Site-specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization

Cellular Microbiology

Volumn 7, Issue 3, 2005, Pages 363-371

  Brugirard Ricaud, Karine ^a   Duchaud, Eric ^a   Givaudan, Alain ^a   Girard, Pierre Alain ^a   Kunst, Frank ^b   Boemare, Noel ^a   Brehélin, Michel ^a   Zumbihl, Robert ^a  

^a UNIV MONTPELLIER   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; CYTOTOXIN; GUANOSINE TRIPHOSPHATASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

AMINO ACID SEQUENCE; ARMYWORM; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL COLONIZATION; BACTERIAL GENOME; CONTROLLED STUDY; ELECTROPHORESIS; EUKARYOTIC CELL; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENE TRANSLOCATION; GENOME ANALYSIS; HOST CELL; HOST PATHOGEN INTERACTION; IN VITRO STUDY; IN VIVO STUDY; INSECT CELL; INTRACELLULAR TRANSPORT; LOCUST; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PHOTORHABDUS LUMINESCENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RNA TRANSLATION; SEQUENCE ANALYSIS; YERSINIA;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CELL MEMBRANE; CYSTEINE ENDOPEPTIDASES; GENOME, BACTERIAL; GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; HELA CELLS; HUMANS; LOCUSTA MIGRATORIA; MOLECULAR SEQUENCE DATA; PHAGOCYTOSIS; PHOTORHABDUS; RECOMBINANT FUSION PROTEINS; RHOA GTP-BINDING PROTEIN; SPODOPTERA;

EID: 14044279227     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2004.00466.x     Document Type: Article

References (33)

