Pseudomonas aeruginosa toxin ExoU induces a PAF-dependent impairment of alveolar fibrin turnover secondary to enhanced activation of coagulation and increased expression of plasminogen activator inhibitor-1 in the course of mice pneumosepsis

Respiratory Research

Volumn 12, Issue , 2011, Pages

  Machado, Gloria Beatriz ^a   de Oliveira, Albanita V ^a   Saliba, Alessandra M ^a   de Lima, Carolina D M ^a   Suassuna, José H R ^a   Plotkowski, Maria Cristina ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Acute respiratory distress syndrome; ExoU; Plasminogen activator inhibitor type I (PAI 1); Platelet activating factor (PAF); Pseudomonas aeruginosa; sepsis

Indexed keywords

BACTERIAL TOXIN; EXOU TOXIN; FIBRIN; INTERLEUKIN 6; MESSENGER RNA; PLASMINOGEN ACTIVATOR INHIBITOR 1; THROMBOCYTE ACTIVATING FACTOR; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PSEUDOMONAS EXOPROTEIN A PROTEIN, PSEUDOMONAS AERUGINOSA; SERPINE1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM MUTANT; BLOOD CLOTTING; CELL LEVEL; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; FIBRINOLYSIS; GENE DELETION; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATION; LUNG BLOOD VESSEL; LUNG LAVAGE; LUNG PARENCHYMA; MACROPHAGE; MICROVASCULATURE; MOUSE; NONHUMAN; PNEUMOSEPSIS; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RESPIRATORY EPITHELIUM; SEPSIS; ANIMAL; BACTERIAL PNEUMONIA; BLOOD; CHEMISTRY; DISEASE MODEL; GENETICS; HUMAN; LUNG ALVEOLUS; METABOLISM; MICROBIOLOGY; MUTATION; RESPIRATORY TRACT MUCOSA; TIME; TUMOR CELL LINE; UPREGULATION;

ANIMALS; BACTERIAL PROTEINS; BLOOD COAGULATION; BRONCHOALVEOLAR LAVAGE FLUID; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FEMALE; FIBRIN; HUMANS; IMMUNOHISTOCHEMISTRY; MACROPHAGES; MICE; MUTATION; PLASMINOGEN ACTIVATOR INHIBITOR 1; PLATELET ACTIVATING FACTOR; PNEUMONIA, BACTERIAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; PULMONARY ALVEOLI; RESPIRATORY MUCOSA; RNA, MESSENGER; SEPSIS; TIME FACTORS; UP-REGULATION;

EID: 79961123815     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-12-104     Document Type: Article

References (36)

