chem. 269: 1883 1888.
27. Botstein, D. 1980. A theory of modular evolution for bacteriophages. Ann. N.Y. Acad. Sci. 354: 484 491.
28. Bramley, A. J.,, A.H. Patel,, M. O’Reilly,, R. Foster,, and T. J. Foster. 1989. Roles of alpha-toxin and beta-toxin in virulence of Staphylococcus aureus for the mouse mammary gland. Infect. Immun. 57: 2489 2494.
29. Carroll, D.,, M. A. Kehoe,, D. Cavanagh,, and D. C. Coleman. 1995. Novel organization of the site-specific integration and excision recombination functions of the Staphylococcus aureus serotype F virulence-converting phages phi 13 and phi 42. Mol. Microbiol. 16: 877 893.
30. Casman, E. P. 1965. Staphylococcal enterotoxin. Ann.N.Y.Acad. Sci. 128: 124 131.
31. Chesbro, W. R.,, F. P. Heydrick,, R. Martineau,, and G. N. Perkins. 1965. Purification of staphylococcal β-hemolysin and its action on staphylococcal and streptococcal cell walls. J. Bacteriol. 89: 329 389.
32. Christensson, B.,, F. J. Fehrenbach,, and S. A. Hedstrom. 1985. A new serological assay for Staphylococcus aureus infections: detection of IgG antibodies to S. aureus lipase with an enzyme-linked immunosorbent assay. J. Infect. Dis. 152: 286 292.
33. Christie, R.,, N. E. Atkins,, and E. Munch-Petersen. 1944. A note on a lytic phenomenon shown by group B streptococci. Aust. J. Exp. Biol. Med. Sci. 22: 197 200.
34. Christie, R.,, and E. A. North. 1941. Observations on staphylococcal beta toxin and its production by strains isolated from staphylococcal lesions in man. Aust. J. Exp. Biol. Med. Sci. 19: 323 327.
35. Christie, R.,, and H. Wilson. 1941. A test of staphylococcal coagulation and fibrinolysin. Aust. J. Exp. Biol. Med. Sci. 19: 329.
36. Ciborowski, P.,, and J. Jeljaszewicz,. 1985. Staphylococcal enzymes and virulence, p. 145 183. In I. A. Holder (ed.), Bacterial Enzymes and Virulence. CRC Press, Inc., Boca Raton, Fla.
37. Clecner, B.,, and S. Sonea. 1966. Acquisition of the delta type of hemolytic property by lysogenic conversion in Staphylococcus aureus. Rev. Can. Biol. 25: 145 148.
38. Coleman, D. C.,, J. P. Arbuthnott,, H. M. Pomeroy,, and T. H. Birkbeck. 1986. 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: 549 564.
39. Coleman, D. C.,, D. J. Sullivan,, R. J. Russell,, J. P. Arbuthnott,, B. F. Carey,, and H. M. Pomeroy. 1989. Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of beta-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. J. Gen. Microbiol. 135: 1679 1697.
40. Collen, D. 1998. Staphylokinase: a potent, uniquely fibrin-selective thrombolytic agent. Nat. Med. 4: 279 284.
41. Colley, C. M.,, R. F. A. Zwaal,, B. Roelofsen,, and L. L. M. Van Deenen. 1973. Lytic and nonlytic degradation of phospholipase in mammalian erythrocytes by pure phospholipases. Biochim. Biophys. Acta 307: 74 82.
42. Couch, J. L.,, M. T. Soltis,, and M. J. Betley. 1988. Cloning and nucleotide sequence of the type E staphylococcal enterotoxin gene. J. Bacteriol. 170: 2954 2960.
43. Cribier, B.,, Y. Piemont,, and E. Grosshans. 1994. Staphylococcal scalded skin syndrome in adults.A clinical review illustrated with a new case. J.Am.Acad. Dermatol. 30: 319 324.
44. Davidson, F. M. 1960. The activation of plasminogen by staphylokinase: comparison with streptokinase. Biochem. J. 76: 56 61.
45. de Haas, C. J. C.,, K. E. Veldkamp,, A. Peschel,, F. Weerkamp,, W. J. B. Van Wamel,, E. C. J. M. Heezius,, M. J. J. G. Poppelier,, K. P. M. Van Kessel,, and J. A. G. van Strijp. 2004. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J.Exp.Med. 199: 687 695.
46. Deresiewicz, R. L., 1997. Staphylococcal toxic shock syndrome, p. 435 479. In D. Y. M. Leung,, B.T. Huber,, and P.M. Schlievert (ed.), Superantigens: Molecular Biology, Immunology, and Relevance to Human Disease. Marcel Dekker, New York,N.Y.
