Bacterial two-component and hetero-heptameric pore-forming cytolytic toxins: Structures, pore-forming mechanism, and organization of the genes

Bioscience, Biotechnology and Biochemistry

Volumn 68, Issue 5, 2004, Pages 981-1003

  Kaneko, Jun ^a   Kamio, Yoshiyuki ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Assembly mechanism; Phage conversion; Single molecular imaging; Staphylococcal two component pore forming cytolysins; Structure

Indexed keywords

BACTERIAL TOXIN; CYTOTOXIN; EXOTOXIN; HEMOLYSIN; LEUKOCIDIN; OUTER MEMBRANE PROTEIN; PANTON VALENTINE LEUKOCIDIN; PANTON-VALENTINE LEUKOCIDIN;

ADULT; AMINO ACID SEQUENCE; BACTERIOPHAGE; CELL MEMBRANE; CHEMISTRY; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; GENE ORDER; GENETICS; HEMOLYSIS; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; REVIEW; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS AUREUS;

ADULT; AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL TOXINS; BACTERIOPHAGES; CELL MEMBRANE; CYTOTOXINS; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; EXOTOXINS; GENE ORDER; HEMOLYSIN PROTEINS; HEMOLYSIS; HUMANS; LEUKOCIDINS; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); MAMMALIA; ORYCTOLAGUS CUNICULUS; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; UNIDENTIFIED BACTERIOPHAGE;

EID: 4544341370     PISSN: 09168451     EISSN: None     Source Type: Journal    
DOI: 10.1271/bbb.68.981     Document Type: Review

References (95)

1. Tomita, T., and Kamio, Y., Molecular biology of the pore-forming cytolysin from Staphylococcus aureus, α-and γ-hemolysins and leukocidin. Biosci. Biotechnol. Biochem., 61, 565-572 (1997).
2. Cooney, J., Kienle, Z., Foster, T. J., and O'Toole, P. W., The gamma-hemolysin locus of Staphylococcus aureus comprises three linked genes, two of which are identical to the genes for the F and S components of leukocidin. Infect. Immun., 61, 768-771 (1993).
3. Supersac, G., Prévost, G., and Piémont, Y., Sequencing of leucocidin R from Staphylococcus aureus P83 suggests that staphylococcal leucocidins and gamma-hemolysin are members of a single, two-component family of toxins. Infect. Immun., 61, 580-587 (1993).
4. Kamio, Y., Rahman, A., Nariya, H., Ozawa, T., and Izaki, K., The two Staphylococcal bi-component toxins, leukocidin and gamma-hemolysin, share one component in common. FEBS Lett., 321, 15-18 (1993).
5. Rahman, A., Izaki, K., and Kamio, Y., Gamma-hemolysin genes in the same family with lukF and lukS genes in methicillin resistant Staphylococcus aureus. Biosci. Biotechnol. Biochem., 57, 1234-1236 (1993).
6. Kamio, Y., Tomita, T., and Kaneko, J., Pore-forming cytolysin from Staphylococcus aureus, α- and γ-hemolysin, and leukocidin. In "Staphylococcal Infection and Immunity", ed. Friedman, I., Kluwer Academic/Plenum Publishers, New York, pp. 179-212 (2001).
7. Gouaux, E., Hobaugh, M. R., and Song, L., α-Hemolysin, γ-Hemolysin, and leukocidin from Staphylococcus aureus: Distant in sequence but similar in structure. Protein Science, 6, 2631-2635 (1997).
8. Gouaux, E., α-Hemolysin from Staphylococcus aureus: an archetype of beta-barrel, channel-forming toxins. J. Struct. Biol., 121, 110-122 (1998).
9. Olson, R., Nariya, H., Yokota, K., Kamio, Y., and Gouaux, E., Crystal structure of staphylococcal LukF delineates conformational changes accompanying formation of a transmembrane channel. Nature Struct. Biol., 6, 134-140 (1999).
10. Pedelacq, J.-D., Maveyraud, L., Prevost, G., Baba-Moussa, L., Gonzalez, A., Courcell, E., Shepard, W., Monteil, H., Samama, J. P., and Mourey, L., The structure of a Staphylococcus aureus leucocidin component (LukF-PV) reveals the fold of the water-soluble species of a family of transmembrane pore-forming toxins. Structure, 7, 277-287 (1999).
