Characterization of a eukaryotic-like tyrosine protein kinase expressed by the Shiga toxin-encoding bacteriophage 933W

Journal of Bacteriology

Volumn 186, Issue 11, 2004, Pages 3472-3479

  Tyler, Jessica S ^a   Friedman, David I ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; PHOSPHOTRANSFERASE; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; SHIGA TOXIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIOPHAGE; BACTERIUM ISOLATE; CATALYSIS; CONTROLLED STUDY; ESCHERICHIA COLI; EUKARYOSIS; LYSOGENIZATION; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; PROPHAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; SKT GENE;

AMINO ACID SEQUENCE; COLIPHAGES; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; SHIGA TOXIN;

BACTERIA (MICROORGANISMS); BACTERIOPHAGE 933W; ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA; UNIDENTIFIED BACTERIOPHAGE;

EID: 2442699025     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.11.3472-3479.2004     Document Type: Article

References (72)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Aster, J. C., E. S. Robertson, R. P. Hasserjian, J. R. Turner, E. Kieff, and J. Sklar. 1997. Oncogenic forms of NOTCH1 lacking either the primary binding site for RBP-Jkappa or nuclear localization sequences retain the ability to associate with RBP-Jkappa and activate transcription. J. Biol. Chem. 272:11336-11343.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1995. Current protocols in molecular biology. John Wiley and Sons, New York, N.Y.
4. Av-Gay, Y., and M. Everett. 2000. The eukaryotic-like Ser/Thr protein kinases of Mycobacterium tuberculosis. Trends Microbiol. 8:238-244.
5. Bakal, C. J., and J. E. Davies. 2000. No longer an exclusive club: eukaryotic signalling domains in bacteria. Trends Cell Biol. 10:32-38.
6. Bliska, J. B., K. L. Guan, J. E. Dixon, and S. Falkow. 1991. Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant. Proc. Natl. Acad. Sci. USA 88:1187-1191.
7. Boyd, E. F., and H. Brussow. 2002. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 10:521-529.
8. Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201:110-149.
9. Campbell, A., and D. Botstein. 1983. Evolution of the lambdoid phages, p. 365-380. In R. W. Hendrix, J. W. Roberts, F. W. Stahl, and R. A. Weisberg (ed.), Lambda II, vol. II. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
10. Court, D. L., and A. B. Oppenheim. 1983. Phage lambda's accessory genes, p. 251-277. In R. W. Hendrix, J. W. Roberts, F. W. Stahl, and R. A. Weisberg (ed.), Lambda II, vol. II. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
11. Craven, M. G., A. E. Granston, A. T. Schauer, C. Zheng, T. A. Gray, and D. I. Friedman. 1994. Escherichia coli-Salmonella typhimurium hybrid nusA genes: identification of a short motif required for action of the lambda N transcription antitermination protein. J. Bacteriol. 176: 1394-1404.
12. Datz, M., C. Janetzki-Mittmann, S. Franke, F. Gunzer, H. Schmidt, and H. Karch. 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.
13. DeVinney, I., I. Steele-Mortimer, and B. B. Finlay. 2000. Phosphatases and kinases delivered to the host cell by bacterial pathogens. Trends Microbiol. 8:29-33.
14. Doublet, P., C. Vincent, C. Grangeasse, A. J. Cozzone, and B. Duclos. 1999. On the binding of ATP to the autophosphorylating protein, Ptk, of the bacterium Acinetobacter johnsonii. FEBS Lett. 445:137-143.
15. Ellis, H. M., D. Yu, T. DiTizio, and D. L. Court. 2001. High efficiency mutagenesis, repair, and engineering of chromosomal DNA using single-stranded oligonucleotides. Proc. Natl. Acad. Sci. USA 98:6742-6746.
16. Engelberg-Kulka, H., M. Reches, S. Narasimhan, R. Schoulaker-Schwarz, Y. Klemes, E. Aizenman, and G. Glaser. 1998. rexB of bacteriophage lambda is an anti-cell death gene. Proc. Natl. Acad. Sci. USA 95:15481-15486.
17. Galyov, E. E., S. Hakansson, A. Forsberg, and H. Wolf-Watz. 1993. A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant. Nature 361:730-732.
18. Gottesman, M. E., and M. B. Yarmolinsky. 1968. Integration-negative mutants of bacteriophage lambda. J. Mol. Biol. 31:487-505.
19. Hanks, S. K., and T. Hunter. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9:576-596.
20. Hanks, S. K., A. M. Quinn, and T. Hunter. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
21. Hendrix, R. W. 2002. Bacteriophages: evolution of the majority. Theor. Popul. Biol. 61:471-480.