47. Devriese, L. A.,, and A. Van De Kerckhove. 1980. A comparison of methods used for testing staphylokinase (fibrinolysin) production in Staphylococcus strains. Antonie Leeuwenhoek 46: 457 465.
48. de Waart, J.,, K. C. Winkler,, and C. Groosten. 1962. Lysogenic conversion in staphylococci. Nature 195: 407.
49. d’Herelle, F. 1921. Le Bactériophages: Son Rôle dans l’Immunité. Masson et Cie, Paris, France.
50. Dinges, M. M.,, P. M. Orwin,, and P. M. Schlievert. 2000. Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 13: 16 34.
51. Dobardzic, R.,, and S. Sonea. 1971. Hemolysin production and lysogenic conversion in Staphylococcus aureus. Ann. Inst. Pasteur (Paris) 120: 42 49.
52. Dulong de Rosnay, C.,, and P. Desnues. 1967. Lysogénisation et critéres de pathogénicité chez Staphylococcus aureus. C. R. Soc. Biol. 161: 1699 1702.
53. Duval-Iflah, Y. 1972. Lysogenic conversion of the lipase in Staphylococcus pyogenes group II strains. Can. J. Microbiol. 18: 1491 1497.
54. Duval-Iflah, Y. 1972. Recombination in staphylococcal bacteriophages. J. Gen.Virol. 16: 237 243.
55. Duval-Iflah, Y.,, J. Van Heijenoort,, M. Rousseau,, and P. Raibaud. 1977. Lysogenic conversion for multiple characters in a strain of Staphylococcus aureus. J. Bacteriol. 130: 1281 1291.
56. Earhart, C. A.,, D. T. Mitchell,, D. L. Murray,, P. M. Schlievert,, and D. H. Ohlendorf,. 1997. Toxic shock syndrome toxin-1, p. 127 148. In D. Y. M. Leung,, B.T. Huber,, and P. M. Schlievert (ed.), Superantigens: Molecular Biology, Immunology, and Relevance to Human Disease. Marcel Dekker, New York, N.Y.
57. Edelwejn, Z.,, J. Jeljaszewicz,, T. Wadström,, R. Möllby,, and G. Pulverer. 1971. Presented at the 2nd International Symposium on Staphylococci and Staphylococcal Infection Recent Progress, Warsaw, Poland.
58. Elek, S. D.,, and E. Levy. 1950. Distribution of haemolysins in pathogenic and non-pathogenic staphylococci. J. Pathol. Bacteriol. 62: 541 554.
59. Erlandsson, E.,, K. Andersson,, A. Cavallin,, A. Nilsson,, U. Larsson-Lorek,, U. Niss,, A. Sjoberg,, M. Wallen-Ohman,, P. Antonsson,, B. Walse,, and G. Forsberg. 2003. Identification of the antigenic epitopes in staphylococcal enterotoxins A and E and design of a superantigen for human cancer therapy. J. Mol. Biol. 333: 893 905.
60. Fitzgerald, J. R.,, S. R. Monday,, T. J. Foster,, G. A. Bohach,, P. J. Hartigan,, W. J. Meaney,, and C. J. Smyth. 2001. Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J. Bacteriol. 183: 63 70.
61. Freer, J. H.,, and J. P. Arbuthnott. 1983. Toxins of Staphylococcus aureus. Pharmacol.Ther. 19: 55 106.
62. Fritsche, D. 1971. The role of lipases in the lipoid and total metabolism of Staphylococcus aureus. Zentbl. Bakteriol. 217: 483 500.
63. Garbe, P. L.,, R. J. Arko,, A. L. Reingold,, L. M. Graves,, P. S. Hayes,, A. W. Hightower,, F.W. Chandler,, and C. V. Broome. 1985. Staphylococcus aureus isolates from patients with non-menstrual toxic shock syndrome. Evidence for additional toxins. JAMA 253: 2538 2542.
64. Gemmell, C. G., 1983. Extracellular toxins and enzymes of coagulase-negative staphylococci, p. 809 827. In C. S. F. Eastmon, and C. Adlam (ed.), Staphylococci and Staphylococcal Infections, vol. 2. Academic Press, London, United Kingdom.
65. Gillet, Y.,, B. Issartel,, P. Vanhems,, J. C. Fournet,, G. Lina,, M. Bes,, F. Vandenesch,, Y. Piemont,, N. Brousse,, D. Floret,, and J. Etienne. 2002. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immuno-competent patients. Lancet 359: 753 759.
