A genome-wide screen identifies a Bordetella type III secretion effector and candidate effectors in other species

Molecular Microbiology

Volumn 58, Issue 1, 2005, Pages 267-279

  Panina, Ekaterina M ^a   Mattoo, Seema ^a,d   Griffith, Natasha ^a   Kozak, Natalia A ^a   Yuk, Ming H ^b   Miller, Jeff F ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE;

ARTICLE; BACTERIAL GENOME; BORDETELLA; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; EFFECTOR CELL; GENE EXPRESSION; GENE INTERACTION; GENE LOCUS; GENETIC TRANSFECTION; GENOME ANALYSIS; HEMOLYSIS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

BACTERIAL PROTEINS; BACTERIAL TOXINS; BLOTTING, WESTERN; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; CELL DEATH; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC TECHNIQUES; GENOME, BACTERIAL; HEMOLYSIS; MOLECULAR CHAPERONES; PHYLOGENY; PROTEIN BINDING; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); BORDETELLA; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; EUKARYOTA; INSECTA; MAMMALIA;

EID: 26244460966     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04823.x     Document Type: Article

References (41)

1. Akerley, B.J., Monack, D.M., Falkow, S., and Miller, J.F. (1992) The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica. J Bacteriol 174: 980-990.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., Rapp, B.A., and Wheeler, D.L. (2000) GenBank. Nucleic Acids Res 28: 15-18.
4. Bjellqvist, B., Hughes, G.J., Pasquali, Ch., Paquet, N., Ravier, F., Sanchez, J.-Ch., et al. (1993) The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis 14: 1023-1031.
5. Brugirard-Ricaud, K., Givaudan, A., Parkhill, J., Boemare, N., Kunst, F., Zumbihl, R., and Duchaud, E. (2004) Variation in the effectors of the type III secretion system among Photorhabdus species as revealed by genomic analysis. J Bacteriol 186: 4376-4381.
6. Cheng, L.W., Anderson, D.M., and Schneewind, O. (1997) Two independent type III secretion mechanisms for YopE in Yersinia enterocolitica. Mol Microbiol 24: 757-765.
7. Cotter, P.A., and Miller, J.F. (2000) Bordetella. In Principles of Bacterial Pathogenesis. Groisman, E. (ed.). San Diego, CA: Academic Press, pp. 619-674.
8. Creasey, E.A., Delahay, R.M., Bishop, A.A., Shaw, R.K., Kenny, B., Knutton, S., et al. (2003) CesT is a bivalent enteropathogenic Escherichia coli chaperone required for translocation of both Tir and Map. Mol Microbiol 47: 209-221.
9. Day, J.B., and Piano, G.V. (1998) A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersinia pestis. Mol Microbiol 30: 777-788.
10. Day, J.B., Ferracci, F., and Piano, G.V. (2003) Translocation of YopE and YopN into eukaryotic cells by Yersinia pestis yopN, tyeA, sycN, yscB and IcrG deletion mutants measured using a phosphorylatable peptide tag and phospho-specific antibodies. Mol Microbiol 47: 807-823.
11. Deng, W., Puente, J.L., Gruenheid, S., Vallance, B., Vasquez, A., Barba, J., et al. (2004) Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 101: 3597-3602.
12. Edwards, R.A., Keller, L.H., and Schifferli, D.M. (1998) Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207: 149-157.
13. van Eerde, A., Hamiaux, C., Perez, J., Parsot, C., and Dijkstra, B.W. (2004) Structure of Spa15, a type III secretion chaperone from Shigella flexneri with broad specificity. EMBO Rep 5: 477-483.
14. Feldman, M.F., and Cornelis, G.R. (2003) The multitalented type III chaperones: all you can do with 15 KDa. FEMS Microbiol Lett 219: 151-158.
15. Felsenstein, J. (1996) Inferring phytogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol 266: 418-427.
16. Fouts, D.E., Abramovitch, R.B., Alfano, U.R., Baldo, A.M., Buell, C.R., Cartinhour, S., et al. (2002) Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc Natl Acad Sci USA 99: 2275-2280.
17. Guttman, D.S., Vinatzer, B.A., Sarkar, S.F., Ranall, M.V., Kettler, G., and Greenberg, J.T. (2002) A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 1722-1726.
18. Kovach, M.E., Elzer, P.M., Hill, D.S., Robertson, G.T., Farris, M.A., Roop, R.M., II, and Peterson, K.M. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
