The Pseudomonas aeruginosa Type III secretion system plays a dual role in the regulation of caspase-1 mediated IL-1β maturation

Journal of Cellular and Molecular Medicine

Volumn 12, Issue 5A, 2008, Pages 1767-1776

  Galle, M ^a,b   Schotte, P ^a,b   Haegman, M ^a,b   Wullaert, A ^a,b   Yang, H J ^c   Jin, S ^c   Beyaert, R ^a,b  

^a GHENT UNIVERSITY   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Caspases; Interleukin 1; Lung inflammation; Pseudomonas; Type III secretion

Indexed keywords

BACTERIAL TOXIN; EXOENZYME S; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ANIMAL; APOPTOSIS; ARTICLE; CELL CULTURE; CYTOLOGY; DBA MOUSE; FEMALE; GENETICS; MACROPHAGE; METABOLISM; MOUSE; PATHOLOGY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; SECRETION;

ADP RIBOSE TRANSFERASES; ANIMALS; APOPTOSIS; BACTERIAL TOXINS; CASPASE 1; CELLS, CULTURED; FEMALE; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, INBRED DBA; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS;

BACTERIA (MICROORGANISMS); MURINAE; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 54049100347     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2007.00190.x     Document Type: Article

References (37)

1. Garau J, Gomez L. Pseudomonas aeruginosa pneumonia. Curr Opin Infect Dis. 2003 16 : 135 43.
2. Hauser AR, Cobb E, Bodi M, Mariscal D, Valles J, Engel JN, Rello J. Type III protein secretion is associated with poor clinical outcomes in patients with ventilator-associated pneumonia caused by Pseudomonas aeruginosa. Crit Care Med. 2002 30 : 521 8.
3. Hueck CJ. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev. 1998 62 : 379 433.
4. Ahuja N, Kumar P, Bhatnagar R. The adenylate cyclase toxins. Crit Rev Microbiol. 2004 30 : 187 96.
5. Sato H, Frank D. W. ExoU is a potent intra-cellular phospholipase. Mol Microbiol. 2004 53 : 1279 90.
6. Barbieri JT, Sun J. Pseudomonas aeruginosa ExoS and ExoT. Rev Physiol Biochem Pharmacol. 2004 152 : 79 92.
7. Kaufman MR, Jia J, Zeng L, Ha U, Chow M, Jin S. Pseudomonas aeruginosa mediated apoptosis requires the ADP-ribo-sylating activity of exoS. Microbiology. 2000 146 : 2531 41.
8. Dinarello CA. Interleukin-1 beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann N Y Acad Sci. 1998 856 : 1 11.
9. Martinon F, Tschopp J. Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ. 2007 14 : 10 22.
10. Yang H, Shan Z, Kim J, Wu W, Lian W, Zeng L, Xing L, Jin S. Regulatory role of PopN and its interacting partners in Type III secretion of Pseudomonas aeruginosa. J Bacteriol. 2007 189 : 2599 609.
11. Dasgupta N, Wolfgang MC, Goodman AL Arora SK, Jyot J, Lory S, Ramphal R. A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol. Microbiol. 2003 50 : 809 24.
12. Desmedt M, Rottiers P, Dooms H, Fiers W, Grooten J. Macrophages induce cellular immunity by activating Th1 cell responses and suppressing Th2 cell responses. J Immunol. 1998 160 : 5300 8.
13. Sawa T, Ohara M, Kurahashi K, Twining SS, Frank DW, Doroques DB, Long T, Gropper MA, Wiener-Kronish JP. In vitro cellular toxicity predicts Pseudomonas aeruginosa virulence in lung infections. Infect Immun. 1998 66 : 3242 9.
14. Schotte P Denecker G, Van Den Broeke A, Vandenabeele P, Cornells GR, Beyaert R. Targeting Rac1 by the Yersinia effector protein YopE inhibits Caspase-1-mediated maturation and release of Interleukin-1β. J Biol Chem. 2004 279 : 25134 42.
15. Wullaert A, Wielockx B, Van Huffel S, Bogaert V De Geest B, Papeleu P, Schotte P, El Bakkouri K, Heyninck K, Libert C, Beyaert R. Adenoviral gene transfer of ABIN-1 protects mice from TNF/ galactosamine-induced acute liver failure and lethality. Hepatology. 2005 42 : 381 9.
16. Grooten J, Goossens V, Vanhaesebroeck B, Fiers W. Cell membrane permeabilization and cellular collapse, followed by loss of dehydrogenase activity: early events in tumour necrosis factor-induced cytotoxicity. Cytokine. 1993 5 : 546 55.
