The pseudomonas aeruginosa type III secretion system has an exotoxin S/T/Y independent pathogenic role during acute lung infection

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Galle, Marlies ^a,b   Jin, Shouguang ^c   Bogaert, Pieter ^a,b   Haegman, Mira ^a,b   Vandenabeele, Peter ^a,b   Beyaert, Rudi ^a,b  

^a GHENT UNIVERSITY   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CASPASE 3; EXOTOXIN S; EXOTOXIN T; EXOTOXIN Y; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN POPB; PSEUDOMONAS EXOTOXIN; UNCLASSIFIED DRUG;

ACUTE LUNG INFECTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS MACROPHAGE; LUNG INFECTION; MEMBRANE PERMEABILITY; MORTALITY; MOUSE; NONHUMAN; PSEUDOMONAS AERUGINOSA; TYPE III SECRETION SYSTEM;

ACUTE DISEASE; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL DEATH; CELL LINE; EXOTOXINS; FEMALE; INTERLEUKIN-1BETA; LUNG; LUNG DISEASES; MACROPHAGES; MICE; MICE, INBRED C57BL; MUTATION; POROSITY; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS;

BACTERIA (MICROORGANISMS); EUKARYOTA; MURINAE; MUS; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 84864200181     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041547     Document Type: Article

References (55)