11. Nariya, H., Nishiyama, A., and Kamio, Y., Identification of the minimum segment in which the threonine246 residue is a potential phosphorylated site by protein kinase A for the LukS-specific function of staphylococcal leukocidin. FEBS Lett., 415, 96-100 (1997).
12. Nishiyama, A., Nariya, H., and Kamio, Y., Phosphorylation of LukS by protein kinase A is crucial for the LukS-specific function of staphylococcal leukocidin on human polymorphonuclear leukocytes. Biosci. Biotechnol. Biochem., 62, 1824-1838 (1998).
13. Alberts, B., Alexander, J., Lewis, J., Raff, M., Roberts, K., and Walter, P., Protein, Cytoskeleton. In "Molecular Biology of the Cell" 4th ed., Garland Science, New York, pp. 147-162, 907-915 (2002).
14. Funatsu, T., Harada, Y., Tokunaga, M., Saito, K., and Yanagida, T., Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature, 374, 555-559 (1995).
15. Ishijima, A., Kojima, H., Funatsu, T., Tokunaga, M., Higuchi, H., Tanaka, H., and Yanagida, T., Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin. Cell, 23, 161-171 (1998).
16. Schütz, G. T., Kada, G., Pastushenko, V. P., and Schindler, H., Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy. EMBO J., 19, 892-901 (2000).
17. Mendelsohn, A. R., and Brent, R., Protein interaction methods: toward an endgame. Science, 284, 1948-1950 (1999).
18. Taguchi, H., Ueno, T., Tadakuma, H., Yoshida, M., and Funatsu, T., Single-molecule observation of protein-protein interactions in the chaperonin system. Nature Biotechnol., 19, 861-865 (2001).
19. Ha, T., Enderle, T., Ogletree, D. F., Chemla, D. S., Selvin, P. R., and Weiss, S., Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl. Acad. Sci. USA, 93, 6264-6268 (1996).
20. Ha, T., Single-molecule fluorescence methods for the study of nucleic acids. Curr. Opin. Struct. Biol., 11, 287-292 (2001).
21. Sako, Y., Minoguchi, S., and Yanagida, T., Single-molecule imaging of EGFR signalling on the surface of living cells. Nature Cell Biol., 2, 168-172 (2000).
22. Van der Goot, G., "Pore-forming Toxins", Springer-Verlag, Berlin, Heidelberg (2001).
23. Nguyen, V. T., Kamio, Y., and Higuchi, H., Single-molecule imaging of cooperative assembly of γ-hemolysin on erythrocyte membranes. EMBO J., 22, 4968-4979 (2003).
24. Prévost, G., Couppié, P., Prévost, P., Gayet, S., Petiau, P., Cribier, B., Monteil, H., and Piémont, Y., Epidemiological data on Staphylococcus aureus strains producing synergohymentropic toxins. J. Med. Microbiol., 42, 237-245 (1995).
25. Kaneko, J., Kimura, T., Kawakami, Y., Tomita, T., and Kamio, Y., Panton-Valentine leukocidin genes in phage-like particle isolated from mitomycin C-treated Staphylococcus aureus V8 (ATCC 49775). Biosci. Biotechnol. Biochem., 61, 1960-1962 (1997).
26. Kaneko, J., Kimura, T., Narita, S., Tomita, T., and Kamio, Y., Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage φPVL carrying Panton-Valentine leukocidin genes. Gene, 215, 57-67 (1998).
27. Narita, S., Kaneko, J., Chiba, J., Piémont, Y., Jarraud, S., Etienne, J., and Kamio, Y., Phage conversion of Panton-Valentine leukocidin (PVL) in Staphylococcus aureus: molecular analysis of a PVL-converting phage, φSLT. Gene, 268, 195-206 (2001).
28. Sugawara, N., Tomita, T., and Kamio, Y., Assembly of Staphylococcus aureus γ-hemolysin into a pore-forming ring-shaped complex on the surface of human erythrocytes. FEBS Lett., 410, 333-337 (1997).
29. Ozawa, T., Kaneko, J., and Kamio, Y., Essential binding of LukF of staphylococcal γ-hemolysin followed by the binding of HlgII for the hemolysis of human erythrocytes. Biosci. Biotechnol. Biochem., 59, 1181-1183 (1995).
