Extracellular Glutathione Decreases the Ability of Burkholderia cenocepacia to Penetrate into Epithelial Cells and to Induce an Inflammatory Response

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  D'Orazio, Melania ^a   Pacello, Francesca ^b   Battistoni, Andrea ^b  

^a IRCCS SAN RAFFAELE PISANA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; INTERLEUKIN 1BETA; INTERLEUKIN 8; MEMBRANE PROTEIN; THIOL DERIVATIVE; TUMOR NECROSIS FACTOR ALPHA;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL INVASION; BACTERIAL TRANSMISSION; BACTERIUM ADHERENCE; BURKHOLDERIA CENOCEPACIA; CELL INTERACTION; CELL SURFACE; CONTROLLED STUDY; CYSTIC FIBROSIS; EPITHELIUM CELL; EXTRACELLULAR SPACE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; NONHUMAN; OXIDATION REDUCTION REACTION; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; SPECIES INVASION;

BRONCHI; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA INFECTIONS; CELL LINE; CYSTIC FIBROSIS; EPITHELIAL CELLS; GLUTATHIONE; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-8; OXIDATION-REDUCTION; PRIMARY CELL CULTURE; RESPIRATORY MUCOSA; TRACHEA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84867664562     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047550     Document Type: Article

References (42)

1. Roum JH, Buhl R, McElvany NG, Borok Z, Crystal RG, (1993) Systemic deficiency of glutathione in cystic fibrosis. J Appl Physiol 75: 2419-2424.
2. 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.
3. Velsor LW, van Heeckeren AM, Day BJ, (2001) Antioxidant imbalance in the lungs of cystic fibrosis transmembrane conductance regulator protein mutant mice. Am J Physiol Lung Cell Mol Physiol 281: L31-L38.
4. 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.
5. Filomeni G, Rotilio G, Ciriolo MR, (2002) Cell signalling and the glutathione redox system. Biochem Pharmacol 64: 1057-1064.
6. Roum JH, Borok Z, McElvaney NG, Grimes GJ, Bokser AD, et al. (1999) Glutathione aerosol suppresses lung epithelial surface inflammatory cell-derived oxidants in cystic fibrosis. J Appl Physiol 87: 438-443.
7. Griese M, Ramakers J, Krasselt A, Starosta V, Van Koningsbruggen S, et al. (2004) Improvement of alveolar glutathione and lung function but not oxidative state in cystic fibrosis. Am J Respir Crit Care Med 169: 822-828.
8. Bishop C, Hudson VM, Hilton SC, Wilde C, (2005) A pilot study of the effect of inhaled buffered reduced glutathione on clinical status of patients with cystic fibrosis. Chest 127: 308-317.
9. Visca A, Bishop CT, Hilton SC, Hudson VM, (2008) Improvement in clinical markers in CF patients using a reduced glutathione regimen: an uncontrolled, observational study. J Cyst Fibros 7: 433-436.
10. Tirouvanziam R, Conrad CK, Bottiglieri T, Herzenberg LA, Moss RB, et al. (2006) High-dose oral N-acetylcysteine, a glutathione prodrug, modulates inflammation in cystic fibrosis. Proc Natl Acad Sci U S A 103: 4628-4633.
11. Dauletbaev N, Fischer P, Aulbach B, Diegel H, von Mallinckrodt C, et al. (2009) A phase II study on safety and efficacy of high-dose N-acetylcysteine in patients with cystic fibrosis. Eur J Med Res 14: 352-358.
12. Nash EF, Stephenson A, Ratjen F, Tullis E, (2009) Nebulized and oral thiol derivatives for pulmonary disease in cystic fibrosis. Cochrane Database Syst Rev. 21: CD007168.
13. Gould NS, Gauthier S, Kariya CT, Min E, Huang J, et al. (2010) Hypertonic saline increases lung epithelial lining fluid glutathione and thiocyanate: two protective CFTR-dependent thiols against oxidative injury. Respir Res. 11: 119-128.
14. Vasu VT, de Cruz SJ, Houghton JS, Hayakawa KA, Morrissey BM, et al. (2011) Evaluation of thiol-based antioxidant therapeutics in cystic fibrosis sputum: Focus on myeloperoxidase. Free Radic Res 45: 165-76.
15. Muller M, (2011) Glutathione modulates the toxicity of, but is not a biologically relevant reductant for, the Pseudomonas aeruginosa redox toxin pyocyanin. Free Radic Biol Med 50: 971-977.
16. Rada B, Gardina P, Myers TG, Leto TL, (2011) Reactive oxygen species mediate inflammatory cytokine release and EGFR-dependent mucin secretion in airway epithelial cells exposed to Pseudomonas pyocyanin. Mucosal Immunol 4: 158-171.
17. Caldwell CC, Chen Y, Goetzmann HS, Hao Y, Borchers MT, et al. (2009) Pseudomonas aeruginosa exotoxin pyocyanin causes cystic fibrosis airway pathogenesis. Am J Pathol 175: 2473-2488.
18. Holden MT, Seth-Smith HM, Crossman LC, Sebaihia M, Bentley SD, et al. (2009) The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 191: 261-277.