1. Garau J, Gomez L, (2003) Pseudomonas aeruginosa pneumonia. Curr Opin Infect Dis 16: 135-143.
2. Valencia M, Torres A, (2009) Ventilator-associated pneumonia. Curr Opin Crit Care 15: 30-35.
3. Lyczak JB, Cannon CL, Pier GB, (2002) Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15: 194-222.
4. Galán JE, Collmer A, (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322-1328.
5. Hueck CJ, (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
6. Hauser AR, (2009) The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol 7: 654-665.
7. Sundin C, Wolfgang MC, Lory S, Forsberg A, Frithz-Lindsten E, (2002) Type IV pili are not specifically required for contact dependent translocation of exoenzymes by Pseudomonas aeruginosa. Microb Pathog 33: 265-277.
8. Goure J, Pastor A, Faudry E, Chabert J, Dessen Aa, et al. (2004) The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes. Infect Immun 72: 4741-4750.
9. Ryndak MB, Chung H, London E, Bliska JB, (2005) Role of predicted transmembrane domains for type III translocation, pore formation, and signaling by the Yersinia pseudotuberculosis YopB protein. Infect Immun 73: 2433-2443.
10. Bröms JE, Forslund AL, Forsberg A, Francis MS, (2003) PcrH of Pseudomonas aeruginosa is essential for secretion and assembly of the type III translocon. J Infect Dis 188: 1909-1921.
11. Dacheux D, Goure J, Chabert J, Usson Y, Attree I, (2001) Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa-infected macrophages. Mol Microbiol 40: 76-85.
12. Goure J, Broz P, Attree O, Cornelis GR, Attree I, (2005) Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes. J Infect Dis 192: 218-225.
13. Urbanowski ML, Brutinel ED, Yahr TL, (2007) Translocation of ExsE into Chinese hamster ovary cells is required for transcriptional induction of the Pseudomonas aeruginosa type III secretion system. Infect Immun 75: 4432-4439.
14. Engel J, Balachandran P, (2009) Role of Pseudomonas aeruginosa type III effectors in disease. Curr Opin Microbiol 12: 61-66.
15. Barbieri JT, Sun J, (2004) Pseudomonas aeruginosa ExoS and ExoT. Rev Physiol Biochem Pharmacol 152: 79-92.
16. Galle M, Schotte P, Haegman M, Wullaert A, Yang HJ, et al. (2008) The Pseudomonas aeruginosa Type III secretion system plays a dual role in the regulation of caspase-1 mediated IL-1beta maturation. J Cell Mol Med 12: 1767-1776.
17. Cowell BA, Evans DJ, Fleiszig SMJ, (2005) Actin cytoskeleton disruption by ExoY and its effects on Pseudomonas aeruginosa invasion. FEMS Microbiol Lett 250: 71-76.
18. Arnoldo A, Curak J, Kittanakom S, Chevelev I, Lee VT, et al. (2008) Identification of small molecule inhibitors of Pseudomonas aeruginosa exoenzyme S using a yeast phenotypic screen. PLoS Genet 4: e1000005.
19. Sitkiewicz I, Stockbauer KE, Musser JM, (2007) Secreted bacterial phospholipase A2 enzymes: better living through phospholipolysis. Trends Microbiol 15: 63-69.
20. Anderson DM, Schmalzer KM, Sato H, Casey M, Terhune SS, et al. (2011) Ubiquitin and ubiquitin-modified proteins activate the Pseudomonas aeruginosa T3SS cytotoxin, ExoU. Mol Microbiol 82: 1452-1467.
21. Feltman H, Schulert G, Khan S, Jain M, Peterson L, et al. (2001) Prevalence of type III secretion genes in clinical and environmental isolates of Pseudomonas aeruginosa. Microbiology 147: 2659-2669.
22. Viboud GI, Bliska JB, (2005) Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59: 69-89.
23. Shin H, Cornelis GR, (2007) Type III secretion translocation pores of Yersinia enterocolitica trigger maturation and release of pro-inflammatory IL-1beta. Cell Microbiol 9: 2893-2902.
24. Zhao Y, Yang J, Shi J, Gong YN, Lu Q, et al. (2011) The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477: 596-600.
25. Kofoed EM, Vance RE, (2011) Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477: 592-595.
26. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, et al. (2010) Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci U S A 107: 3076-3080.
27. Poot M, Gibson LL, Singer VL, (1997) Detection of apoptosis in live cells by MitoTracker red CMXRos and SYTO dye flow cytometry. Cytometry 27: 358-364.
28. van Genderen H, Kenis H, Lux P, Ungeth L, Maassen C, et al. (2006) In vitro measurement of cell death with the annexin A5 affinity assay. Nat Protoc 1: 363-367.
29. Schultz MJ, Rijneveld AW, Florquin S, Edwards CK, Dinarello CA, et al. (2002) Role of interleukin-1 in the pulmonary immune response during Pseudomonas aeruginosa pneumonia. Am J Physiol Lung Cell Mol Physiol 282: L285-290.
30. Wangdi T, Mijares LA, Kazmierczak BI, (2010) In vivo discrimination of type 3 secretion system-positive and-negative Pseudomonas aeruginosa via a caspase-1-dependent pathway. Infect Immun 78: 4744-4753.