66. Gladysheva, I. P.,, R. B. Turner,, I. Y. Sazonova,, L. Liu,, and G. L. Reed. 2003. Coevolutionary patterns in plasminogen activation. Proc. Natl. Acad. Sci. USA 100: 9168 9172.
67. Gonzalez-Zorn, B.,, G. Dominguez-Bernal,, M. Suarez,, M.T. Ripio,, Y. Vega,, S. Novella,, and J. A. Vazquez-Boland. 1999. The smcL gene of Listeria ivanovii encodes a sphingomyelinase C that mediates bacterial escape from the phagocytic vacuole. Mol. Microbiol. 33: 510 523.
68. Gow, J.A.,, and J. Robinson. 1969. Properties of purified staphylococcal beta-hemolysin. J. Bacteriol. 97: 1026 1032.
69. Hanakawa, Y.,, N. M. Schechter,, C. Lin,, L. Garza,, H. Li,, T. Yamaguchi,, Y. Fudaba,, K. Nishifuji,, M. Sugai,, M. Amagai,, and J. R. Stanley. 2002. Molecular mechanisms of blister formation in bullous impetigo and staphylococcal scalded skin syndrome. J. Clin. Investig. 110: 53 60.
70. Hedstrom, S.A. 1975. Lipolytic activity of Staphylococcus aureus strains from cases of human chronic osteomyelitis and other infections. Acta Pathol. Microbiol. Scand. B 83: 285 292.
71. Hedstrom, S. A.,, and T. Malmqvist. 1982. Sphingomyelinase activity of Staphylococcus aureus strains from recurrent furunculosis and other infections. Acta Pathol. Microbiol. Immunol. Scand. B 90: 217 220.
72. Iandolo, J. J.,, V. Worrell,, K. H. Groicher,, Y. Qian,, R. Tian,, S. Kenton,, A. Dorman,, H. Ji,, S. Lin,, P. Loh,, S. Qi,, H. Zhu,, and B. A. Roe. 2002. Comparative analysis of the genomes of the temperate bacteriophages phi 11, phi 12 and phi 13 of Staphylococcus aureus 8325. Gene 289: 109 118.
73. Jackson, M. P.,, J. DeSena,, J. Lednicky,, B. McPherson,, R. Haile,, R. G. Garrison,, and M. Rogolsky. 1983. Isolation and characterization of a bacteriophage factor that confers competence for genetic transformation to an exfoliative toxin-producing strain of Staphylococcus aureus. Infect. Immun. 39: 939 947.
74. Jarvis, A. W.,, and R. C. Lawrence. 1971. Production of extracellular enzymes and enterotoxins A, B, and C by Staphylococcus aureus. Infect. Immun. 4: 110 115.
75. Jarvis, W. D.,, R. N. Kolesnick,, F.A. Fornari,, R. S. Traylor,, D.A. Gewirtz,, and S. Grant. 1994. Induction of apoptotic DNA damage and cell death by activation of the sphingomyelin pathway. Proc. Natl. Acad. Sci. USA 91: 73 77.
76. Jasper, D. E.,, and N. C. Jain. 1966. Hemolytic behavior of staphylococci isolated from cows’ milk. Can. J. Comp. Med.Vet. Sci. 30: 63 70.
77. Jeljaszewicz, J., 1972. Toxins (hemolysins), p. 249 280. In J. O. Cohen (ed.), The Staphylococci. Wiley-Interscience, New York,N.Y.
78. Jessen, O.,, K. Rosendal,, V. Faber,, K. Hove,, and K. Riewerts Eriksen. 1963. Some properties of Staphylococcus aureus, possibly related to pathogenicity. III. Bacteriological investigations of Staphylococcus aureus strains from 462 cases of bacteraemia. Acta Pathol. Microbiol. Scand. 58: 85 98.
79. Jin, T.,, M. Bokarewa,, T. Foster,, J. Mitchell,, J. Higgins,, and A. Tarkowski. 2004. Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J. Immunol. 172: 1169 1176.
80. Johnson, L. P.,, and P. M. Schlievert. 1984. Group A streptococcal phage T12 carries the structural gene for pyrogenic exotoxin type A. Mol. Gen. Genet. 194: 52 56.
