Pseudomonas aeruginosa Pyocyanin Activates NRF2-ARE-Mediated Transcriptional Response via the ROS-EGFR-PI3K-AKT/MEK-ERK MAP Kinase Signaling in Pulmonary Epithelial Cells

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Xu, Ying ^a,b   Duan, Chaohui ^b   Kuang, Zhizhou ^a   Hao, Yonghua ^a   Jeffries, Jayme L ^a   Lau, Gee W ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PYOCYANINE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL DEATH; CELL HYPERPLASIA; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; EPITHELIUM CELL; GOBLET CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LUNG ALVEOLUS EPITHELIUM; METAPLASIA; MOUSE; MUCUS SECRETION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PSEUDOMONAS AERUGINOSA; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; CELL LINE; CELL NUCLEUS; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; LUNG; MAP KINASE SIGNALING SYSTEM; MICE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PSEUDOMONAS AERUGINOSA; PYOCYANINE; REACTIVE OXYGEN SPECIES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSCRIPTION, GENETIC;

EID: 84883202650     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072528     Document Type: Article

References (36)

1. Ojeniyi B, Frederiksen B, Hoiby N, (2000) Pseudomonas aeruginosa cross-infection among patients with cystic fibrosis during a winter camp. Pediatr Pulmonol 29: 177-181.
2. Farrell PM, Collins J, Broderick LS, Rock MJ, Li Z, et al. (2009) Association between mucoid Pseudomonas infection and bronchiectasis in children with cystic fibrosis. Radiology 252: 534-543.
3. Lyczak JB, Cannon CL, Pier GB, (2002) Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15: 194-222.
4. Lau GW, Hassett DJ, Ran H, Kong F, (2004) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10: 599-606.
5. Lau GW, Ran H, Kong F, Hassett DJ, Mavrodi D, (2004) Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice. Infect Immun 72: 4275-4278.
6. Lau GW, Hassett DJ, Britigan BE, (2005) Modulation of lung epithelial functions by Pseudomonas aeruginosa. Trends Microbiol 13: 389-397.
7. Wilson R, Sykes DA, Watson D, Rutman A, Taylor GW, et al. (1988) Measurement of Pseudomonas aeruginosa phenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory epithelium. Infect Immun 56: 2515-2517.
8. Hunter RC, Klepac-Ceraj V, Lorenzi MM, Grotzinger H, Martin TR, et al. (2012) Phenazine content in the cystic fibrosis respiratory tract negatively correlates with lung function and microbial complexity. Am J Respir Cell Mol Biol 47: 738-45.
9. Reimer A, Edvaller B, Johansson B (2000) Concentrations of the Pseudomonas aeruginosa toxin pyocyanin in human ear secretions. Acta Otolaryngol Suppl 543: 86-88.
10. 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.
11. Hao Y, Kuang Z, Walling BE, Bhatia S, Sivaguru M, et al. (2012) Pseudomonas aeruginosa pyocyanin causes airway goblet cell hyperplasia and metaplasia and mucus hypersecretion by inactivating the transcriptional factor FoxA2. Cell Microbiol 14: 401-415.
12. Muller M, (2002) Pyocyanin induces oxidative stress in human endothelial cells and modulates the glutathione redox cycle. Free Radic Biol Med 33: 1527-1533.
13. Look DC, Stoll LL, Romig SA, Humlicek A, Britigan BE, et al. (2005) Pyocyanin and its precursor phenazine-1-carboxylic acid increase IL-8 and intercellular adhesion molecule-1 expression in human airway epithelial cells by oxidant-dependent mechanisms. J Immunol 175: 4017-4023.
14. Gloyne LS, Grant GD, Perkins AV, Powell KL, McDermott CM, et al. (2011) Pyocyanin-induced toxicity in A549 respiratory cells is causally linked to oxidative stress. Toxicol In Vitro 25: 1353-8.
15. 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.
