Characterizing spontaneous induction of Stx encoding phages using a selectable reporter system
dc.contributor.author | Livny, Jonathan | en_US |
dc.contributor.author | Friedman, David I. | en_US |
dc.date.accessioned | 2010-06-01T18:13:31Z | |
dc.date.available | 2010-06-01T18:13:31Z | |
dc.date.issued | 2004-03 | en_US |
dc.identifier.citation | Livny, Jonathan; Friedman, David I. (2004). "Characterizing spontaneous induction of Stx encoding phages using a selectable reporter system." Molecular Microbiology 51(6): 1691-1704. <http://hdl.handle.net/2027.42/71436> | en_US |
dc.identifier.issn | 0950-382X | en_US |
dc.identifier.issn | 1365-2958 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/71436 | |
dc.identifier.uri | http://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=15009895&dopt=citation | en_US |
dc.description.abstract | Shiga toxin (Stx) genes in Stx producing Escherichia coli (STEC) are encoded in prophages of the λ family, such as H-19B. The subpopulation of STEC lysogens with induced prophages has been postulated to contribute significantly to Stx production and release. To study induced STEC, we developed a s electable in vivo e xpression t echnology, SIVET, a reporter system adapted from the RIVET system. The SIVET lysogen has a defective H-19B prophage encoding the TnpR resolvase gene downstream of the phage P R promoter and a cat gene with an inserted tet gene flanked by targets for the TnpR resolvase. Expression of resolvase results in excision of tet , restoring a functional cat gene; induced lysogens survive and are chloramphenicol resistant. Using SIVET we show that: (i) approximately 0.005% of the H-19B lysogens are spontaneously induced per generation during growth in LB. (ii) Variations in cellular physiology (e.g. RecA protein) rather than in levels of expressed repressor explain why members of a lysogen population are spontaneously induced. (iii) A greater fraction of lysogens with stx encoding prophages are induced compared to lysogens with non-Stx encoding prophages, suggesting increased sensitivity to inducing signal(s) has been selected in Stx encoding prophages. (iv) Only a small fraction of the lysogens in a culture spontaneously induce and when the lysogen carries two lambdoid prophages with different repressor/operators, 933W and H-19B, usually both prophages in the same cell are induced. | en_US |
dc.format.extent | 463051 bytes | |
dc.format.extent | 3109 bytes | |
dc.format.mimetype | application/pdf | |
dc.format.mimetype | text/plain | |
dc.publisher | Blackwell Science Ltd | en_US |
dc.rights | 2004 Blackwell Publishing Ltd | en_US |
dc.title | Characterizing spontaneous induction of Stx encoding phages using a selectable reporter system | en_US |
dc.type | Article | en_US |
dc.subject.hlbsecondlevel | Microbiology and Immunology | en_US |
dc.subject.hlbtoplevel | Science | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Program in Cell and Molecular Biology, University of Michigan, Ann Arbor, MI 48109, USA. | en_US |
dc.contributor.affiliationum | Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109, USA. | en_US |
dc.identifier.pmid | 15009895 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/71436/1/j.1365-2958.2003.03934.x.pdf | |
dc.identifier.doi | 10.1111/j.1365-2958.2003.03934.x | en_US |
dc.identifier.source | Molecular Microbiology | en_US |
dc.identifier.citedreference | Barksdale, L., and Arden, S. B. ( 1974 ) Persisting bacteriophage infections, lysogeny, and phage conversions. Annu Rev Microbiol 0: 265 – 299. | en_US |
dc.identifier.citedreference | Bertani, G. ( 1951 ) Studies of Lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62: 293 – 300. | en_US |
dc.identifier.citedreference | Bochner, B. R., Huang, H. C., Schieven, G. L., and Ames, B. N. ( 1980 ) Positive selection for loss of tetracycline resistance. J Bacteriol 143: 926 – 933. | en_US |