81. Jollick, J. D. 1972. Evidence for bacteriophage conversion in Staphylococcus. Microbios 6: 97 100.
82. Kaneko, J.,, T. Kimura,, Y. Kawakami,, T. Tomita,, and Y. Kamio. 1997. Panton-Valentine leukocidin genes in a phage-like particle isolated from mitomycin C-treated Staphylococcus aureus V8 (ATCC 49775). Biosci. Biotechnol. Biochem. 61: 1960 1962.
83. Kaneko, J.,, T. Kimura,, S. Narita,, T. Tomita,, and Y. Kamio. 1998. Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. Gene 215: 57 67.
84. Kondo, I.,, and K. Fujise. 1977. Serotype B staphylococcal bacteriophage singly converting staphylokinase. Infect. Immun. 18: 266 272.
85. Krut, O.,, O. Utermohlen,, X. Schlossherr,, and M. Kronke. 2003. Strain-specific association of cytotoxic activity and virulence of clinical Staphylococcus aureus isolates. Infect. Immun. 71: 2716 2723.
86. Kuroda, M.,, T. Ohta,, I. Uchiyama,, T. Baba,, H. Yuzawa,, I. Kobayashi,, L. Cui,, A. Oguchi,, K. Aoki,, Y. Nagai,, J. Lian,, T. Ito,, M. Kanamori,, H. Matsumaru,, A. Maruyama,, H. Murakami,, A. Hosoyama,, Y. Mizutani-Ui,, N. K. Takahashi,, T. Sawano,, R. Inoue,, C. Kaito,, K. Sekimizu,, H. Hirakawa,, S. Kuhara,, S. Goto,, J. Yabuzaki,, M. Kanehisa,, A. Yamashita,, K. Oshima,, K. Furuya,, C. Yoshino,, T. Shiba,, M. Hattori,, N. Ogasawara,, H. Hayashi,, and K. Hiramatsu. 2001. Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357: 1225 1240.
87. Lack, C. H.,, and K. L. A. Glanville. 1979. Staphylokinase. Methods Enzymol. 1979: 209 714.
88. Ladhani, S.,, and R. W. Evans. 1998. Staphylococcal scalded skin syndrome. Arch. Dis. Child 78: 85 88.
89. Lahteenmaki, K.,, P. Kuusela,, and T. K. Korhonen. 2001. Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25: 531 552.
90. Lang, S.,, and M. Palmer. 2003. Characterization of Streptococcus agalactiae CAMP factor as a pore-forming toxin. J. Biol. Chem. 278: 38167 38173.
91. Lee, C.Y.,, S. L. Buranen,, and Z. H. Ye. 1991. Construction of single-copy integration vectors for Staphylococcus aureus. Gene 103: 101 105.
92. Lee, C.Y.,, and J. J. Iandolo. 1986. Integration of staphylococcal phage L54a occurs by sitespecific recombination: structural analysis of the attachment sites. Proc. Natl. Acad. Sci.USA 83: 5474 5478.
93. Lee, C.Y.,, and J. J. Iandolo. 1986. Lysogenic conversion of staphylococcal lipase is caused by insertion of the bacteriophage L54a genome into the lipase structural gene. J. Bacteriol. 166: 385 391.
94. Lee, C.Y.,, and J. J. Iandolo. 1985. Mechanism of bacteriophage conversion of lipase activity in Staphylococcus aureus. J. Bacteriol. 164: 288 293.
95. Le Loir, Y.,, F. Baron,, and M. Gautier. 2003. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2: 63 76.
96. Lina, G.,, J. Etienne,, and F. Vandenesch,. 2000. Biology and pathogenicity of staphylococci other than Staphylococcus aureus and Staphylococcus epidermidis, p. 450 462. In V. A. Fischetti (ed.), Gram-Positive Pathogens. American Society for Microbiology, Washington, D.C.
97. Lina, G.,, Y. Piemont,, F. Godail-Gamot,, M. Bes,, M. O. Peter,, V. Gauduchon,, F. Vandenesch,, and J. Etienne. 1999. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis. 29: 1128 1132.
98. Lindsay, J.A.,, A. Ruzin,, H. F. Ross,, N. Kurepina,, and R. P. Novick. 1998. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol. Microbiol. 29: 527 543.
99. Low, D. K. R.,, and J. H. Freer. 1977. Biological effects of highly purified beta-lysin (sphingomyelinase C) from Staphylococcus aureus. FEMS Microbiol. Lett. 2: 133 138.
100. Lowe, A. M.,, D.T. Beattie,, and R. L. Deresiewicz. 1998. Identification of novel staphylococcal virulence genes by in vivo expression technology. Mol. Microbiol. 27: 967 976.