19. Petrucca A, Cipriani P, Valenti P, Santapaola D, Cimmino C, et al. (2003) Molecular characterization of Burkholderia cepacia isolates from cystic fibrosis (CF) patients in an Italian CF center. Res Microbiol 154: 491-498.
20. Sokol PA, Darling P, Woods DE, Mahenthiralingam E, Kooi C, (1999) Role of Ornibactin biosynthesis in the virulence of Burkholderia cepacia: characterization of pvdA, the gene encoding l-ornithine N5-oxygenase. Infect Immun 67: 4443-4455.
21. Buhler T, Ballestero S, Desai M, Brown MR, (1998) Generation of a reproducible nutrient-depleted biofilm of Escherichia coli and Burkholderia cepacia. J Appl Microbiol. 85: 457-462.
22. Greunert DC, Basbaum CB, Welsh MJ, Li M, Finkbeiner WE, et al. (1988) Characterization of human tracheal epithelial cells transformed by an origin-defective simian virus 40. Proc Natl Acad Sci USA 85: 5951-5955.
23. Kunzelmann K, Schwiebert EM, Zeitlin PL, Kuo W-L, Stanton BA, et al. (1993) An immortalized cystic fibrosis tracheal epithelial cell line homozygous for the ΔF508 CFTR Mutation. Am J Respir Cell Mol Biol 8: 522-529.
24. Martin DW, Mohr CD, (2000) Invasion and intracellular survival of Burkholderia cepacia. Infect Immun. 68: 24-29.
25. Sajjan U, Keshavjee S, Forstner J, (2004) Responses of well-differentiated airway epithelial cell cultures from healthy donors and patients with cystic fibrosis to Burkholderia cenocepacia infection. Infect Immun. 72: 4188-4199.
26. Sajjan U, Corey M, Humar A, Tullis E, Cutz E, et al. (2001) Immunolocalization of Burkholderia cepacia in the lungs of cystic fibrosis patients. J Med Microbiol 50: 535-546.
27. Nicolis E, Lampronti I, Dechecchi MC, Borgatti M, Tamanini A, et al. (2008) Pyrogallol, an active compound from the medicinal plant Emblica officinalis, regulates expression of pro-inflammatory genes in bronchial epithelial cells Int Immunopharmacol. 8: 1672-1680.
28. Tipper JL, Ingham E, Cove JH, Todd NJ, Kerr KG, (1998) Survival and multiplication of Burkholderia cepacia within respiratory epithelial cells. Clin Microbiol Infect 8: 450-459.
29. Duff C, Murphy PG, Callaghan M, McClean S, (2006) Differences in invasion and translocation of Burkholderia cepacia complex species in polarised lung epithelial cells in vitro. Microb Pathog. 41: 183-192.
30. Pirone L, Bragonzi A, Farcomeni A, Paroni M, Auriche C, et al. (2008) Burkholderia cenocepacia strains isolated from cystic fibrosis patients are apparently more invasive and more virulent than rhizosphere strains. Environ Microbiol 10: 2773-2784.
31. Ghezzi P, (2011) Role of glutathione in immunity and inflammation in the lung. Int J Gen Med. 4: 105-113.
32. Nencioni L, Iuvara A, Aquilano K, Ciriolo MR, Cozzolino F, et al. (2003) Influenza A virus replication is dependent on an antioxidant pathway that involves GSH and Bcl-2. FASEB J. 6: 758-760.
33. Staal FJ, Roederer M, Herzenberg LA, Herzenberg LA, (1990) Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. Proc Natl Acad Sci USA 87: 9943-9947.
34. Venketaraman V, Millman A, Salman M, Swaminathan S, Goetz M, et al. (2008) Glutathione levels and immune responses in tuberculosis patients. Microb Pathog. 44: 255-261.
35. Lee CA, Falkow S, (1990) The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc. Natl.Acad. Sci. USA 87: 4304-4308.
36. Ernst RK, Dombroski DM, Merrick JM, (1990) Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium. Infect.Immun. 58: 2014-2016.
37. Skalska J, Brookes PS, Nadtochiy SM, Hilchey SP, Jordan CT, et al. (2009) Modulation of cell surface protein free thiols: a potential novel mechanism of action of the sesquiterpene lactone parthenolide. Plos One 4: e8115.
38. Metcalfe C, Cresswell P, Ciaccia L, Thomas B, Barclay AN, (2011) Labile disulfide bonds are common at the leucocyte cell surface. Open Biol. 1: 110010.
39. Ou W, Silver J, (2006) Role of protein disulfide isomerase and other thiol-reactive proteins in Hiv-1 envelope protein-mediated fusion. Virology 350: 406-417.
40. Schwertassek U, Balmer Y, Gutscher M, Weingarten L, Preuss M, et al. (2007) Selective redox regulation of cytokine receptor signaling by extracellular thioredoxin-1. EMBO J 26: 3086-3097.
41. Imhoff BR, Hansen JM, (2009) Extracellular redox status regulates Nrf2 activation through mitochondrial reactive oxygen species. Biochem J 424: 491-500.
42. Sajjan US, Hershenson MB, Forstner JF, LiPuma JJ, (2008) Burkholderia cenocepacia ET12 strain activates TNFR1 signaling in cystic fibrosis airway epithelial cells Cell Microbiol. 10: 188-201.