dc.identifier.citedreference | Bolivar, F. ( 1978 ) Construction and characterization of new cloning vehicles. III. Derivatives of plasmid pBR322 carrying unique Eco RI sites for selection of Eco RI generated recombinant DNA molecules. Gene 4: 121 – 136. | en_US |
dc.identifier.citedreference | Boyd, E. F., and Brussow, H. ( 2002 ) Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol 10: 521 – 529. | en_US |
dc.identifier.citedreference | Brooks, K., and Clark, A. J. ( 1967 ) Behavior of lambda bacteriophage in a recombination deficienct strain of Escherichia coli. J Virol 1: 283 – 293. | en_US |
dc.identifier.citedreference | Broudy, T. B., Pancholi, V., and Fischetti, V. A. ( 2001 ) Induction of lysogenic bacteriophage and phage-associated toxin from group a streptococci during coculture with human pharyngeal cells. Infect Immun 69: 1440 – 1443. | en_US |
dc.identifier.citedreference | Calderwood, S. B., Auclair, F., Donohue-Rolfe, A., Keusch, G. T., and Mekalanos, J. J. ( 1987 ) Nucleotide sequence of the Shiga-like toxin genes of Escherichia coli. Proc Natl Acad Sci USA 84: 4364 – 4368. | en_US |
dc.identifier.citedreference | Camilli, A., and Mekalanos, J. J. ( 1995 ) Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection. Mol Microbiol 18: 671 – 683. | en_US |
dc.identifier.citedreference | Camilli, A., Beattie, D. T., and Mekalanos, J. J. ( 1994 ) Use of genetic recombination as a reporter of gene expression. Proc Natl Acad Sci USA 91: 2634 – 2638. | en_US |
dc.identifier.citedreference | Court, D. L., and Oppenheim, A. ( 1983 ) Phage lambda's accessory genes. In Lambda II. Hendrix, R. W., Roberts, J. W., Stahl, F. W., and Weisberg, R. A., (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, pp. 251 – 278. | en_US |
dc.identifier.citedreference | Court, D. L., Sawitzke, J. A., and Thomason, L. C. ( 2002 ) Genetic engineering using homologous recombination. Annu Rev Genet 36: 361 – 388. | en_US |
dc.identifier.citedreference | Datz, M., Janetzki-Mittmann, C., Franke, S., Gunzer, F., Schmidt, H., and Karch, H. ( 1996 ) Analysis of the enterohemorrhagic Escherichia coli O157 DNA region containing lambdoid phage gene P and Shiga-like toxin structural genes. Appl Environ Microbiol 62: 791 – 797. | en_US |
dc.identifier.citedreference | De Grandis, S., Ginsberg, J., Toone, M., Climie, S., Friesen, J., and Brunton, J. ( 1987 ) Nucleotide sequence and promoter mapping of the Escherichia coli Shiga-like toxin operon of bacteriophage H-19B. J Bacteriol 169: 4313 – 4319. | en_US |
dc.identifier.citedreference | Dodd, I. B., Perkins, A. J., Tsemitsidis, D., and Egan, J. B. ( 2001 ) Octamerization of lambda CI repressor is needed for effective repression of P (RM) and efficient switching from lysogeny. Genes Dev 15: 3013 – 3022. | en_US |
dc.identifier.citedreference | Eisen, H., Pereira da Silva, L., and Jacob, F. ( 1968 ) The regulation and mechanism of DNA synthesis in bacteriophage lambda. Cold Spring Harb Symp Quant Biol 33: 755 – 764. | en_US |
dc.identifier.citedreference | Friedberg, E. C., Walker, G. C., and Siede, W. S. ( 1995 ) DNA repair and mutagenesis. Washington, DC: Am Soc Microbiol Press. | en_US |
dc.identifier.citedreference | Fuchs, S., Muhldorfer, I., Donohue-Rolfe, A., Kerenyi, M., Emody, L., Alexiev, R., et al. ( 1999 ) Influence of RecA on in vivo virulence and Shiga toxin 2 production in Escherichia coli pathogens. Microb Pathog 27: 13 – 23. | en_US |
dc.identifier.citedreference | Gottesman, M. E., and Yarmolinsky, M. B. ( 1968 ) Integration-negative mutants of bacteriophage lambda. J Mol Biol 31: 487 – 505. | en_US |
dc.identifier.citedreference | Grindley, N. D. ( 1983 ) Transposition of Tn 3 and related transposons. Cell 32: 3 – 5. | en_US |
dc.identifier.citedreference | Gussin, G. N., Johnson, A. D., Pabo, C. O., and Sauer, R. T. ( 1983 ) Repressor and Cro protein: structure, function, and role in lysogenization. In Lambda II. Hendrix, R. W., Roberts, J. W., Stahl, F. W., and Weisberg, R. A., (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, pp. 93 – 121. | en_US |