31. Kooguchi K, Hashimoto S, Kobayashi A, Kitamura Y, Kudoh I, et al. (1998) Role of alveolar macrophages in initiation and regulation of inflammation in Pseudomonas aeruginosa pneumonia. Infect Immun 66: 3164-3169.
32. Ader F, Le Berre R, Faure K, Gosset P, Epaulard O, et al. (2005) Alveolar response to Pseudomonas aeruginosa: role of the type III secretion system. Infect Immun 73: 4263-4271.
33. Ojielo CI, Cooke K, Mancuso P, Standiford TJ, Olkiewicz KM, et al. (2003) Defective phagocytosis and clearance of Pseudomonas aeruginosa in the lung following bone marrow transplantation. J Immunol 171: 4416-4424.
34. Marriott HM, Dockrell DH, (2007) The role of the macrophage in lung disease mediated by bacteria. Exp Lung Res 33: 493-505.
35. Faure K, Sawa T, Ajayi T, Fujimoto J, Moriyama K, et al. (2004) TLR4 signaling is essential for survival in acute lung injury induced by virulent Pseudomonas aeruginosa secreting type III secretory toxins. Respir Res 5: 1.
36. Roy-Burman A, Savel RH, Racine S, Swanson BL, Revadigar NS, et al. (2001) Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J Infect Dis 183: 1767-1774.
37. Hauser AR, Cobb E, Bodi M, Mariscal D, Vallés J, et al. (2002) Type III protein secretion is associated with poor clinical outcomes in patients with ventilator-associated pneumonia caused by Pseudomonas aeruginosa. Crit Care Med 30: 521-528.
38. Fink SL, Cookson BT, (2005) Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73: 1907-1916.
39. Usher LR, Lawson RA, Geary I, Taylor CJ, Bingle CD, et al. (2002) Induction of neutrophil apoptosis by the Pseudomonas aeruginosa exotoxin pyocyanin: a potential mechanism of persistent infection. J Immunol 168: 1861-1868.
40. Allen L, Dockrell DH, Pattery T, Lee DG, Cornelis P, et al. (2005) Pyocyanin production by Pseudomonas aeruginosa induces neutrophil apoptosis and impairs neutrophil-mediated host defenses in vivo. J Immunol. 174: 3643-3649.
41. Vance RE, Rietsch A, Mekalanos JJ, (2005) Role of the type III secreted exoenzymes S, T, and Y in systemic spread of Pseudomonas aeruginosa PAO1 in vivo. Infect Immun 73: 1706-1713.
42. Lee VT, Smith RS, Tümmler B, Lory S, (2005) Activities of Pseudomonas aeruginosa effectors secreted by the Type III secretion system in vitro and during infection. Infect Immun 73: 1695-1705.
43. Shafikhani SH, Morales C, Engel J, (2008) The Pseudomonas aeruginosa type III secreted toxin ExoT is necessary and sufficient to induce apoptosis in epithelial cells. Cell Microbiol 10: 994-1007.
44. Viboud GI, So SSK, Ryndak MB, Bliska JB, (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.
45. Chen Y, Smith MR, Thirumalai K, Zychlinsky A, (1996) A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J 15: 3853-3860.
46. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, et al. (1999) The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96: 2396-2401.
47. Imamura Y, Yanagihara K, Fukuda Y, Kaneko Y, Seki M, et al. (2007) Effect of anti-PcrV antibody in a murine chronic airway Pseudomonas aeruginosa infection model. Eur Respir J 29: 965-968.
48. François B, Luyt CE, Dugard A, Wolff M, Diehl JL, et al. (2012) Safety and pharmacokinetics of an anti-PcrV PEGylated monoclonal antibody fragment in mechanically ventilated patients colonized with Pseudomonas aeruginosa: A randomized, double-blind, placebo-controlled trial. Crit Care Med 40: 1-7.
49. Lee VT, Pukatzki S, Sato H, Kikawada E, Kazimirova AA, et al. (2007) Pseudolipasin A is a specific inhibitor for phospholipase A2 activity of Pseudomonas aeruginosa cytotoxin ExoU. Infect Immun 75: 1089-1098.
50. Aiello D, Williams JD, Majgier-Baranowska H, Patel I, Peet NP, et al. (2010) Discovery and characterization of inhibitors of Pseudomonas aeruginosa type III secretion. Antimicrob Agents Chemother 54: 1988-1999.
51. Kaufman MR, Jia J, Zeng L, Ha U, Chow M, et al. (2000) Pseudomonas aeruginosa mediated apoptosis requires the ADP-ribosylating activity of exoS. Microbiology 146: 2531-2541.
52. Yang H, Shan Z, Kim J, Wu W, Lian W, et al. (2007) Regulatory role of PopN and its interacting partners in type III secretion of Pseudomonas aeruginosa. J Bacteriol 189: 2599-2609.
53. Desmedt M, Rottiers P, Dooms H, Fiers W, Grooten J, (1998) Macrophages induce cellular immunity by activating Th1 cell responses and suppressing Th2 cell responses. J Immunol 160: 5300-5308.
54. Sawa T, Ohara M, Kurahashi K, Twining SS, Frank DW, et al. (1998) In vitro cellular toxicity predicts Pseudomonas aeruginosa virulence in lung infections. Infect Immun 66: 3242-3249.
55. Wullaert A, Wielockx B, Van Huffel S, Bogaert V, De Geest B, et al. (2005) Adenoviral gene transfer of ABIN-1 protects mice from TNF/galactosamine-induced acute liver failure and lethality. Hepatology 42: 381-389.