1. Martin GS, Bernard GR. Airway and lung in sepsis. Intensive Care Med 2001, 27(suppl 1):S63-S79.
2. Schultz MJ, Levi M. Pulmonary coagulopathy: a potential therapeutic target in different forms of lung injury. Thorax 2000, 62:563-564.
3. Seeger W, Hübel J, Klapettek K, Pison U, Obertacke U, Joka T, Roka L. Procoagulant activity in bronchoalveolar lavage of severely traumatized patients - relation to the development of acute respiratory distress. Thromb Res 1991, 61:53-64.
4. Levi M, van der Poll T. Two-way interactions between inflammation and coagulation. Trends Cardiovasc Med 2005, 15:254-259. 10.1016/j.tcm.2005.07.004, 16226680.
5. Prabhakaran P, Ware L, White K, Cross M, Matthay M, Olman M. Elevated levels of plasminogen activator inhibitor-1 in pulmonary edema fluid are associated with mortality in acute lung injury. Am J Physiol Lung Cell Mol Physiol 2003, 285:L20-L28.
6. Scheetz MH, Pharm D, Hoffman M, Bolon MK, Schulert G, Estrellado W, Baraboutis IG, Sriram P, Dinh M, Owens LK, Hauser AR. Morbidity associated with Pseudomonas aeruginosa bloodstream infections. Diagn Microbiol Infect Dis 2009, 64:311-319. 10.1016/j.diagmicrobio.2009.02.006, 2693471, 19345039.
7. Sato H, Frank DW. ExoU is a potent intracellular phospholipase. Mol Microbiol 2004, 53:1279-1290. 10.1111/j.1365-2958.2004.04194.x, 15387809.
8. Feltman HG, Schulert G, Khan S, Jain M, Peterson L, Hauser AR. Prevalence of type III secretion genes in clinical and environmental isolates of Pseudomonas aeruginosa. Microbiology 2001, 147:2659-2669.
9. Hurley BP, McCormick BA. Multiple roles of phospholipase A2 during lung infection and inflammation. Infect Immun 2008, 76:2259-2272. 10.1128/IAI.00059-08, 2423084, 18411286.
10. Yost CC, Weyrich AS, Zimmerman GA. The platelet Activating factor (PAF) signaling cascade in systemic inflammatory responses. Biochimie 2010, 92:692-697. 10.1016/j.biochi.2010.02.011, 2878918, 20167241.
11. Zimmerman GA, McIntyre TM, Prescott SM, Stafforini DM. The platelet-activating factor signaling system and its regulators in syndromes of inflammation and thrombosis. Crit Care Med 2002, 30:S294-301. 10.1097/00003246-200205001-00020, 12004251.
12. Mathiak G, Szewczyk D, Abdullah F, Ovadia P, Rabinovici R. Platelet-activating factor in experimental and clinical sepsis. Shock 1997, 7:391-404. 10.1097/00024382-199706000-00001, 9185238.
13. Touqui L, Hatmi M, Vargaftig BB. Human platelets stimulated by thrombin produce platelet-activating factor (1-O-alkyl-2-acetyl-sn-glycero-3-phosphocholine) when the degrading enzyme acetyl hydrolase is blocked. Biochem J 1985, 229:811-6. 1145129, 4052028.
14. Howard KM, Miller JE, Miwa M, Olson MS. Cell-specific regulation of expression of plasma-type platelet-activating factor acetylhydrolase in the liver. J Biol Chem 1997, 272:27543-27548. 10.1074/jbc.272.44.27543, 9346888.
15. Cao Y, Stafforini DM, Zimmerman GA, McIntyre TM, Prescott SM. Expression of plasma platelet-activating factor acetylhydrolase is transcriptionally regulated by mediators of inflammation. J Biol Chem 1998, 273:4012-4020. 10.1074/jbc.273.7.4012, 9461591.
16. Saliba AM, Nascimento DO, Silva MC, Assis MC, Gayer CR, Raymond B, Coelho MG, Marques EA, Touqui L, Albano RM, Lopes UG, Paiva DD, Bozza PT, Plotkowski MC. Eicosanoid-mediated proinflammatory activity of Pseudomonas aeruginosa ExoU. Cell Microbiol 2005, 7:1811-1822. 10.1111/j.1462-5822.2005.00635.x, 16309466.
17. Plotkowski MC, Brandão BA, Assis MC, Feliciano LFP, Saliba AM, Raymond B, Marques EA, Zahm JM, Touqui L, Bozza PT. Lipid body mobilization in the ExoU-induced release of inflammatory mediators by airway epithelial. Microbial Pathogenesis 2008, 45:30-37. 10.1016/j.micpath.2008.01.008, 18486438.
18. Plotkowski MC, Feliciano LF, Machado GB, Cunha LG, Freitas C, Saliba AM, de Assis MC. ExoU-induced procoagulant activity in Pseudomonas aeruginosa-infected airway cells. Eur Respir J 2008, 32:1591-1598. 10.1183/09031936.00086708, 18684846.
19. Machado GB, de Assis MC, Leão R, Saliba AM, Silva MC, Suassuna JH, de Oliveira AV, Plotkowski MC. ExoU-induced vascular hyperpermeability and platelet activation in the course of experimental Pseudomonas aeruginosa pneumosepsis. Shock 2010, 33:315-321. 10.1097/SHK.0b013e3181b2b0f4, 19543153.
