Recent insight into the pathogenicity mechanisms of the emergent pathogen Photorhabdus asymbiotica

Microbes and Infection

Volumn 12, Issue 3, 2010, Pages 182-189

  Costa, Sónia C P ^a,b,c   Chavez, Carolina Varela ^a,b   Jubelin, Grégory ^a,b   Givaudan, Alain ^a,b   Escoubas, Jean Michel ^a,b   Brehélin, Michel ^a,b   Zumbihl, Robert ^a,b  

^a University of Montpellier II   (France)

^b UNIV MONTPELLIER   (France)

^c UNIVERSITY OF THE AZORES   (Portugal)

Author keywords

Apoptosis; Comparative genomics; Emergent pathogen; Insect; Man; Phagocytosis; Photorhabdus asymbiotica; Virulence factors

Indexed keywords

VIRULENCE FACTOR;

APOPTOSIS; BACTERIAL CELL; BACTERIUM ISOLATE; COMPARATIVE GENOMIC HYBRIDIZATION; ENTOMOPATHOGENIC BACTERIUM; HUMAN; INFLAMMATION; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PHOTORHABDUS; PHOTORHABDUS ASYMBIOTICA; PRIORITY JOURNAL; SHORT SURVEY;

BACTERIAL PROTEINS; GENOME, BACTERIAL; HUMANS; PHOTORHABDUS; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); HEXAPODA; PHOTORHABDUS ASYMBIOTICA;

EID: 76549098480     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2009.12.003     Document Type: Short Survey

References (57)