101. Marshall, M. J.,, G. A. Bohach,, and D. F. Boehm. 2000. Characterization of Staphylococcus aureus beta-toxin induced leukotoxicity. J. Nat.Toxins 9: 125 138.
102. Mason, R. E.,, and W. E. Allen. 1975. Characteristics of Staphylococcus aureus associated with lysogenic conversion to loss of beta-hemolysin production. Can. J. Microbiol. 21: 1113 1116.
103. Mead, P. S.,, L. Slutsker,, V. Dietz,, L. F. Mc-Caig,, J. S. Bresee,, C. Shapiro,, P. M. Griffin,, and R. V. Tauxe. 15 September 1999, posting date. Food-related illness and death in the United States. Centers for Disease Control and Prevention, Atlanta, Ga. [Online.] http://www.cdc.gov.
104. Mehindate, K.,, J. Thibodeau,, M. Dohlsten,, T. Kalland,, R. P. Sekaly,, and W. Mourad. 1995. Cross-linking of major histocompatibility complex class II molecules by staphylococcal enterotoxin A superantigen is a requirement for inflammatory cytokine gene expression. J. Exp. Med. 182: 1573 1577.
105. Melish, M. E.,, and L. A. Glasgow. 1970. The staphylococcal scalded-skin syndrome. N. Engl. J. Med. 282: 1114 1119.
106. 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.
107. Mitchell, D. T.,, P. M. Schlievert,, D. H. Ohlendorf,, J.K. Kim,, D. C. Wiley,, R. G. Urban,, and J. L. Strominger,. 1997. Comparison of structures of toxic shock syndrome toxin-1 unbound and bound to a class II major histocompatibility molecule, p. 149 166. In D. Y. M. Leung,, B. T. Huber,, and P. M. Schlievert (ed.), Superantigens: Molecular Biology,Immunology, and Relevance to Human Disease. Marcel Dekker, New York, N.Y.
108. Mlynarczyk, A.,, G. Mlynarczyk,, D. Zabicka,, and A. Sawicka-Grzelak. 1993. Bacteriophages of serologic group A converting synthesis of staphylokinase and beta toxin in S. aureus. Med. Dosw. Mikrobiol. 45: 15 18.
109. Mlynarczyk, G.,, P. Garlinski,, A. Mlynarczyk,, K. Zabuska,, A. Sawicka-Grzelak,, G. Machowska,, H. Osowiecki,, and W. Roszkowski. 1989. Bacteriophage conversion as a factor modifying the intensity of phagocytosis of Staphylococcus aureus by human leukocytes. Med. Dosw. Mikrobiol. 41: 86 91.
110. Möllby, R., 1983. Isolation and properties of membrane damaging toxins, p. 619 662. In C. S. F. Eastmon, and C. Adlam (ed.), Staphylococci and Staphylococcal Infections, vol. 2. Academic Press, London, United Kingdom.
111. Monday, S. R.,, G. M. Vath,, W. A. Ferens,, C. Deobald,, J. V. Rago,, P. J. Gahr,, D. D. Monie,, J. J. Iandolo,, S.K. Chapes,, W. C. Davis,, D. H. Ohlendorf,, P. M. Schlievert,, and G. A. Bohach. 1999. Unique superantigen activity of staphylococcal exfoliative toxins. J. Immunol. 162: 4550 4559.
112. Musser, J. M.,, P. M. Schlievert,, A. W. Chow,, P. Ewan,, B. N. Kreiswirth,, V. T. Rosdahl,, A. S. Naidu,, W. Witte,, and R. K. Selander. 1990. A single clone of Staphylococcus aureus causes the majority of cases of toxic shock syndrome. Proc. Natl. Acad. Sci. USA 87: 225 229.
113. Narita, S.,, J. Kaneko,, J. Chiba,, Y. Piemont,, S. Jarraud,, J. Etienne,, and Y. Kamio. 2001. Phage conversion of Panton-Valentine leukocidin in Staphylococcus aureus: molecular analysis of a PVL-converting phage, phiSLT. Gene 268: 195 206.
114. Nariya, H.,, A. Shimatani,, T. Tomita,, and Y. Kamio. 1997. Identification of the essential amino acid residues in lukS for the hemolytic activity of staphylococcal leukocidin towards rabbit erythrocytes. Biosci. Biotechnol. Biochem. 61: 2095 2099.
115. Novick, R. P. 1967. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33: 155 166.
116. Novick, R. P.,, I. Edelman,, and S. Lofdahl. 1986. Small Staphylococcus aureus plasmids are transduced as linear multimers that are formed and resolved by replicative processes. J. Mol. Biol. 192: 209 220.