16. Gardner PR, (1996) Superoxide production by the mycobacterial and pseudomonad quinoid pigments phthiocol and pyocyanine in human lung cells. Arch Biochem Biophys 333: 267-274.
17. O'Malley YQ, Reszka KJ, Spitz DR, Denning GM, Britigan BE, (2004) Pseudomonas aeruginosa pyocyanin directly oxidizes glutathione and decreases its levels in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 287: L94-L103.
18. Ricciardolo FL, Di Stefano A, Sabatini F, Folkerts G, (2006) Reactive nitrogen species in the respiratory tract. Eur J Pharmacol 533: 240-252.
19. Ho YS, Vincent R, Dey MS, Slot JW, Crapo JD, (1998) Transgenic models for the study of lung antioxidant defense: enhanced manganese-containing superoxide dismutase activity gives partial protection to B6C3 hybrid mice exposed to hyperoxia. Am J Respir Cell Mol Biol 18: 538-547.
20. Lee PJ, Choi AM, (2003) Pathways of cell signaling in hyperoxia. Free Radic Biol Med 35: 341-350.
21. Ishii T, Itoh K, Yamamoto M, (2002) Roles of NRF2 in activation of antioxidant enzyme genes via antioxidant responsive elements. Methods Enzymol 348: 182-190.
22. Nguyen T, Sherratt PJ, Pickett CB, (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol 43: 233-260.
23. Motohashi H, Yamamoto M, (2004) NRF2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10: 549-557.
24. Cho HY, Jedlicka AE, Reddy SP, Kensler TW, Yamamoto M, et al. (2002) Role of NRF2 in protection against hyperoxic lung injury in mice. Am J Respir Cell Mol Biol 26: 175-182.
25. Cantley LC, (2002) The phosphoinositide 3-kinase pathway. Science 296: 1655-1657.
26. Papaiahgari S, Zhang Q, Kleeberger SR, Cho HY, Reddy SP, (2006) Hyperoxia stimulates an NRF2-ARE transcriptional response via ROS-EGFR-PI3K-Akt/ERK MAP kinase signaling in pulmonary epithelial cells. Antioxid Redox Signal 8: 43-52.
27. Roper JM, Mazzatti DJ, Watkins RH, Maniscalco WM, Keng PC, et al. (2004) In vivo exposure to hyperoxia induces DNA damage in a population of alveolar type II epithelial cells. Am J Physiol Lung Cell Mol Physiol 286: L1045-L1054.
28. Deng X, Rui W, Zhang F, Ding W, (2013) PM induces Nrf2-mediated defense mechanisms against oxidative stress by activating PIK3/AKT signaling pathway in human lung alveolar epithelial A549 cells. Cell Biol Toxicol 29: 143-57.
29. Tirumalai R, Rajesh KT, Mai KH, Biswal S, (2002) Acrolein causes transcriptional induction of phase II genes by activation of Nrf2 in human lung type II epithelial (A549) cells. Toxicol Lett 132: 27-36.
30. Malec V, Gottschald OR, Li S, Rose F, Seeger W, et al. (2010) HIF-1 alpha signaling is augmented during intermittent hypoxia by induction of the Nrf2 pathway in NOX1-expressing adenocarcinoma A549 cells. Free Radic Biol Med 48: 1626-35.
31. Kode A, Rajendrasozhan S, Caito S, Yang SR, Megson IL, et al. (2008) Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 294: L478-88.
32. Kong F, Young L, Chen Y, Ran H, Meyers M, et al. (2006) Pseudomonas aeruginosa pyocyanin inactivates lung epithelial vacuolar ATPase-dependent cystic fibrosis transmembrane conductance regulator expression and localization. Cell Microbiol 8: 1121-1133.
33. Wang X, McCullough KD, Franke TF, Holbrook NJ, (2000) Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J Biol Chem 275: 14624-14631.
34. Papaiahgari S, Kleeberger SR, Cho HY, Kalvakolanu DV, Reddy SP, (2004) NADPH oxidase and ERK signaling regulates hyperoxia-induced NRF2-ARE transcriptional response in pulmonary epithelial cells. J Biol Chem 279: 42302-42312.
35. Ran H, Hassett DJ, Lau GW, (2003) Human targets of Pseudomonas aeruginosa pyocyanin. Proc Natl Acad Sci U S A 100: 14315-14320.
36. Cho HY, Kleeberger SR, (2010) NRF2 protects against airway disorders. Toxicol Appl Pharmacol 244: 43-56.