22. Hendrix, R. W., J. G. Lawrence, G. F. Hatfull, and S. Casjens. 2000. The origins and ongoing evolution of viruses. Trends Microbiol. 8:504-508.
23. Hirsch-Kauffmann, M., P. Herrlich, H. Ponta, and M. Schweiger. 1975. Helper function of T7 protein kinase in virus propagation. Nature 255:508-510.
24. Horton, R. M., H. D. Hunt, S. N. Ho, J. K. Pullen, and L. R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
25. Hubbard, S. R., L. Wei, L. Ellis, and W. A. Hendrickson. 1994. Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 372: 746-754.
26. Ilan, O., Y. Bloch, G. Frankel, H. Ullrich, K. Geider, and I. Rosenshine. 1999. Protein tyrosine kinases in bacterial pathogens are associated with virulence and production of exopolysaccharide. EMBO J. 18:3241-3248.
27. Johansen, B. K., Y. Wasteson, P. E. Granum, and S. Brynestad. 2001. Mosaic structure of Shiga-toxin-2-encoding phages isolated from Escherichia. coli O157:H7 indicates frequent gene exchange between lambdoid phage genomes. Microbiology 147:1929-1936.
28. Juris, S. J., A. E. Rudolph, D. Huddler, K. Orth, and J. E. Dixon. 2000. A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption. Proc. Natl. Acad. Sci. USA 97:9431-9436.
29. Karch, H., M. Bielaszewska, M. Bitzan, and H. Schmidt. 1999. Epidemiology and diagnosis of Shiga toxin-producing Escherichia coli infections. Diagn. Microbiol. Infect. Dis. 34:229-243.
30. Knighton, D. R., D. L. Cadena, J. Zheng, L. F. Ten Eyck, S. S. Taylor, J. M. Sowadski, and G. N. Gill. 1993. Structural features that specify tyrosine kinase activity deduced from homology modeling of the epidermal growth factor receptor. Proc. Natl. Acad. Sci. USA 90:5001-5005.
31. Knighton, D. R., J. H. Zheng, L. F. Ten Eyck, V. A. Ashford, N. H. Xuong, S. S. Taylor, and J. M. Sowadski. 1991. Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253:407-414.
32. Landsmann, J., M. Kroger, and G. Hobom. 1982. The rex region of bacteriophage lambda: two genes under three-way control. Gene 20:11-24.
33. Matz, K., M. Schmandt, and G. N. Gussin. 1982. The rex gene of bacteriophage lambda is really two genes. Genetics 102:319-327.
34. Miller, J. H. 1992. A short course in bacterial genetics: a laboratory manual for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
35. Moran, M. F., C. A. Koch, I. Sadowski, and T. Pawson. 1988. Mutational analysis of a phosphotransfer motif essential for v-fps tyrosine kinase activity. Oncogene 3:665-672.
36. Morona, J. K., J. C. Paton, D. C. Miller, and R. Morona. 2000. Tyrosine phosphorylation of CpsD negatively regulates capsular polysaccharide biosynthesis in Streptococcus pneumoniae. Mol. Microbiol. 35:1431-1442.
37. Muniesa, M., J. Recktenwald, M. Bielaszewska, H. Karch, and H. Schmidt. 2000. Characterization of a Shiga toxin 2e-converting bacteriophage from an Escherichia coli strain of human origin. Infect. Immun. 68:4850-4855.
38. Nakar, D., and D. L. Gutnick. 2003. Involvement of a protein tyrosine kinase in production of the polymeric bioemulsifier emulsan from the oil-degrading strain Acinetobacter lwoffii RAG-1. J. Bacteriol. 185:1001-1009.
39. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
40. Neely, M. N., and D. I. Friedman. 1998. 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.
41. Nickels, B. E., S. L. Dove, K. S. Murakami, S. A. Darst, and A. Hochschild. 2002. Protein-protein and protein-DNA interactions of sigma70 region 4 involved in transcription activation by lambdacI. J. Mol. Biol. 324:17-34.
42. Niemeyer, D., and A. Becker. 2001. The molecular weight distribution of succinoglycan produced by Sinorhizobium meliloti is influenced by specific tyrosine phosphorylation and ATPase activity of the cytoplasmic domain of the ExoP protein. J. Bacteriol. 183:5163-5170.
43. O'Brien, A. D., J. W. Newland, S. F. Miller, R. K. Holmes, H. W. Smith, and S. B. Formal. 1984. Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226:694-696.
44. O'Brien, K. B., L. S. Argetsinger, M. Diakonova, and C. Carter-Su. 2003. YXXL motifs in SH2-Bbeta are phosphorylated by JAK2, JAK1, and platelet-derived growth factor receptor and are required for membrane ruffling. J. Biol. Chem. 278:11970-11978.
45. Ortiz-Lombardia, M., F. Pompeo, B. Boitel, and P. M. Alzari. 2003. Crystal structure of the catalytic domain of the PknB serine/threonine kinase from Mycobacterium tuberculosis. J. Biol. Chem. 278:13094-13100.
46. Parma, D. H., M. Snyder, S. Sobolevski, M. Nawroz, E. Brody, and L. Gold. 1992. The Rex system of bacteriophage lambda: tolerance and altruistic cell death. Genes Dev. 6:497-510.