1. Gerrard J., Waterfield N., Vohra R., and Ffrench-Constant R.H. Human infection with Photorhabdus asymbiotica: an emerging bacterial pathogen. Microbes Infect. 6 (2004) 229-237
2. Ehlers R.U. Entomopathogenic nematodes in the European biocontrol market. Commun. Agric. Appl. Biol. Sci. 68 (2003) 3-16
3. Forst S., Dowds B., Boemare N.E., and Stackebrandt E. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu. Rev. Microbiol. 51 (1997) 47-72
4. Waterfield N.R., Ciche T., and Clarke D. Photorhabdus and a host of hosts. Annu. Rev. Microbiol. 63 (2009) 557-574
5. Waterfield N., Wren B.W., and Ffrench-Constant R.H. Invertebrates as a source of emerging human pathogens. Nat. Rev. Microbiol. 2 (2004) 833-841
6. Farmer J.J., Jorgensen J.H., Grimont P.A., Akhurst R.J., Poinar G.O., Ageron E., Pierce G.V., Smith J.A., Carter G.P., Wilson K.L., and Hickman-Brenner W. Xenorhabdus luminescens (DNA hybridization group 5) from human clinical specimens. J. Clin. Microbiol. 27 (1989) 1594-1600
7. Weissfeld A.S., Halliday R.J., Simmons D.E., Trevino E.A., Vance P.H., O'Hara C.M., Sowers E.G., Kern R., Koy R.D., Hodde K., Bing M., Lo C., Gerrard J., Vohra R., and Harper J. Photorhabdus asymbiotica, a pathogen emerging on two continents that proves that there is no substitute for a well-trained clinical microbiologist. J. Clin. Microbiol. 43 (2005) 4152-4155
8. Peel M.M., Alfredson D.A., Gerrard J.G., Davis J.M., Robson J.M., McDougall R.J., Sculli B.L., and Akhurst R.J. Isolation, identification, and molecular characterization of strains of Photorhabdus luminescens from infected humans in Australia. J. Clin. Microbiol. 37 (1999) 3647-3653
9. Fischer-Le Saux M., Viallard V., Brunel B., Normand P., and Boemare N.E. 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. and P asymbiotica sp. nov. Int. J. Syst. Bacteriol. 49 (1999) 1645-1656
10. Gerrard J.G., Joyce S.A., Clarke D.J., Ffrench-Constant R.H., Nimmo G.R., Looke D.F., Feil E.L., Pearce L., and Waterfield N. Nematode symbiont for Photorhabdus asymbiotica. Emerg. Infect. Dis. 12 (2006) 1562-1564
11. Plichta K.L., Joyce S.A., Clarke D., Waterfield N., and Stock S.P. Heterorhabditis gerrardi n. sp. (Nematoda: Heterorhabditidae): the hidden host of Photorhabdus asymbiotica (Enterobacteriaceae: gamma-Proteobacteria). J. Helminthol. 16 (2009) 1-12
12. Kuwata R., Yoshiga T., Yoshida M., and Kondo E. Mutualistic association of Photorhabdus asymbiotica with Japanese Heterorhabditid entomopathogenic nematodes. Microbes Infect. 10 (2008) 734-741
13. Hinnebusch B.J. Bubonic plague: a molecular genetic case history of the emergence of an infectious disease. J. Mol. Med. 75 (1997) 645-652
14. Gerrard J.G., Vohra R., and Nimmo G.R. Identification of Photorhabdus asymbiotica in cases of human infection. Commun. Dis. Intell. 27 (2003) 540-541
15. Brüssow H., Canchaya C., and Hardt W.D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68 (2004) 560-602
16. Wilkinson P., Waterfield N., Crossman L., Corton C., Sanchez-Contreras M., Vlisidou I., Barron A., Bignell A., Clark L., Ormond D., Mayho M., Bason N., Smith F., Simmonds M., Churcher C., Harris D., Thompson N.R., Quail M., Parkhill J., and Ffrench-Constant R.H. Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens. BMC Genomics 10 (2009) 302
17. Hinnebusch B.J., Rudolph A.E., Cherepanov P., Dixon J.E., Schwan T.G., and Forsberg A. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296 (2002) 733-735
18. Lee V.T., and Schneewind O. Protein secretion and the pathogenesis of bacterial infections. Genes Dev. 15 (2001) 1725-1752
19. Duchaud E., Rusniok C., Frangeul L., Buchrieser C., Givaudan A., Taourit S., Bocs S., Boursaux-Eude C., Chandler M., Charles J.F., Dassa E., Derose R., Derzelle S., Freyssinet G., Gaudriault S., Médigue C., Lanois A., Powell K., Siguier P., Vincent R., Wingate V., Zouine M., Glaser P., Boemare N., Danchin A., and Kunst F. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat. Biotechnol. 21 (2003) 1307-1313
20. Pukatzki S., McAuley S.B., and Miyata S.T. The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12 (2009) 11-17
21. Waterfield N., Sanchez-Contreras M., Eleftherianos I., Dowling A., Yang G., Wilkinson P., Parkhill J., Thomson N., Reynolds S.E., Bode H.B., Dorus S., and Ffrench-Constant R.H. Rapid Virulence Annotation (RVA): identification of virulence factors using a bacterial genome library and multiple invertebrate hosts. Proc. Natl. Acad. Sci. U S A 105 (2008) 15967-15972
22. Ma A.T., McAuley S., Pukatzki S., and Mekalanos J.J. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5 (2009) 234-243
23. Fauvart M., and Michiels J. Rhizobial secreted proteins as determinants of host specificity in the Rhizobium-legume symbiosis. FEMS Microbiol. Lett. 285 (2008) 1-9
24. Mueller C.A., Broz P., and Cornelis G.R. The type III secretion system tip complex and translocon. Mol. Microbiol. 68 (2008) 1085-1095
25. Tounsi S., Blight M., Jaoua S., and de Lima Pimenta A. From insects to human hosts: identification of major genomic differences between entomopathogenic strains of Photorhabdus and the emerging human pathogen Photorhabdus asymbiotica. Int. J. Med. Microbiol. 296 (2006) 521
26. Yarbrough M.L., Li Y., Kinch L.N., Grishin N.V., Ball H.L., and Orth K. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323 (2009) 269-272
27. Brugirard-Ricaud K., Givaudan A., Parkhill J., Boemare N., Kunst F., Zumbihl R., and Duchaud E. Variation in the effectors of the type III secretion system among Photorhabdus species as revealed by genomic analysis. J. Bacteriol. 186 (2004) 4376-4381
28. Samba-Louaka A., Taieb F., Nougayrède J.P., and Oswald E. Cif type III effector protein: a smart hijacker of the host cell cycle. Future Microbiol. 4 (2009) 867-877