30. Kaneko, J., Ozawa, T., Tomita, T., and Kamio, Y., Sequential binding of Staphylococcal γ-hemolysin to human erythrocytes and complex formation of the hemolysin on the cell surface. Biosci. Biotechnol. Biochem., 61, 846-851 (1997).
31. Sugawara, N., Tomita, T., Sato, T., and Kamio, Y., Assembly of Staphylococcus aureus leukocidin into a pore-forming ring-shaped oligomer on human polymorphonuclear leukocytes and rabbit erythrocytes. Biosci. Biotechnol. Biochem., 63, 884-891 (1999).
32. Finck-Barbançon, V., Duportail, G., Meunier, O., and Colin, D. A., Pore formation by a two-component leukocidin from Staphylococcus aureus within the membrane of human polymorphonuclear leukocytes. Biochim. Biophys. Acta, 1182, 275-282 (1993).
33. 2+ channels in the membrane of human polymorphonuclear neutrophils. J. Membr. Biol., 162, 209-216 (1998).
34. Sugawara-Tomita, N., Tomita, T., and Kamio, Y., Stochastic assembly of two-component staphylococcal γ-hemolysin into heteroheptameric transmembrane pores with alternate subunit arrangements in ratios of 3:4 and 4:3. J. Bacteriol., 184, 4747-4756 (2002).
35. Ferreras, M., Frank, H., Serra, M. D., Colin, D. A., Prevost, G., and Menestrina, G., The interaction of Staphylococcus aureus bi-component γ-hemolysins and leucocidins with cells and lipid membranes. Biochim. Biophys. Acta, 1414, 108-126 (1998).
36. Miles, G., Movileanu, L., and Bayley, H., Subunit composition of a bi-component toxin: Staphylococcal leukocidin forms an octameric transmembrane pore. Protein Science, 11, 894-902 (2002).
37. Nguyen, T. V., Higuchi, H., and Kamio, Y., Controlling pore assembly of Staphylococcal γ-hemolysin by low temperature and by disulfide bond formation in double-cysteine LukF mutants. Mol. Microbiol., 45, 1485-1498 (2002).
38. Walker, B., Krishnasastry, M., Zorn, L., and Bayley, H., Assembly of the oligomeric membrane pore formed by Staphylococcal alpha-hemolysin examined by truncation mutagenesis. J. Biol. Chem., 267, 21782-21786 (1992).
39. Valeva, A., Palmer, M., Hilgert, K., Kehoe, M., and Bhakdi, S., Correct oligomerization is a prerequisite for insertion of the central molecular domain of Staphylococcal alpha-toxin into the lipid bilayer. Biochim. Biophys. Acta, 1236, 213-218 (1995).
40. Valeva, A., Palmer, M., and Bhakdi, S., Staphylococcal alpha-toxin: formation of the heptameric pore is partially cooperative and proceeds through multiple intermediate stages. Biochemistry, 36, 13298-13304 (1997).
41. Cheley, S., Malghani, M. S., Song, L., Hobaugh, M., Gouaux, E., Young, J., and Bayley, H., Spontaneous oligomerization of a staphylococcal alpha-hemolysin conformationally constrained by removal of residues that form the transmembrane beta-barrel. Protein Eng., 10, 1433-1443 (1997).
42. Walker, B., Braha, O., Cheley, S., and Bayley, H., An intermediate in the assembly of a pore-forming protein trapped with a genetically-engineered switch. Chem. Biol., 2, 99-105 (1995).
43. Song, L., Hobaugh, M. R., Shustak, C., Cheyley, A., Bayley, H., and Gouaux, E., Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science, 274, 1859-1866 (1996).
44. Miles, G., Cheley, S., Braha, O., and Bayley, H., The staphylococcal leukocidin bi-component toxin forms large ionic channels. Biochemistry, 40, 8514-8522 (2001).
45. Kaneko, J., Mascarenas, A. L., Huda, M. N., Tomita, T., and Kamio, Y., An N-terminal region of LukF of staphylococcal leukocidin/γ-hemolysin crucial for the biological activity of toxin. Biosci. Biotechnol. Biochem., 62, 1465-1467 (1998).