dc.identifier.citedreference | Heffron, F. ( 1983 ) Tn 3 and its relatives. In Mobile Genetic Elements. Shapiro, J. A., (ed). New York, NY: Academic Press, pp. 223 – 260. | en_US |
dc.identifier.citedreference | Hendrix, R. W., Roberts, J. W., Stahl, F. W., and Weisberg, R. A. ( 1983 ) Lambda II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory. | en_US |
dc.identifier.citedreference | Hertman, I., and Luria, S. E. ( 1967 ) Transduction studies on the role of a rec+ gene in the ultraviolet induction of prophage lambda. J Mol Biol 23: 117 – 133. | en_US |
dc.identifier.citedreference | Heyderman, R. S., Soriani, M., and Hirst, T. R. ( 2001 ) Is immune cell activation the missing link in the pathogenesis of post-diarrhoeal HUS? Trends Microbiol 9: 262 – 266. | en_US |
dc.identifier.citedreference | Karch, H., Bielaszewska, M., Bitzan, M., and Schmidt, H. ( 1999 ) Epidemiology and diagnosis of Shiga toxin-producing Escherichia coli infections. Diagn Microbiol Infect Dis 34: 229 – 243. | en_US |
dc.identifier.citedreference | Kim, B., and Little, J. W. ( 1993 ) LexA and lambda Cl repressors as enzymes: specific cleavage in an intermolecular reaction. Cell 73: 1165 – 1173. | en_US |
dc.identifier.citedreference | Lee, S. H., Hava, D. L., Waldor, M. K., and Camilli, A. ( 1999 ) Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99: 625 – 634. | en_US |
dc.identifier.citedreference | Levine, A., Bailone, A., and Devoret, R. ( 1979 ) Cellular levels of the prophage lambda and 434 repressors. J Mol Biol 131: 655 – 661. | en_US |
dc.identifier.citedreference | Lin, L. L., and Little, J. W. ( 1988 ) Isolation and characterization of noncleavable (Ind-) mutants of the LexA repressor of Escherichia coli K-12. J Bacteriol 170: 2163 – 2173. | en_US |
dc.identifier.citedreference | Little, J. W. ( 1984 ) Autodigestion of lexA and phage lambda repressors. Proc Natl Acad Sci USA 81: 1375 – 1379. | en_US |
dc.identifier.citedreference | Little, J. W., and Mount, D. W. ( 1982 ) The SOS regulatory system of Escherichia coli. Cell 29: 11 – 22. | en_US |
dc.identifier.citedreference | Little, J. W., Shepley, D. P., and Wert, D. W. ( 1999 ) Robustness of a gene regulatory circuit. EMBO J 18: 4299 – 4307. | en_US |
dc.identifier.citedreference | Lwoff, A. ( 1953 ) Lysogeny. Bacteriol Rev 17: 269 – 337. | en_US |
dc.identifier.citedreference | Miller, H. I., and Friedman, D. I. ( 1980 ) An E. coli gene product required for lambda site-specific recombination. Cell 20: 711 – 719. | en_US |
dc.identifier.citedreference | Neely, M. N., and Friedman, D. I. ( 1998a ) Functional and genetic analysis of regulatory regions of coliphage H-19B: location of shiga-like toxin and lysis genes suggest a role for phage functions in toxin release. Mol Microbiol 28: 1255 – 1267. | en_US |
dc.identifier.citedreference | Neely, M. N., and Friedman, D. I. ( 1998b ) Arrangement and functional identification of genes in the regulatory region of lambdoid phage H-19B, a carrier of a Shiga-like toxin. Gene 223: 105 – 113. | en_US |
dc.identifier.citedreference | Newland, J. W., and Neill, R. J. ( 1988 ) DNA probes for Shiga-like toxins I and II and for toxin-converting bacteriophages. J Clin Microbiol 26: 1292 – 1297. | en_US |
dc.identifier.citedreference | O'Brien, A. D., Newland, J. W., Miller, S. F., Holmes, R. K., Smith, H. W., and Formal, S. B. ( 1984 ) Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226: 694 – 696. | en_US |
dc.identifier.citedreference | Pirrotta, V., and Ptashne, M. ( 1969 ) Isolation of the 434 phage repressor. Nature 222: 541 – 544. | en_US |
dc.identifier.citedreference | Plunkett, G., 3rd, Rose, D. J., Durfee, T. J., and Blattner, F. R. ( 1999 ) Sequence of Shiga toxin 2 phage 933W from Escherichia coli O157: H7: Shiga toxin as a phage late-gene product. J Bacteriol 181: 1767 – 1778. | en_US |
dc.identifier.citedreference | Ptashne, M. ( 1992 ) A Genetic Switch. Cambridge, MA: Cell Press and Blackwell Publications. | en_US |