29. Jubelin G., Chavez C.V., Taieb F., Banfield M.J., Samba-Louaka A., Nobe R., et al. Cycle inhibiting factors (CIFs) are a growing family of functional cyclomodulins present in invertebrate and mammal bacterial pathogens. PLoS ONE 4 (2009) e4855
30. Yang G., Dowling A.J., Gerike U., Ffrench-Constant R.H., and Waterfield N.R. Photorhabdus virulence cassettes confer injectable insecticidal activity against the wax moth. J. Bacteriol. 188 (2006) 2254-2261
31. Shao F., Merritt P.M., Bao Z., Innes R.W., and Dixon J.E. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109 (2002) 575-588
32. Iriarte M., and Cornelis G.R. YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. 29 (1998) 915-929
33. Brugirard-Ricaud K., Duchaud E., Givaudan A., Girard P.A., Kunst F., Boemare N., et al. Site-specific antiphagocytic function of Photorhabdus luminescens type III secretion system associated to Yersinia YopT homologues expression during insect colonization. Cell. Microbiol. 7 (2004) 363-371
34. Hsu Y., Jubelin G., Taieb F., Nougayrède J.P., Oswald E., and Stebbins C.E. Structure of the cyclomodulin Cif from pathogenic Escherichia coli. J. Mol. Biol. 384 (2008) 465-477
35. Yao Q., Cui J., Zhu Y., Wang G., Hu L., Long C., Cao R., Liu X., Huang N., Chen S., Liu L., and Shao F. A bacterial type III effector family uses the papain-like hydrolytic activity to arrest the host cell cycle. Proc. Natl. Acad. Sci. U S A 106 (2009) 3716-3721
36. Crow A., Race P.R., Jubelin G., Varela Chavez C., Escoubas J.M., Oswald E., and Banfield M.J. Crystal structures of Cif from bacterial pathogens Photorhabdus luminescens and Burkholderia pseudomallei. PLoS ONE 4 (2009) e5582
37. Costa S.C.P., Girard P.A., Brehélin M., and Zumbihl R. The emerging human pathogen Photorhabdus asymbiotica is a facultative intracellular bacterium and induces apoptosis of macrophage-like cells. Infect. Immun. 77 (2009) 1022-1030
38. Ciche T.A., Kim K.S., Kaufmann-Daszczuk B., Nguyen K.C., and Hall D.H. Cell invasion and matricide during Photorhabdus luminescens transmission by Heterorhabditis bacteriophora nematodes. Appl. Environ. Microbiol. 74 (2008) 2275-2287
39. Marcus S.L., Knodler L.A., and Finlay B.B. Salmonella enteric serovar Typhimurium effector SigD/SopB is membrane-associated and ubiquitinated inside host cells. Cell. Microbiol. 4 (2002) 435-446
40. Engel J., and Balachandran P. Role of Pseudomonas aeruginosa type III effectors in disease. Curr. Opin. Microbiol. 12 (2009) 61-66
41. Pukatzki S., Kessin R.H., and Mekalanos J.J. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc. Natl. Acad. Sci. U S A 99 (2002) 3159-3164
42. Abd H., Wretlind B., Saeed A., and Dsund I. Pseudomonas aeruginosa utilises its type III secretion system to kill the free-living amoeba Acanthamoeba castellanii. J. Eukaryot. Microbiol. 55 (2008) 235-243
43. VanRheenen S.M., Luo Z.Q., O'Connor T., and Isberg R.R. Members of a Legionella pneumophila family of proteins with ExoU (phospholipase A) active sites are translocated to target cells. Infect. Immun. 74 (2006) 3597-3606
44. Chowdhury I., Tharakan B., and Bhat G.K. Current concepts in apoptosis: the physiological suicide program revisited. Cell. Mol. Biol. Lett. 11 (2006) 506-525
45. Zychlinsky A., Prevost M.C., and Sansonetti P.J. Shigella flexneri induces apoptosis in infected macrophages. Nature 358 (1992) 167-169
46. Ruckdeschel K., Roggenkamp A., Lafont V., Mangeat P., Heesemann J., and Rouot B. Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis. Infect. Immun. 65 (1997) 4813-4821
47. Ruckdeschel K., Harb S., Roggenkamp A., Hornef M., Zumbihl R., Köhler S., Heesemann J., and Rouot B. Yersinia enterocolitica impairs activation of transcription factor NF κB: involvement in the induction of programmed cell death and in the suppression of the macrophage tumor necrosis factor α production. J. Exp. Med. 187 (1998) 1069-1079
48. Monack D.M., Mecsas J., Bouley D., and Falkow S. Yersinia-induced apoptosis in vivo aids in the establishment of a systemic infection of mice. J. Exp. Med. 188 (1998) 2127-2137
49. Gao L., and Abu Kwaik Y. Hijacking of apoptotic pathways by bacterial pathogens. Microbes Infect. 2 (2000) 1705-1719
50. Chang H.Y., and Yang X. Proteases for cell suicide: functions and regulation of caspases. Microbiol. Mol. Biol. Rev. 64 (2000) 821-846
51. Vigneux F., Zumbihl R., Jubelin G., Ribeiro C., Poncet J., Baghdiguian S., Givaudan A., and Brehèlin M. The xaxAB genes encoding a new apoptotic toxin from the insect pathogen Xenorhabdus nematophila are present in plant and human pathogens. J. Biol. Chem. 282 (2007) 9571-9580
52. Brillard J., Ribeiro C., Boemare N., Brehélin M., and Givaudan A. Two distinct, hemolytic activities in Xenorhabdus nematophila are active against immunocompetent insect cells. Appl. Environ. Microbiol. 67 (2001) 2515-2525
53. Daborn P.J., Waterfield N., Silva C.P., Au C.P., Sharma S., and Ffrench-Constant R.H. A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc. Natl. Acad. Sci. U S A 99 (2002) 10742-10747
54. Dowling A.J., Daborn P.J., Waterfield N., Wang P., Streuli C.H., and Ffrench-Constant R.H. The insecticidal toxin Makes caterpillars floppy (Mcf) promotes apoptosis in mammalian cells. Cell. Microbiol. 6 (2004) 345-353
55. Vlisidou I., Dowling A.J., Evans I.R., Waterfield N., Ffrench-Constant R.H., and Wood W. Drosophila embryos as model systems for monitoring bacterial infection in real time. PLoS Pathog. 7 (2009) e1000518
56. Denecker G., Declercq W., Geuijen C.A., Boland A., Benabdillah R., van Gurp M.P., Sory M.P., Vandenabeele P., and Cornelis G.R. Yersinia enterocolitica YopP-induced apoptosis of macrophages involves the apoptotic signaling cascade upstream of bid. J. Biol. Chem. 276 (2001) 19706-19714
57. Samba-Louaka A., Nougayrède J.P., Watrin C., Oswald E., and Taieb F. The EPEC effector Cif induces delayed apoptosis in epithelial cells. Infect. Immun. 77 (2009) 5471-5477