46. Rossjohn, J., Raja, S. M., Nelson, K. L., Feil, S. C., van der Goot, F. G., Parker, M. W., and Buckley, J. T., Movement of a loop in domain 3 of aerolysin is required for channel formation. Biochemistry, 37, 741-746 (1998).
47. Hotze, E. M., Wilson-Kubalek, E. M., Rossjohn, J., Parker, M. W., Johnson, A. E., and Tweten, R. K., Arresting pore formation of a cholesterol-dependent cytolysin by disulfide trapping synchronizes the insertion of the transmembrane beta-sheet from a prepore intermediate. J. Biol. Chem., 276, 8261-8268 (2001).
48. Kawate, T., and Gouaux, E., Arresting and releasing Staphylococcal α-hemolysin at intermediate stages of pore formation by engineered disulfide bonds. Protein Sci., 12, 997-1006 (2003).
49. Yokota, K., and Kamio, Y., Tyrosine72 residue at the bottom of rim domain in LukF crucial for the sequential binding of the staphylococcal γ-hemolysin to human erythrocytes. Biosci. Biotechnol. Blochem., 64, 2744-2747 (2000).
50. Monma, N., Nguyen, V. T., Yokota, K., Kaneko, J., Higuchi, H., and Kamio, Y., To be published elsewhere (2004).
51. Nariya, H., Izaki, K., and Kamio, Y., The C-terminal region of the S component of staphylococcal leukocidin is essential for the biological activity of the toxin. FEBS Lett., 329, 219-222 (1993).
52. Noda, M., Kato, I., Hirayama, T., and Matsuda, F., Mode of action of staphylococcal leukocidin: effects of the S and F components on the activities of membrane-associated enzymes of rabbit polymorphonuclear leukocytes. Infect. Immun., 35, 38-45 (1982).
53. 2+-activation from the pore-forming function of the bi-component Panton-Valentine leucocidin in human PMNs. FEBS Lett., 461, 280-286 (1999).
54. Prévost, G., Bouakham, T., Piémont, Y., and Momteil, H., Characterization of a synergohymentropic toxin produced by Staphylococcus intermedius. FEBS lett., 376, 135-140 (1995).
55. Nishiyama, A., Guerra, M. A., Sugawara, N., Yokota, K., Kaneko, J., and Kamio, Y., Identification of serine 138 residue in the 4-residue segment K135K1361137S138 of LukS-I component of Staphylococcus intermedius leukocidin crucial for the LukS-I-specific function of staphylococcal leukocidin. Biosci. Biotechnol. Biochem., 66, 328-335 (2002).
56. Daughterly, M. A., Brenowitz, M., and Fried, M. G., The TATA-binding protein from Saccharomyces cerevisiae oligomerizes in solution at micromolar concentrations to form tetramers and octamers. J. Mol. Biol., 285, 1389-1399 (1999).
57. Comai, M., Dalla-Serra, M., Coraiola, M., Werner, S., Colin, D. A., Monteil, H., Prévost, G., and Menestrina, G., Protein engineering modulates the transport properties and ion selectivity of the pores formed by staphylococcal gamma-haemolysins in lipid membranes. Mol. Microbiol., 44, 1251-1267 (2002).
58. Wallace, A. J., Stillman, T. J., Atkinsm, A., Jamieson, S. J., Bullough, P. A., Green, J., and Artymiuk, P. J., E. coli hemolysin E (HIyE, ClyA, SheA): X-ray crystal structure of the toxin and observation of membrane pores by electron microscopy. Cell, 100, 265-276 (2000).
59. Oosawa, F., and Kasai, M., A theory of linear and helical aggregations of macromolecules. J. Mol. Biol., 4, 10-21 (1962).
60. Rahman, A., Izaki, K., Kato, I., and Kamio, Y., Nucleotide sequence of leukocidin S-component gene (lukS) from methicillin resistant Staphylococcus aureus. Biochem. Biophys. Res. Commun., 181, 138-144 (1991).
61. Rahman, A., Nariya, H., Izaki, K., Kato, I., and Kamio, Y., Molecular cloning and nucleotide sequence of leukocidin F-component gene (lukF) from methicillin resistant Staphylococcus aureus. Biochem. Biophys. Res. Commun., 184, 640-646 (1992).
