Reactions of Pseudomonas aeruginosa pyocyanin with reduced glutathione

• Autorzy: Cheluvappa R. , Shimmon R. , Dawson M. , Hilmer S.N. , Le Couteur D.G.
• Języki publikacji: EN

Abstrakty

EN

Pseudomonas aeruginosa is the most common cause of chronic and recurrent lung infections in patients with cystic fibrosis (CF) whose sputa contain copious quantities of P. aeruginosatoxin, pyocyanin. Pyocyanin triggers tissue damage mainly by its redox cycling and induction of reactive oxygen species (ROS). The reactions between reduced glutathione (GSH) and pyocyanin were observed using absorption spectra from spectrophotometry and the reaction products analysed by nuclear magnetic resonance imaging. Pyocyanin reacted with GSH non-enzymatically at 37°C resulting in the production of red-brown products, spectophotometrically visible as a 480 nm maximum absorption peak after 24 h of incubation. The reaction was concentration-dependent on reduced glutathione but not on pyocyanin. Minimizing the accessibility of oxygen to the reaction decreased its rate. The anti-oxidant enzyme catalase circumvented the reaction. Proton-NMR analysis demonstrated the persistence of the original aromatic ring and the methyl-group of pyocyanin in the red-brown products. Anti-oxidant agents having thiol groups produced similar spectophotometrically visible peaks. The presence of a previously unidentified non-enzymatic GSH-dependent metabolic pathway for pyocyanin has thus been identified. The reaction betweenpyocyanin and GSH is concentration-, time-, and O2-dependent. The formation of H2O2 as an intermediate and the thiol group in GSH seem to be important in this reaction.

Słowa kluczowe

PL

lung infection; patient; cystic fibrosis; Pseudomonas aeruginosa; catalase; superoxide dismutase; glutathione; pyocyanine; oxidative stress; spectrophotometry; nuclear magnetic resonance imaging

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2008
• Tom: 55
• Numer: 3
• Opis fizyczny: p.571-580,fig.,ref.

Twórcy

autor

Cheluvappa R.

• Centre of Education and Research on Ageing, Concord RG Hospital, Hospital Road, Concord, Sydney, NSW 2139, Australia

autor

Shimmon R.

autor

Dawson M.

autor

Hilmer S.N.

autor

Le Couteur D.G.