17. Martinon F, Agostini L, Meylan E, Tschopp J. Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr Biol. 2004 14 : 1929 34.
18. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A. The Salmonella invasin SipB induces macrophage apoptosis by binding to Caspase-1. Proc Natl Acad Sci USA. 1999 96 : 2396 2401.
19. Chen Y, Smith MR, Thirumalai K, Zychlinsky A. A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J. 1996 15 : 3853 60.
20. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, Aderem A. Cytoplasmic Flagellin activates Caspase-1 and secretion of interleukin 1βvia Ipaf. Nat Immunol. 2006 7 : 569 75.
21. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozoren N, Jagirdar R, Inohara N, Vandenabeele P, Bertin J, Coyle A, Grant EP, Nunez G. Cytosolic Flagellin requires Ipaf for activation of Caspase-1 and interleukin 1β in Salmonella-infected macrophages. Nat Immunol. 2006 7 : 576 82.
22. Fink SL, Cookson BT. Apoptosis, pyropto-sis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun. 2005 73 : 1907 16.
23. Roy-Burman A, Savel RH, Racine S, Swanson BL, Revadigar NS, Fujimoto J, Sawa T, Frank DW, Wiener-Kronish JP. Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J Infect Dis. 2001 183 : 1767 74.
24. Shaver CM, Hauser AR. Relative contributions of Pseudomonas aeruginosa ExoU ExoS, and ExoT to virulence in the lung. Infect Immun. 2004 72 : 6969 77.
25. Krall R, Sun J, Pederson KJ, Barbieri JT. In vivo rho GTPase-activating protein activity of Pseudomonas aeruginosa cyto-toxin ExoS. Infect Immun. 2002 70 : 360 7.
26. Epelman S, Stack D, Bell C, Wong E, Neely GG, Krutzik S, Miyake K, Kubes P, Zbytnuik LD, Ma LL, Xie X, Woods DE, Mody CH. Different domains of Pseudomonas aeruginosa Exoenzyme S activate distinct TLRs. J Immunol. 2004 173 : 2031 40.
27. Reiniger N, Lee MM, Coleman FT, Ray C, Golan DE, Pier GB. Resistance to Pseudomonas aeruginosa chronic lung infection requires cystic fibrosis trans-membrane conductance regulator-modulated Interleukin-1 (IL-1) release and signaling through the IL-1 receptor. Infect Immun. 2007 75 : 1598 608.
28. Horino T, Matsumoto T, Uramatsu M, Tanabe M, Tateda K, Miyazaki S, Nakane A, Iwakura Y, Yamaguchi K. Interleukin-1-deficient mice exhibit high sensitivity to gut-derived sepsis caused by Pseudomonas aeruginosa. Cytokine. 2005 30 : 339 46.
29. Schultz MJ, Rijneveld AW, Florquin S, Edwards CK, Dinarello CA, Van der Poll T. Role of Interleukin-1 in the pulmonary immune response during Pseudomonas aeruginosa pneumonia. Am J Physiol Lung Cell Mol Physiol. 2002 282 : L285 90.
30. DiNovo AA, Schey KL, Vachon WS, McGuffie EM, Olson JC, Vincent TS. ADP-ribosylation of Cyclophilin A by Pseudomonas aeruginosa Exoenzyme S. Biochemistry. 2006 45 : 4664 73.
31. Kanneganti TD, Lamkanfi M, Kim YG, Chen G, Park JH, Franchi L, Vandenabeele P, Nunez G. Pannexin-1-mediated recognition of bacterial molecules activates the Cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity. 2007 26 : 433 43.
32. Shin H, Cornells GR. Type III secretion translocation pores of Yersinia enterocolitica trigger maturation and release of pro-inflammatory IL-1β. Cell Microbiol. 2007 9 : 2893 902.
33. Blocker A, Komoriya K, Aizawa S. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc Natl Acad Sci USA. 2003 100 : 3027 30.
34. Sun YH, Rolan HG, Tsolis RM. Injection of Flagellin into the host cell cytosol by Salmonella enterica serotype typhimurium. J Biol Chem. 2007 282 : 33897 901.
35. Solle M, Labasi J, Perregaux DG, Stam E, Petrushova N, Koller BH, Griffiths RJ, Gabel CA. Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem. 2001 276 : 125 32.
36. Franchi L, Stoolman J, Kanneganti TD, Verma A, Ramphal R, Núñez G. Critical role for Ipaf in Pseudomonas aeruginosa-induced Caspase-1 activation. Eur J Immunol. 2007 37 : 3030 9.
37. Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR. A Type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature. 2007 447 : 284 8.