117. Novick, R. P.,, P. Schlievert,, and A. Ruzin. 2001. Pathogenicity and resistance islands of staphylococci. Microbes Infect. 3: 585 594.
118. O’Leary, W. M.,, and J.T. Weld. 1964. Lipolytic activities of Staphylococcus aureus. I. Nature of the enzyme producing free fatty acids from plasma lipids. J. Bacteriol. 88: 1356 1363.
119. Pantucek, R.,, A. Rosypalova,, J. Doskar,, J. Kailerova,, V. Ruzickova,, P. Borecka,, S. Snopkova,, R. Horvath,, F. Gotz,, and S. Rosypal. 1998. The polyvalent staphylococcal phage phi 812: its host-range mutants and related phages. Virology 246: 241 252.
120. Prevost, G.,, B. Cribier,, P. Couppie,, P. Petiau,, G. Supersac,, V. Finck-Barbancon,, H. Monteil,, and Y. Piemont. 1995. Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological activities. Infect. Immun. 63: 4121 4129.
121. Prevost, G.,, G. Menestrina,, D. A. Colin,, S. Werner,, S. Bronner,, M. Dalla Sera,, L. Baba Moussa,, M. Coraiola,, A. Gravet,, and H. Monteil,. 2003. Staphylococcal biocomponent leucotoxins, mechanisms of action, impact on cells and contribution to virulence, p. 3 26. In G. Menestrina,, M. Dalla Sera,, and P. Lazarovici (ed.), Pore-Forming Peptides and Proteins. Taylor & Francis Group, London, United Kingdom.
122. Proft, T.,, and J. D. Fraser. 2003. Bacterial superantigens. Clin. Exp. Immunol. 133: 299 306.
123. Qasim, W. 1998. Superantigen scalded skin syndromes. Arch. Dis. Child 79: 290.
124. Rago, J.V.,, G. M. Vath,, G. A. Bohach,, D. H. Ohlendorf,, and P. M. Schlievert. 2000. Mutational analysis of the superantigen staphylococcal exfoliative toxin A (ETA). J. Immunol. 164: 2207 2213.
125. Recsei, P.,, B. Kreiswirth,, M. O’Reilly,, P. Schlievert,, A. Gruss,, and R. P. Novick. 1986. Regulation of exoprotein gene expression in Staphylococcus aureus by agar. Mol. Gen. Genet. 202: 58 61.
126. 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.
127. Rollof, J.,, J. H. Braconier,, C. Soderstrom,, and P. Nilsson-Ehle. 1988. Interference of Staphylococcus aureus lipase with human granulocyte function. Eur. J. Clin. Microbiol. Infect. Dis. 7: 505 510.
128. Rosendal, K.,, P. Bulow,, and O. Jessen. 1964. Lysogenic conversion in Staphylococcus aureus to a change in the production of extracellular “Tween”-splitting enzyme. Nature 204: 1222.
129. Rosenstein, R.,, and F. Götz. 2000. Staphylococcal lipases: biochemical and molecular characterization. Biochimie 82: 1005 1014.
130. Rountree, P. M. 1947. Some observations on fibrinolysin and beta toxin of staphylococci. Aust. J. Exp. Biol. Med. Sci. 25.
131. Russell, R. J.,, P.C. Wilkinson,, R. J. McInroy,, S. McKay,, A. C. McCartney,, and J. P. Arbuthnott. 1976. Effects of staphylococcal products on locomotion and chemotaxis of human blood neutrophils and monocytes. J. Med. Microbiol. 9: 433 439.
132. Ruzin, A.,, J. Lindsay,, and R. P. Novick. 2001. Molecular genetics of SaPI1—a mobile pathogenicity island in Staphylococcus aureus. Mol. Microbiol. 41: 365 377.
133. Sako, T.,, and N. Tsuchida. 1983. Nucleotide sequence of the staphylokinase gene from Staphylococcus aureus. Nucleic Acids Res. 11: 7679 7693.
134. Sawicka-Grzelak, A.,, A. Szymanowska,, A. Mlynarczyk,, and G. Mlynarczyk. 1993. Production of staphylokinase and hemolysin by coagulase-negative staphylococcus. Med.Dosw. Mikrobiol. 45: 7 10.
