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Original Articles

Bacterial Two-component and Hetero-heptameric Pore-forming Cytolytic Toxins: Structures, Pore-forming Mechanism, and Organization of the Genes

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Pages 981-1003 | Published online: 22 May 2014

  • 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) Staali, L., Monteil, H., and Colin, D. A., The staphylococcal pore-forming leukotoxins open Ca2+ 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. Biochem., 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) Baba-Moussa, L., Werner, S., Colin, D. A., Mourey, L., Pedelacq, J. D., Samama, J. P., Sanni, A., Monteil, H., and Prévost, G., Discoupling the Ca2+-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 serine138 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) Daugherty, 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 (HlyE, 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 activities. 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) Doškar, J., Pallová, P., Pantucek, R., Rosypal, S., Ruzicková, V., Pantucková, P., Kailerová, J., Klepárnik, K., Malá, Z., and Bocek, 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).

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