19. Kozak, N.A., Mattoo, S., Foreman-Wykert, A.K., Whiteleggie, J.P., and Miller, J.F. (2005) Interactions between partner switcher orthologs BtrW and BtrV regulate type III secretion in Bordetella. J Bacteriol 187: 5665-5676.
20. Kuwae, A., Ohishi, M., Watanabe, M., Nagai, M., and Abe, A. (2003) BopB is a type III secreted protein in Bordetella bronchiseptica and is required for cytotoxicity against cultured mammalian cells. Cell Microbiol 5: 973-983.
21. McGuffin, L.J., Bryson, K., and Jones, D.T. (2000) The PSIPRED protein structure prediction server. Bioinformatics 16: 404-405.
22. Marenne, M.N., Journet, L., Mota, L.J., and Cornelis, G.R. (2003) Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb Pathog 35: 243-258.
23. Martinez de Tejada, G., Miller, J.F., and Cotter, P.A. (1996) Comparative analysis of the virulence control systems of Bordetella pertussis and Bordetella bronchiseptica. Mol Microbiol 22: 895-908.
24. Mattoo, S., Yuk, M.H., Huang, L.L., and Miller, J.F. (2004) Regulation of type III secretion in Bordetella. Mol Microbiol 52: 1201-1214.
25. Miao, E.A., and Miller, S.I. (2000) A conserved amino acid sequence directing intracellular type III secretion by Salmonella typhimurium. Proc Natl Acad Sci USA 97: 7539-7544.
26. Page, A.L., and Parsot, C. (2002) Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol 46: 1-11.
27. Page, A.L., Sansonetti, P., and Parsot, C. (2002) Spa15 of Shigella flexneri, a third type of chaperone in the type III secretion pathway. Mol Microbiol 43: 1533-1542.
28. Park, K.S., Ono, T., Rokuda, M., Jang, M.H., Okada, K., Iida, T., and Honda, T. (2004) Functional characterization of two type III secretion systems of Vibrio parahaemolyticus. Infect Immun 72: 6659-6665.
29. Parsot, C., Hamiaux, C., and Page, A.L. (2003) The various and varying roles of specific chaperones in type III secretion systems. Curr Opin Microbiol 6: 7-14.
30. Pellegrini, M., Marcotte, E.M., Thompson, M.J., Eisenberg, D., and Yeates, T.O. (1999) Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Proc Natl Acad Sci USA 96: 4285-4288.
31. Rainbow, L., Hart, C.A., and Winstanley, C. (2002) Distribution of type III secretion gene clusters in Burkholderia pseudomallei, B. thailandensis and B. mallei. J Med Microbiol 51: 374-384.
32. Roe, A.J., Hoey, D.E., and Gally, D.L. (2003) Regulation, secretion and activity of type III-secreted proteins of enterohaemorrhagic Escherichia coli O157. Biochem Soc Trans 31: 98-103.
33. Sansonetti, P.J., Ryter, A., Clerc, P., Maurelli, A.T., and Mounier, J. (1986) Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect Immun 51: 461-469.
34. Schubot, F.D., Jackson, M.W., Penrose, K.J., Cherry, S., Tropea, J.E., Piano, G.V., and Waugh, D.S. (2005) Three-dimensional structure of a macromolecular assembly that regulates type III secretion in Yersinia pestis. J Mol Biol 346: 1147-1161.
35. Stockbauer, K.E., Foreman-Wykert, A.K., and Miller, J.F. (2003) Bordetella type III secretion induces caspase 1-independent necrosis. Cell Microbiol 5: 123-132.
36. Subtil, A., Blocker, A., and Dautry-Varsat, A. (2000) Type III secretion system in Chlamydia species: identified members and candidates. Microbes Infect 2: 367-369.
37. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgons, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
38. Waterman, S.R., and Holden, D.W. (2003) Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5: 501-511.
39. Yuk, M.H., Harvill, E.T., and Miller, J.F. (1998) The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica. Mol Microbiol 28: 945-959.
40. Yuk, M.H., Harvill, E.T., Cotter, P.A., and Miller, J.F. (2000) Modulation of host immune responses, induction of apoptosis and inhibition of NF-kappaB activation by the Bordetella type III secretion system. Mol Microbiol 35: 991-1004.
41. Zaharik, M.L., Gruenheid, S., Perrin, A.J., and Finlay, B.B. (2002) Delivery of dangerous goods: type III secretion in enteric pathogens. Int J Med Microbiol 291: 593-603.