135. Schiffenbauer, J.,, H. Johnson,, and J. Soos,. 1997. Superantigens in autoimmunity: their role as etiologic and therapeutic agents, p. 525 549. In D. Y. M. Leung,, B.T. Huber,, and P. M. Schlievert (ed.), Superantigens: Molecular Biology, Immunology, and Relevance to Human Disease. Marcel Dekker, New York, N.Y.
136. Schlievert, P. M.,, K. N. Shands,, B. B. Dan,, G. P. Schmid,, and R. D. Nishimura. 1981. Identification and characterization of an exotoxin from Staphylococcus aureus associated with toxicshock syndrome. J. Infect. Dis. 143: 509 516.
137. Shupp, J. W.,, M. Jett,, and C. H. Pontzer. 2002. Identification of a transcytosis epitope on staphylococcal enterotoxins. Infect. Immun. 70: 2178 2186.
138. Siqueira, J. A.,, C. Speeg-Schatz,, F. I. Freitas,, J. Sahel,, H. Monteil,, and G. Prevost. 1997. Channel-forming leucotoxins from Staphylococcus aureus cause severe inflammatory reactions in a rabbit eye model. J. Med. Microbiol. 46: 486 494.
139. Sjostrom, J. E.,, M. Lindberg,, and L. Philipson. 1973. Competence for transfection in Staphylococcus aureus. J. Bacteriol. 113: 576 585.
140. Slanetz, L.W.,, and C. H. Bartley. 1953. The diagnosis of mastitis, with special reference to the characteristics of mastitis staphylococci. J. Infect. Dis. 92: 139 151.
141. Smith, P. B., 1972. Bacteriophage typing of Staphylococcus aureus, p. 431 441. In J. O. Cohen (ed.), The Staphylococci. Wiley-Interscience, New York,N.Y.
142. Soltis, M.T.,, J. J. Mekalanos,, and M. J. Betley. 1990. Identification of a bacteriophage containing a silent staphylococcal variant enterotoxin gene ( sezA +). Infect. Immun. 58: 1614 1619.
143. Stewart, P. R.,, H. G. Waldron,, J. S. Lee,, and P. R. Matthews. 1985. Molecular relationships among serogroup B bacteriophages of Staphylococcus aureus. J.Virol. 55: 111 116.
144. Sumby, P.,, and M. K. Waldor. 2003. Transcription of the toxin genes present within the staphylococcal phage phiSa3ms is intimately linked with the phage’s life cycle. J. Bacteriol. 185: 6841 6851.
145. Svensson, L.A.,, E.M. Schad,, M. Sundstrom,, P. Antonsson,, T. Kalland,, and M. Dohlsten,. 1997. Staphylococcal enterotoxins A,D, and E, p. 199 299. In D.Y.M. Leung,, B.T. Huber,, and P.M. Schlievert (ed.), Superantigens: Molecular Biology, Immunology, and Relevance to Human Disease. Marcel Dekker, New York, N.Y.
146. Szmigielski, S.,, J. Jeljaszewicz,, M. Kobus,, M. Luczak,, A. Ludwicka,, R. Mollby,, and T. Wadstrom. 1976. Cytotoxic effects of staphylococcal alpha- beta- and gamma-hemolysins. Zentbl. Bakteriol. 5(Suppl.): 691 705.
147. Thelestam, M., 1983. Modes of membrane damaging action of staphylococcal toxins, p. 705 744. In C. S. F. Eastmon, and C. Adlam (ed.), Staphylococci and Staphylococcal Infections, vol. 2. Academic Press, London, United Kingdom.
148. Thelestam, M.,, R. Mollby,, and T. Wadstrom. 1973. Effects of staphylococcal alpha-, beta-, delta-, and gamma-hemolysins on human diploid fibroblasts and HeLa cells: evaluation of a new quantitative assay for measuring cell damage. Infect. Immun. 8: 938 946.
149. Tomita, T.,, and Y. Kamio. 1997. Molecular biology of the pore-forming cytolysins from Staphylococcus aureus, alpha- and gamma-hemolysins and leukocidin. Biosci. Biotechnol. Biochem. 61: 565 572.
150. Tremaine, M.T.,, D. K. Brockman,, and M. J. Betley. 1993. Staphylococcal enterotoxin A gene ( sea) expression is not affected by the accessory gene regulator ( agr). Infect. Immun. 61: 356 359.
151. Ubeda, C.,, M. A. Tormo,, C. Cucarella,, P. Trotonda,, T. J. Foster,, I. Lasa,, and J. R. Penades. 2003. Sip, an integrase protein with excision, circularization and integration activities, defines a new family of mobile Staphylococcus aureus pathogenicity islands. Mol. Microbiol. 49: 193 210.