1. Boyd, A.P., Lambermont, I., and Cornelis, G.R. (2000) Competition between the Yops of Yersinia enterocolitica for delivery into eukaryotic cells: role of the SycE chaperone binding domain of YopE. J Bacteriol 182: 4811-4821.
2. Brehélin, M., and Zachary, D. (1986) Insect haemocytes: a new classification to rule out the controversy. In Immunity in Invertebrates. Brehélin, M. (ed.). Berlin-Heidelberg: Springer Verlag, pp. 36-48.
3. Brillard, J., Duchaud, E., Boemare, N., Kunst, F., and Givaudan, A. (2002) The PhlA hemolysin from the entomopathogenic bacterium Photorhabdus luminescens belongs to the two-partner secretion family of hemolysins. J Bacteriol 184: 3871-3878.
4. Brugirard-Ricaud, K., Givaudan, A., Parkhill, J., Boemare, N., Zumbihl, R., and Duchaud, E. (2004) Variation in the effectors of the Photorhabdus type III secretion system among species revealed by genomic analysis. J Bacteriol 186: 4376-4381.
5. Duchaud, E., Rusniok, C., Frangeul, L., Buchrieser, C., Givaudan, A., Taourit, S., et al. (2003) The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat Biotechnol 21: 1307-1313.
6. Farmer, J.J., III, Jorgensen, J.H., Grimont, P.A., Akhurst, R.J., Poinar, G.O., Jr, Ageron, E., et al. (1989) Xenorhabdus luminescens (DNA hybridization group 5) from human clinical specimens. J Clin Microbiol 27: 1594-1600.
7. Fellay, R., Frey, J., and Krisch, H. (1987) Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene 52: 147-154.
8. Fischer-Le Saux, M., Viallard, V., Brunel, B., Normand, P., and Boemare, N.E. (1999) Polyphasic classification of the genus Photorhabdus and proposal of new taxa: P. luminescens subsp. luminescens subsp. nov., P. luminescens subsp. akhurstii subsp. nov., P. luminescens subsp. laumondii subsp. nov., P. temperata sp. nov., P. temperata subsp. temperata subsp. nov. & P. asymbiotica sp. nov. Int J Syst Bacteriol 49: 1645-1656.
9. Forst, S., Dowds, B., Boemare, N., and Stackebrandt, E. (1997) Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol 51: 47-72.
10. Gerrard, J.G., McNevin, S., Alfredson, D., Forgan-Smith, R., and Fraser, N. (2003) Photorhabdus species: bioluminescent bacteria as emerging human pathogens? Emerg Infect Dis 9: 251-254.
11. Givaudan, A., and Lanois, A. (2000) flhDC, the flagellar master operon of Xenorhabdus nematophilus: requirement for motility, lipolysis, extracellular hemolysis, and full virulence in insects. J Bacteriol 182: 107-115.
12. Grosdent, N., Maridonneau-Parini, I., Sory, M.P., and Cornelis, G.R. (2002) Role of Yops and adhesins in resistance of Yersinia enterocolitica to phagocytosis. Infect Immun 70: 4165-4176.
13. Hoffmann, J. (1969) Etude de la récupération hémocytaire après hémorragies expérimentales chez l'orthoptère Locusta migratoria. J Insect Physiol 15: 1375-1384.
14. Hoffmann, D., Brehélin, M., and Hoffmann, J. (1974) Modifications of the hemogram and of the hemocytipoietic tissue of male adults of Locusta migratoria (Orthoptera) after injection of Bacillus thuriengiensis. J Invertebr Pathol 24: 238-247.
15. Hoffmann, J., Zachary, D., Hoffmann, D., and Brehélin, M. (1979) Postembryonic development and differenciation: hematopoietic tissues and their functions in some insects. In Insects Hemocytes. Gupta, A.P. (ed.) London: Cambridge University press, pp. 29-66.
16. Hovey, A.K., and Frank, D.W. (1995) Analyses of the DNA-binding and transcriptional activation properties of ExsA, the transcriptional activator of the Pseudomonas aeruginosa exoenzyme S regulon. J Bacteriol 177: 4427-4436.
17. Iriarte, M., and Cornelis, G.R. (1998) YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol Microbiol 29: 915-929.
18. Jacobi, C.A., Roggenkamp, A., Rakin, A., Zumbihl, R., Leitritz, L., and Heesemann, J. (1998) In vitro and in vivo expression studies of yopE from Yersinia enterocolitica using the gfp reporter gene. Mol Microbiol 30: 865-882.
19. Kanter-Smoler, G., Dahlkvist, A., and Sunnerhagen, P. (1994) Improved method for rapid transformation of intact Schizosaccharomyces pombe cells. Biotechniques 16: 798-800.
20. Kim, B., and Kim, J. (1997) Role of Rac GTPase in the nuclear signaling by EGF. FEBS Lett 407: 7-12.
21. Koster, M., Bitter, W., de Cock, H., Allaoui, A., Cornelis, G.R., and Tommassen, J. (1997) The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex. Mol Microbiol 26: 789-797.
22. Liu, D., Burton, S., Glancy, T., Li, Z.S., Hampton, R., Meade, T., and Merlo, D.J. (2003) Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nat Biotechnol 21: 1222-1228.
23. Miller, J.S., Howard, R.W., Rana, R.L., Tunaz, H., and Stanley, D.W. (1999) Eicosanoids mediate nodulation reactions to bacterial infections in adults of the cricket, Gryllus assimilis. J Insect Physiol 45: 75-83.
24. Miyata, S., Casey, M., Frank, D.W., Ausubel, F.M., and Drenkard, E. (2003) Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect Immun 71: 2404-2413.
25. Ouahrani-Bettache, S., Porte, F., Teyssier, J., Liautard, J.P., and Kohler, S. (1999) pBBR1-GFP: a broad-host-range vector for prokaryotic promoter studies. Biotechniques 26: 620-622.
26. Peel, M.M., Alfredson, D.A., Gerrard, J.G., Davis, J.M., Robson, J.M., McDougall, R.J., et al. (1999) Isolation, identification, and molecular characterization of strains of Photorhabdus luminescens from infected humans in Australia. J Clin Microbiol 37: 3647-3653.
27. Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., Gustafsson, M., Magnusson, K.E., and Wolf-Watz, H. (1996) Modulation of virulence factor expression by pathogen target cell contact. Science 273: 1231-1233.
28. Ratcliffe, N. (1993) Cellular responses of Insects: Unresolved Problems. In Parasites and Pathogens of Insects. Beckage, N., Thompson, S., and Federici, B. (eds). San Diego: Academic Press, pp. 267-304.
29. Shao, F., Merritt, P.M., Bao, Z., Innes, R.W., and Dixon, J.E. (2002) A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109: 575-588.
30. Silva, C.P., Waterfield, N.R., Daborn, P.J., Dean, P., Chilver, T., Au, C.P., et al. (2002) Bacterial infection of a model insect: Photorhabdus luminescens and Manduca sexta. Cell Microbiol 4: 329-339.
31. Sorg, I., Hoffmann, C., Dumbach, J., Aktories, K., and Schmidt, G. (2003) The C terminus of YopT is crucial for activity and the N terminus is crucial for substrate binding. Infect Immun 71: 4623-4632.
32. Viboud, G.I., So, S.S., Ryndak, M.B., and Bliska, J.B. (2003) Proinflammatory signalling stimulated by the type III translocation factor YopB is counteracted by multiple effectors in epithelial cells infected with Yersinia pseudotuberculosis. Mol Microbiol 47: 1305-1315.
33. Zumbihl, R., Aepfelbacher, M., Andor, A., Jacobi, C.A., Ruckdeschel, K., Rouot, B., and Heesemann, J. (1999) The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J Biol Chem 274: 29289-29293.