20. Ottino P, Taheri F, Bazan HE. Platelet-activating factor induces the gene expression of TIMP-1, -2, and PAI-1: imbalance between the gene expression of MMP-9 and TIMP-1 and -2. Exp Eye Res 2002, 74:393-402. 10.1006/exer.2001.1135, 12014920.
21. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, Tada K. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer 1980, 26:171-176. 10.1002/ijc.2910260208, 6970727.
22. Howard KM, Abdel-Al M, Ditmyer M, Patel N. Lipopolysaccharide and platelet-activating factor stimulate expression of platelet-activating factor acetylhydrolase via distinct signaling pathways. Inflamm Res 2011, 60:735-744. 10.1007/s00011-011-0326-5, 21432021.
23. Schulert GS, Feltman H, Rabin SDP, Martin CG, Battle SE, Rello J, Hauser AR. Secretion of the toxin ExoU is a marker for highly virulent Pseudomonas aeruginosa isolates obtained from patients with hospital-acquired pneumonia. J Infect Dis 2003, 188:1695-1706. 10.1086/379372, 14639541.
24. Idell S, James KK, Levin EG, Schwartz BS, Manchanda N, Maunder RJ, Martin TR, McLarty J, Fair DS. Local abnormalities in coagulation and fibrinolytic pathways predispose to alveolar fibrin deposition in the adult respiratory distress syndrome. J Clin Invest 1989, 84:695-705. 10.1172/JCI114217, 548934, 2788176.
25. Bastarache JA, Wang L, Geiser T, Wang Z, Albertine KH, Matthay MA, Ware LB. The alveolar epithelium can initiate the extrinsic coagulation cascade through expression of tissue factor. Thorax 2007, 62:608-616. 10.1136/thx.2006.063305, 2117249,2117249, 17356058.
26. Bastarache JA, Wang L, Wang Z, Albertine KH, Matthay MA, Ware LB. Intra-alveolar tissue factor pathway inhibitor is not sufficient to block tissue factor procoagulant activity. Am J Physiol Lung Cell Mol Physiol 2008, 294:L874-L881. 10.1152/ajplung.00372.2007, 2764534, 18310227.
27. Higuchi DA, Wun TC, Likert KM, Broze GJ. The effect of leukocyte elastase on tissue factor pathway inhibitor. Blood 1992, 79:1712-1719.
28. Belaaouaj AA, Li A, Wun TC, Welgus HG, Shapiro SD. Matrix metalloproteinases cleave tissue factor pathway inhibitor. Effects on coagulation. J Biol Chem 2000, 275:27123-128.
29. Gando S, Kameue T, Matsuda N, Hayakawa M, Morimoto Y, Ishitani T, Kemmotsu O. Imbalances between the levels of tissue factor and tissue factor pathway inhibitor in ARDS patients. Thromb Res 2003, 109:119-124. 10.1016/S0049-3848(03)00151-8, 12706640.
30. Günther A, Mosavi P, Heinemann S, Ruppert C, Muth H, Markart P, Grimminger F, Walmrath D, Temmesfeld-Wollbrück B, Seeger W. Alveolar fibrin formation caused by enhanced procoagulant and depressed fibrinolytic capacities in severe pneumonia: comparison with the acute respiratory distress syndrome. Am J Respir Crit Care Med 2000, 161:454-462.
31. Shetty S, Padijnayayveetil J, Tucker T, Stankowska D, Idell S. The fibrinolytic system and the regulation of lung epithelial cell proteolysis, signaling and cellular viability. Am J Physiol Lung Cell Mol Physiol 2008, 295:L967-975. 10.1152/ajplung.90349.2008, 18836029.
32. Srinivasan R, Song Y, Wiener-Kronish J, Flori HR. Plasminogen activation inhibitor concentrations in bronchoalveolar lavage fluid distinguishes ventilator-associated pneumonia from colonization in mechanically ventilated pediatric patients. Pediatr Crit Care Med 2011, 12:21-27. 10.1097/PCC.0b013e3181e2a352, 20473240.
33. Song Y, Wiener-Kronish JP, Flanagan J, Lynch SV. Alveolar hemostasis in patients with species-specific bacterial-mediated ventilator-associated pneumonia. Crit Care Med 2007, 35:652-653. 10.1097/01.CCM.0000254050.98225.6B, 17251717.
34. Nakos G, Kitsiouli E, Hatzidaki E, Koulouras V, Touqui L, Lekka ME. Phospholipases A2 and platelet-activating factor acetylhydrolase in patients with acute respiratory distress syndrome. Crit Care Med 2005, 33:772-779. 10.1097/01.CCM.0000158519.80090.74, 15818104.
35. Knapp S, von Aulock S, Leendertse M, Haslinger I, Draing C, Golenbock DT, van der Poll T. Lipoteichoic acid-induced lung inflammation depends on TLR2 and the concerted action of TLR4 and the platelet-activating factor receptor. J Immunol 2008, 180:3478-3484.
36. Levitt JE, Gould MK, Ware LB, Matthay MA. The pathogenetic and prognostic value of biologic markers in acute lung injury. J Intensive Care Med 2009, 24:151-167. 10.1177/0885066609332603, 19282296.