152. Van den Bussche, R. A.,, J. D. Lyon,, and G.A. Bohach. 1993. Molecular evolution of the staphylococcal and streptococcal pyrogenic toxin gene family. Mol. Phylogenet. Evol. 2: 281 292.
153. van der Vijver, J. C.,, M. van Es-Boon,, and M. F. Michel. 1972. Lysogenic conversion in Staphylococcus aureus to leucocidin production. J.Virol. 10: 318 319.
154. Vybiral, D.,, M. Takac,, M. Loessner,, A. Witte,, U. von Ahsen,, and U. Blasi. 2003. Complete nucleotide sequence and molecular characterization of two lytic Staphylococcus aureus phages: 44AHJD and P68. FEMS Microbiol. Lett. 219: 275 283.
155. Wadström, T., 1983. Biological effects of cell damaging toxins. In C. S. F. Eastmon, and C. Adlam (ed.), Staphylococci and Staphylococcal Infections, vol. 2. Academic Press, London, United Kingdom.
156. Wadstrom, T.,, and R. Mollby. 1972. Studies on extracellular proteins of Staphylococcus aureus.VII. Studies on beta-hemolysin. Biochim. Biophys. Acta 242: 308 420.
157. Weeks, C. R.,, and J. J. Ferretti. 1984. The gene for type A streptococcal exotoxin (erythrogenic toxin) is located in bacteriophage T12. Infect. Immun. 46: 531 536.
158. Weld, J.T.,, B. H. Kean,, and W. M. O’Leary. 1963. Production of octadecenoic acid in plasma by Staphylococcus aureus. Proc. Soc. Exp. Biol. Med. 112: 448.
159. Wilkinson, P. C. 1975. Inhibition of leukocyte locomotion and chemotaxis by lipid-specific bacterial toxins. Nature 255: 485 487.
160. Willis, A.T.,, S. I. Jacobs,, and G. M. Goodburn. 1963. Observations on multiple-antibiotic-resistant epidemic strains of Staphylococcus aureus. Lancet ii: 67.
161. Winkler, K. C.,, J. de Waart,, and C. Grootsen. 1965. Lysogenic conversion of staphylococci to loss of beta-toxin. J. Gen. Microbiol. 39: 321 333.
162. 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.
163. Ye, Z. H.,, and C. Y. Lee. 1989. Nucleotide sequence and genetic characterization of staphylococcal bacteriophage L54a int and xis genes. J. Bacteriol. 171: 4146 4153.
164. Yoshizawa, Y.,, J. Sakurada,, S. Sakurai,, K. Machida,, I. Kondo,, and S. Masuda. 2000. An exfoliative toxin A-converting phage isolated from Staphylococcus aureus strain ZM. Microbiol. Immunol. 44: 189 191.
165. Zabicka, D.,, A. Mlynarczyk,, B. Windyga,, and G. Mlynarczyk. 1993. Phage-related conversion of enterotoxin A, staphylokinase and betatoxin in Staphylococcus aureus. Acta Microbiol. Pol. 42: 235 241.
166. Zabriskie, J. B. 1964. The role of temperate bacteriophage in the production of erythrogenic toxin by group A streptococci. J. Exp. Med. 119: 761 780.
167. Zabriskie, J. B. 1966. Viral induced bacterial toxins. Annu. Rev. Med. 17: 337 350.
168. Zavizion, B.,, J.H. White,, and A. J. Bramley. 1997. Staphylococcus aureus stimulates urokinase-type plasminogen activator expression by bovine mammary cells. J. Infect. Dis. 176: 1637 1640.
169. Zou, D.,, J. Kaneko,, S. Narita,, and Y. Kamio. 2000. Prophage, phiPV83-pro, carrying Panton-Valentine leucocidin genes, on the Staphylococcus aureus P83 chromosome: comparative analysis of the genome structures of phiPV83-pro, phiPVL, phi11, and other phages. Biosci. Biotechnol. Biochem. 64: 2631 2643.


Generic image for table

Indirect evidence of recombination and modularity in staphylococcal phages

Negative conversion of beta-hemolysin is caused by integration of the prophage into . The specificity of the phage integrase determines the site of insertion. The serotype is determined by the phage particle proteins.

Citation: Matthews A, Novick R. 2005. Staphylococcal Phages, p 297-318. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch15
Generic image for table

Medically important bacteriophages of the staphylococci

Citation: Matthews A, Novick R. 2005. Staphylococcal Phages, p 297-318. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch15

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