dc.identifier.citedreference | Reed, R. R., Shibuya, G. I., and Steitz, J. A. ( 1982 ) Nucleotide sequence of gamma delta resolvase gene and demonstration that its gene product acts as a repressor of transcription. Nature 300: 381 – 383. | en_US |
dc.identifier.citedreference | Revet, B., von Wilcken-Bergmann, B., Bessert, H., Barker, A., and Muller-Hill, B. ( 1999 ) Four dimers of lambda repressor bound to two suitably spaced pairs of lambda operators form octamers and DNA loops over large distances. Curr Biol 9: 151 – 154. | en_US |
dc.identifier.citedreference | Roberts, J. W., and Devoret, R. ( 1983 ) Lysogenic induction. In Lambda II. Hendrix, R. W., Roberts, J. W., Stahl, F. W., and Weisberg, R. A., (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, pp. 123 – 144. | en_US |
dc.identifier.citedreference | Sambrook, J., and Fritsch,, E. M. ( 1989 ) Molecular Cloning, A laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Press. | en_US |
dc.identifier.citedreference | Shi, T., and Friedman, D. I. ( 2001 ) The operator-early promoter regions of Shiga-toxin bearing phage H-19B. Mol Microbiol 41: 585 – 599. | en_US |
dc.identifier.citedreference | Shinagawa, H., and Ito, T. ( 1973 ) Inactivation of DNA-binding activity of repressor in extracts of lambda-lysogen treated with mitomycin C. Mol Gen Genet 126: 103 – 110. | en_US |
dc.identifier.citedreference | Sjogren, R., Neill, R., Rachmilewitz, D., Fritz, D., Newland, J., Sharpnack, D., et al. ( 1994 ) Role of Shiga-like toxin I in bacterial enteritis: comparison between isogenic Escherichia coli strains induced in rabbits. Gastroenterology 106: 306 – 317. | en_US |
dc.identifier.citedreference | Smith, H. W., and Linggood, M. A. ( 1971 ) The transmissible nature of enterotoxin production in a human enteropathogenic strain of Escherichia coli. J Med Microbiol 4: 301 – 305. | en_US |
dc.identifier.citedreference | Sussman, R., and Jacob, F. ( 1962 ) Sur un systeme de repression thermosensible ch2 le bacteriophage 1 d’ Escherichia coli. C R Acad Sci Paris 254: 1517 – 1519. | en_US |
dc.identifier.citedreference | Sutcliffe, J. G. ( 1979 ) Complete nucleotide sequence of the Escherichia coli plasmid pBR322. Cold Spring Harb Symp Quant Biol 43 Part 1: 77 – 90. | en_US |
dc.identifier.citedreference | Thomason, L. C., Bubunenko, M., Constantino, N., Wilson, H. R., Oppenheim, A., and Court, D. L. ( 2003 ) Recombineering-genetic engineering in bacteria using homologous recombination. In Current Protocols in Molecular Biology. Ausubel, F. M., Brent, R. E., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, K., and Struhl, K., (eds). John Wiley and Sons, Unit.1.16. | en_US |
dc.identifier.citedreference | Toman, Z., Dambly-Chaudiere, C., Tenenbaum, L., and Radman, M. ( 1985 ) A system for detection of genetic and epigenetic alterations in Escherichia coli induced by DNA-damaging agents. J Mol Biol 186: 97 – 105. | en_US |
dc.identifier.citedreference | Unkmeir, A., and Schmidt, H. ( 2000 ) Structural analysis of phage-borne stx genes and their flanking sequences in shiga toxin-producing Escherichia coli and Shigella dysenteriae type 1 strains. Infect Immun 68: 4856 – 4864. | en_US |
dc.identifier.citedreference | Wagner, P. L., and Waldor, M. K. ( 2002 ) Bacteriophage control of bacterial virulence. Infect Immun 70: 3985 – 3993. | en_US |
dc.identifier.citedreference | Wagner, P. L., Acheson, D. W., and Waldor, M. K. ( 2001a ) Human neutrophils and their products induce Shiga toxin production by enterohemorrhagic Escherichia coli. Infect Immun 69: 1934 – 1937. | en_US |
dc.identifier.citedreference | Wagner, P. L., Neely, M. N., Zhang, X., Acheson, D. W., Waldor, M. K., and Friedman, D. I. ( 2001b ) Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J Bacteriol 183: 2081 – 2085. | en_US |
dc.identifier.citedreference | Wagner, P. L., Livny, J., Neely, M. N., Acheson, D. W., Friedman, D. I., and Waldor, M. K. ( 2002 ) Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol Microbiol 44: 957 – 970. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.