62. Kuroda, M., Ohta, T., Uchiyama, I., Baba, T., Yuzawa, H., Kobayashi, I., Cui, L., Oguchi, A., Aoki, K., Nagai, Y., Lian, J., Ito, T., Kanamori, M., Matsumaru, H., Maruyama, A., Murakami, H., Hosoyama, A., Mizutani-Ui, Y., Takahashi, N. K., Sawano, T., Inoue, R., Kaito, C., Sekimizu, K., Hirakawa, H., Kuhara, S., Goto, S., Yabuzaki, J., Kanehisa, M., Yamashita, A., Oshima, K., Furuya, K., Yoshino, C., Shiba, T., Hattori, M., Ogasawara, N., Hayashi, H., and Hiramatsu, K., Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet, 357, 1225-1240 (2001).
63. N315 website; http://www.bio.nite.go.jp:8080/dogan/MicroTop?GENOME_ID= n315G1
64. Mu50 website; http://w3.grt.kyushu-u.ac.jp/VRSA/
65. Baba, T., Takeuchi, F., Kuroda, M., Yuzawa, H., Aoki, K., Oguchi, A., Nagai, Y., Iwama, N., Asano, K., Naimi, T., Kuroda, H., Cui, L., Yamamoto, K., and Hiramatsu, K., Genome and virulence determinants of high virulence community-acquired MRSA. Lancet, 359, 1819-1827 (2002).
66. 2MW website; http://www.bio.nite.go.jp:8080/dogan/MicroTop?GENOME_ID=mw2
67. 8325 website; http://www.genome.ou.edu/staph.html
68. COL website; http://www.tigr.org/tigr-scripts/CMR2/GenomePage3.spl? database=gsa
69. Prévost, G., Cribier, B., Couppié, P., Petiau, P., Supersac, G., Finck-Barbançon, V., Monteil, H., and Piémont, Y., Panton-Valentine leucocidin and gamma-hemolysin from Staphylococcus aureus ATCC 49775 are encoded by distinct genetic loci and have different biological aclivities. Infect. Immun., 63, 4121-4129 (1995).
70. Lina, G., Piémont, Y., Godail-Gamot, F., Bes, M., Peter, M.-O., Gauduchon, V., Vandenesch, F., and Etienne, J., Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin. Infect. Dis., 29, 1128-1132 (1999).
71. Choorit, W., Kaneko, J., Muramoto, K., and Kamio, Y., Existence of a new protein component with the same function as the LukF component of leukocidin or g-hemolysin and its gene in Staphylococcus aureus. FEBS lett., 357, 260-264 (1995).
72. Kaneko, J., Muramoto, K., and Kamio, Y., Gene of the LukF-PV-like component of Panton-Valentine leukocidin in Staphylococcus aureus P83 is linked with lukM. Biosci. Biotechnol. Biochem., 61, 541-544 (1997).
73. Zou, D., Kaneko, J., Narita, S., and Kamio, Y., Prophage, φPV83-pro, carrying Panton-Valentine leukocidin genes, on the Staphylococcus aureus P83 chromosome: comparative analysis of the genome structures of φPV83-pro, φPVL, φ11, and other phages. Biosci. Biotechnol. Biochem., 64, 2631-2643 (2000).
74. Rainard, P., Corrailes, J.-C., Barrio, M. B., Cochard, T., and Pautrel, B., Leucotoxic activities of Staphylococcus aureus strain isolated from cows, ewes, and goats with mastitis: importance of LukM/LukF′-PV leukocidin. Clin. Diagn. Lab. Immunol., 10, 272-277 (2003).
75. Gravet, A., Colin, D. A., Keller, D., Giradot, R., Monteil, H., and Prévost, G., Characterization of a novel structural member, LukE-LukD, of the bi-component staphylococcal leucotoxins family. FEBS lett., 436, 202-207 (1998).
76. Morinaga, N., Kaihou, Y., and Noda, M., Purification, cloning and characterization of variant LukE-LukD with strong leukocidal activity of staphylococcal bi-component leucocidin family. Microbial. Immunol., 47, 81-90 (2003).
77. Van der Vijver, J. C. M., van Es-Boon, M., and Michel, M. F., Lysogenic conversion in Staphylococcus aureus to leucocidin production. J. Virol., 10, 318-319 (1972).