Bibliografia

• Barbero GJ (1994) Adverse life events and exacerbations of cystic fibrosis. Pediatr Pulmonol 18:73-76.
• Beers SL, Abramo TJ (2004) Otitis externa review. Pediatr Emerg Care 20:250-256.
• Birrer P (1995) Proteases and antiproteases in cystic fibrosis: pathogenetic considerations and therapeutic strategies. Respiration 62 (Suppl 1): 25-28.
• Britigan BE, Roeder TL, Rasmussen GT, Shasby DM, McCormick ML, Cox CD (1992) Interaction of the Pseudomonas aeruginosasecretory products pyocyanin and pyochelin generates hydroxyl radical and causes synergistic damage to endothelial cells. Implications for Pseudomonas-associated tissue injury. J Clin Invest 90:2187-2196.
• Britigan BE, Railsback MA, Cox CD (1999) The Pseudomonas aeruginosasecretory product pyocyanin inactivates alpha1 protease inhibitor: implications for the pathogenesis of cystic fibrosis lung disease. Infect Immun 67:1207-1212.
• Buhl R, Vogelmeier C, Critenden M, Hubbard RC, Hoyt RF Jr, Wilson EM, Cantin AM, Crystal RG (1990) Augmentation of glutathione in the fluid lining the epithelium of the lower respiratory tract by directly administering glutathione aerosol. Proc Natl Acad Sci USA 87:4063-4067.
• Cantin AM, North SL, Hubbard RC, Crystal RG (1987) Normal alveolar epithelial lining fluid contains high levels of glutathione. J Appl Physiol 63:152-157.
• Conway SP (1999) Evidence for using nebulised antibiotics in cystic fibrosis. Arch Dis Child 80:307-309.
• Conway SP, Brownlee KG, Denton M, Peckham DG (2003) Antibiotic treatment of multidrug-resistant organisms in cystic fibrosis. Am J Respir Med 2:321-332.
• Dauletbaev N, Viel K, Buhl R, Wagner TO, Bargon J (2004) Glutathione and glutathione peroxidase in sputum samples of adult patients with cystic fibrosis. J Cyst Fibros 3:119-124.
• Denning GM, Railsback MA, Rasmussen GT, Cox CD, Britigan BE (1998) Pseudomonas pyocyanine alters calcium signaling in human airway epithelial cells. Am J Physiol 274:L893-L900.
• Gao L, Kim KJ, Yankaskas JR, Forman HJ (1999) Abnormal glutathione transport in cystic fibrosis airway epithelia. Am J Physiol 277:L113-L118.
• Hingley ST, Hastie AT, Kueppers F, Higgins ML, Weinbaum G, Shryock T (1986) Effect of ciliostatic factors from Pseudomonas aeruginosa on rabbit respiratory cilia. Infect Immun 51:254-262.
• Hudson VM (2001) Rethinking cystic fibrosis pathology: the critical role of abnormal reduced glutathione (GSH) transport caused by CFTR mutation. Free Radic Biol Med 30:1440-1461.
• Hudson VM (2004) New insights into the pathogenesis of cystic fibrosis: pivotal role of glutathione system dysfunction and implications for therapy. Treat Respir Med 3:353-363.
• Jain A, Martensson J, Mehta T, Krauss AN, Auld PA, Meister A (1992) Ascorbic acid prevents oxidative stress in glutathione-deficient mice: effects on lung type 2 cell lamellar bodies, lung surfactant, and skeletal muscle. Proc Natl Acad Sci USA 89:5093-5097.
• Kamath JM, Britigan BE, Cox CD, Shasby DM (1995) Pyocyanin from Pseudomonas aeruginosa inhibits prostacyclin release from endothelial cells. Infect Immun 63:4921-4923.
• Khalid M, Saleemi S, Zeitouni M, Al Dammas S, Khaliq MR (2004) Effect of obstructive airway disease in patients with non-cystic fibrosis bronchiectasis. Ann Saudi Med 24:284-287.
• Knight M, Hartman PE, Hartman Z, Young VM (1979) A new method of preparation of pyocyanin and demonstration of an unusual bacterial sensitivity. Anal Biochem 95:19-23.
• Konstan MW, Hilliard KA, Norvell TM, Berger M (1994) Bronchoalveolar lavage findings in cystic fibrosis patients with stable, clinically mild lung disease suggest ongoing infection and inflammation. Am J Respir Crit Care Med 150:448-454.
• Lau GW, Hassett DJ, Ran H, Kong F (2004a) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10:599-606.
• Lau GW, Ran H, Kong F, Hassett DJ, Mavrodi D (2004b) Pseudomonas aeruginosapyocyanin is critical for lung infection in mice. Infect Immun 72:4275-4278.
• Lyczak JB, Cannon CL, Pier GB (2000) Establishment of Pseudomonas aeruginosainfection: lessons from a versatile opportunist. Microbes Infect 2:1051-1060.
• Lyczak JB, Cannon CL, Pier GB (2002) Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15:194-222.
• Mahajan-Miklos S, Tan MW, Rahme LG, Ausubel FM (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96:47-56.
• Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711-760.
• Miller RA, Rasmussen GT, Cox CD, Britigan BE (1996) Protease cleavage of iron-transferrin augments pyocyanin-mediated endothelial cell injury via promotion of hydroxyl radical formation. Infect Immun 64:182-188.
• Morrison D, Rahman I, Lannan S, MacNee W (1999) Epithelial permeability, inflammation, and oxidant stress in the air spaces of smokers. Am J Respir Crit Care Med 159:473-479.
• Muller M (2002) Pyocyanin induces oxidative stress in human endothelial cells and modulates the glutathione redox cycle. Free Rad Biol Med 33:1527-1533.
• Muller M, Sorrell TC (1992) Leukotriene B4 omega-oxidation by human polymorphonuclear leukocytes is inhibited by pyocyanin, a phenazine derivative produced by Pseudomonas aeruginosa. Infect Immun 60:2536-2540.
• Munro NC, Barker A, Rutman A, Taylor G, Watson D, McDonald-Gibson WJ, Towart R, Taylor WA, Wilson R, Cole PJ (1989) Effect of pyocyanin and 1-hydroxyphenazine on in vivotracheal mucus velocity. J Appl Physiol 67:316-323.
• O'Malley YQ, Reszka KJ, Rasmussen GT, Abdalla MY, Denning GM, Britigan BE (2003) The Pseudomonas secretory product pyocyanin inhibits catalase activity in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 285:L1077-L1086.
• O'Malley YQ, Reszka KJ, Spitz DR, Denning GM, Britigan BE (2004) Pseudomonas aeruginosapyocyanin directly oxidizes glutathione and decreases its levels in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 287:L94-L103.
• Pitt TL (1986) Biology of Pseudomonas aeruginosa in relation to pulmonary infection in cystic fibrosis. J R Soc Med 79 (Suppl 12): 13-18.
• Rahman I, MacNee W (2000) Oxidative stress and regulation of glutathione in lung inflammation. Eur Respir J 16:534-554.
• Roum JH, Buhl R, McElvaney NG, Borok Z, Crystal RG (1993) Systemic deficiency of glutathione in cystic fibrosis. J Appl Physiol 75:2419-2424.
• Roum JH, Borok Z, McElvaney NG, Grimes GJ, Bokser AD, Buhl R, Crystal RG (1999) Glutathione aerosol suppresses lung epithelial surface inflammatory cell-derived oxidants in cystic fibrosis. J Appl Physiol 87:438-443.
• Samiec PS, Drews-Botsch C, Flagg EW, Kurtz JC, Sternberg P Jr, Reed RL, Jones DP (1998) Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic Biol Med 24:699-704.
• Sorensen RU, Klinger JD (1987) Biological effects of Pseudomonas aeruginosaphenazine pigments. Antibiot Chemother 39:113-124.
• Watson D, MacDermot J, Wilson R, Cole PJ, Taylor GW (1986) Purification and structural analysis of pyocyanin and 1-hydroxyphenazine. Eur J Biochem 159:309-313.
• Wilson R, Pitt T, Taylor G, Watson D, MacDermot J, Sykes D, Roberts D, Cole P (1987) Pyocyanin and 1-hydroxyphenazine produced by Pseudomonas aeruginosainhibit the beating of human respiratory cilia in vitro. J Clin Invest 79:221-229.
• Wilson R, Sykes DA, Watson D, Rutman A, Taylor GW, Cole PJ (1988) Measurement of Pseudomonas aeruginosaphenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory epithelium. Infect Immun 56:2515-2517.
• Zachara BA, Gromadzinska J, Wasowicz W, Zbrog Z (2006) Red blood cell and plasma glutathione peroxidase activities and selenium concentration in patients with chronic kidney disease: a review. Acta Biochim Polon 53:663-77.