47. Paton, A. W., P. Srimanote, M. C. Woodrow, and J. C. Paton. 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 69:6999-7009.
48. Plunkett, G., III, D. J. Rose, T. J. Durfee, and F. R. Blattner. 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.
49. Ptashne, M. 1992. A genetic switch, 2nd ed. Cell Press & Blackwell Scientific Publications, Cambridge, United Kingdom.
50. Ptashne, M., K. Backman, M. Z. Humayun, A. Jeffrey, R. Maurer, B. Meyer, and R. T. Sauer. 1976. Autoregulation and function of a repressor in bacteriophage lambda. Science 194:156-161.
51. Recktenwald, J., and H. Schmidt. 2002. The nucleotide sequence of Shiga toxin (Stx) 2e-encoding phage φP27 is not related to other Stx phage genomes, but the modular genetic structure is conserved. Infect. Immun. 70: 1896-1908.
52. Reichardt, L., and A. D. Kaiser. 1971. Control of lambda repressor synthesis. Proc. Natl. Acad. Sci. USA 68:2185-2189.
53. Riley, L. W., R. S. Remis, S. D. Helgerson, H. B. McGee, J. G. Wells, B. R. Davis, R. J. Hebert, E. S. Olcott, L. M. Johnson, N. T. Hargrett, P. A. Blake, and M. L. Cohen. 1983. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308:681-685.
54. 2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect. Immun. 71: 7129-7139.
55. Sambrook, J., and D. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed., vol. 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
56. Sato, T., T. Shimizu, M. Watarai, M. Kobayashi, S. Kano, T. Hamabata, Y. Takeda, and S. Yamasaki. 2003. Distinctiveness of the genomic sequence of Shiga toxin 2-converting phage isolated from Escherichia coli O157:H7 Okayama strain as compared to other Shiga toxin 2-converting phages. Gene 309:35-48.
57. Spiegelman, W. G. 1971. Two states of expression of genes cl, rex, and N in lambda. Virology 43:16-33.
58. Tan, J. L., and J. A. Spudich. 1990. Developmentally regulated protein-tyrosine kinase genes in Dictyostelium discoideum. Mol. Cell. Biol. 10:3578-3583.
59. Taylor, S. S., E. Radzio-Andzelm, and T. Hunter. 1995. How do protein kinases discriminate between serine/threonine and tyrosine? Structural insights from the insulin receptor protein-tyrosine kinase. FASEB J. 9:1255-1266.
60. Tomizawa, J., and T. Ogawa. 1967. Effect of ultraviolet irradiation on bacteriophage lambda immunity. J. Mol. Biol. 23:247-263.
61. Unkmeir, A., and H. Schmidt. 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.
62. Vincent, C., B. Duclos, C. Grangeasse, E. Vaganay, M. Riberty, A. J. Cozzone, and P. Doublet. 2000. Relationship between exopolysaccharide production and protein-tyrosine phosphorylation in gram-negative bacteria. J. Mol. Biol. 304:311-321.
63. Wagner, P. L., D. W. K. Acheson, and M. K. Waldor. 1999. Isogenic lysogens of diverse Shiga toxin 2-encoding bacteriophages produce markedly different amounts of Shiga toxin. Infect. Immun. 67:6710-6714.
64. Wagner, P. L., J. Livny, M. N. Neely, D. W. Acheson, D. I. Friedman, and M. K. Waldor. 2002. Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol. Microbiol. 44:957-970.
65. Wagner, P. L., M. N. Neely, X. Zhang, D. W. K. Acheson, M. K. Waldor, and D. I. Friedman. 2001. Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J. Bacteriol. 183:2081-2085.
66. Walker, J. E., M. Saraste, M. J. Runswick, and N. J. Gay. 1982. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:945-951.
67. Watarai, M., T. Sato, M. Kobayashi, T. Shimizu, S. Yamasaki, T. Tobe, C. Sasakawa, and Y. Takeda. 1998. Identification and characterization of a newly isolated Shiga toxin 2-converting phage from Shiga toxin-producing Escherichia coli. Infect. Immun. 66:4100-4107.
68. Wu, J., N. Ohta, J. L. Zhao, and A. Newton. 1999. A novel bacterial tyrosine kinase essential for cell division and differentiation. Proc. Natl. Acad. Sci. USA 96:13068-13073.
69. Wugeditsch, T., A. Paiment, J. Hocking, J. Drummelsmith, C. Forrester, and C. Whitfield. 2001. Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J. Biol. Chem. 276:2361-2371.
70. Yu, D., H. M. Ellis, E. C. Lee, N. A. Jenkins, N. G. Copeland, and D. L. Court. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl. Acad. Sci. USA 97:5978-5983.
71. Zhang, C. C. 1996. Bacterial signalling involving eukaryotic-type protein kinases. Mol. Microbiol. 20:9-15.
72. Zhang, Z. Y., J. C. Clemens, H. L. Schubert, J. A. Stuckey, M. W. Fischer, D. M. Hume, M. A. Saper, and J. E. Dixon. 1992. Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase. J. Biol. Chem. 267:23759-23766.