78. Lee, C. Y., and Iandoro, J. J., Structural analysis of Staphylococcal bacteriophage φ11 attachment sites. J. Bacteriol., 170, 2409-2411 (1988).
79. Duda, R. L., Martincic, K., Xie, Z., and Hendrix, R. W., Bacteriophage HK97 head assembly. FEMS Microbiol. Rev., 18, 41-46 (1995).
80. Desiere, F., Lucchini, S., and Brüssow, H., Comparative sequence analysis of the DNA packaging, head, and tail morphogenesis modules in the temperate cos-site Streptococcus thermophilus bacteriophage Sfi21. Virology, 260, 244-253 (1999).
81. Narita, S., Kaneko, J., and Kamio, Y., The staphylococcal infection by a PVL-converting phage, φSLT starts with molecular interaction between lipoteichoic acid and the structural protein ORF636 of the phage. To be published elsewhere (2004).
82. Pattee, P. A., Tompson, N. E., Haubrich, B., and Novick, R. P., Chromosomal map locations of integrated plasmids and related elements in Staphylococcus aureus. Plasmid, 1, 38-51 (1977).
83. Novick, R. P., Mobile genetic element and bacterial toxins: the super antigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid, 49, 93-105 (2003).
84. Novick, R. P., The Staphylococcus as a molecular genetic system. In "Molecular Biology of the Staphylococci", VCH Publisers, NY, pp. 1-37 (1990).
85. Doškař, J., Pallová, P., Pantůček, R., Rosypal, S., Růžičková, V., Pantůč ková, P., Kailerová, J., Klepárnik, K., Malá, Z., and Boćek, P., Genomic relatedness of Staphylococcus aureus phages of the International Typing Set and detection of serotype A, B, F prophages in lysogenic strains. Can. J. Microbiol., 46, 1066-1076 (2000).
86. Canchana, C., Proux, C., Fournous, C., Bruttin, A., and Brüssow, H., Prophage genomics. Microbiol. Mol. Biol. Rev., 67, 238-276 (2003).
87. Colmon, D., Knight, J., Russell, R., Shanley, D., Birkbeck, T. H., Dougan, G., and Charles, I., Insertional inactivation of the Staphylococcus aureus β-toxin by bacteriophage φ13 occurs by site- and orientation-specific integration of the φ13 genome. Mol. Microbiol., 5, 933-939 (1991).
88. Carroll, D., Kehoe, M. A., Cavanagh, D., and Coleman, D. C., Novel organization of site-specific integration and excision recombination function of the Staphylococcus aureus serotype F virulence converting phages φ13 and φ42. Molecular Microbiol., 16, 877-893 (1995).
89. Iandolo, J. J., Worrell, V., Groicher, K. H., Qian, Y., Tian, R., Kenton, S., Dorman, A., Ji, H., Lin, S., Loh, P., Qi, S., Zhu, H., and Roe, B. A., Comparative analysis of the genomes of the temperate bacteriophages phi 11, phi 12 and phi 13 of Staphylococcus aureus 8325. Gene, 289, 109-118 (2002).
90. Bachi, B., Physical mapping of the BglI, BglII, PstI and EcoRI restriction fragments of staphylococcal phage φ11 DNA. Mol. Gen. Genet., 180, 391-398 (1980).
91. Yamaguchi, T., Hayashi, T., Takami, H., Ohnishi, M., Murata, T., Nakayama, K., Asakawa, K., Ohara, M., Komatsuzawa, H., and Sugai, M., Complete nucleotide sequence of a Staphylococcus aureus exfoliative toxin B plasmid and identification of a novel ADP-ribosyl transferase, EDIN-B. Infect. Immun., 69, 7760-7771 (2001).
92. Botstein, D., A theory of modular evolution for bacteriophages. Ann. N.Y. Acad. Sci., 354, 484-491 (1980).
93. Lee, C. Y., and Iandolo, J. J., Integration of staphylococcal phage L54a occurs by site-specific recombination: Structural analysis of the attachment sites. Proc. Natl. Acad. Sci. USA, 83, 5474-5478 (1986).
94. Chiba, J., personal communication.
95. Sumby, P., and Waldor, M. K., Transcription of the toxin genes present within the staphylococcal phage φSa3ms is intimately linked with the phage's life cycle. J. Bacteriol., 185, 6841-6851 (2003).