Pyocyanin effects on respiratory epithelium: Relevance in Pseudomonas aeruginosa airway infections

Trends in Microbiology

Volumn 21, Issue 2, 2013, Pages 73-81

  Rada, Balázs ^a,b   Leto, Thomas L ^b  

^a UNIVERSITY OF GEORGIA   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Epithelium; Pseudomonas; Pyocyanin; Redox; Respiratory

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GLUTATHIONE; INTERLEUKIN 11; INTERLEUKIN 19; INTERLEUKIN 20; INTERLEUKIN 23; INTERLEUKIN 24; INTERLEUKIN 6; MUCIN; PYOCYANINE; REACTIVE OXYGEN METABOLITE;

BACTERIAL VIRULENCE; BRONCHIECTASIS; CHRONIC OBSTRUCTIVE LUNG DISEASE; COLONY FORMING UNIT; CYSTIC FIBROSIS; CYTOKINE RELEASE; DOWN REGULATION; ENZYME SYNTHESIS; FORCED EXPIRATORY VOLUME; IMMUNE RESPONSE; LUNG FUNCTION; NEUTROPHIL; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; OXYGENATION; PATHOGENESIS; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; PURIFICATION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT INFECTION; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

CYSTIC FIBROSIS; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; MUCINS; OXIDATION-REDUCTION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; PYOCYANINE; RESPIRATORY MUCOSA; VIRULENCE FACTORS;

ANIMALIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 84873161425     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2012.10.004     Document Type: Review

References (74)

1. Lyczak J.B., et al. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2000, 2:1051-1060.
2. Murphy T.F. The many faces of Pseudomonas aeruginosa in chronic obstructive pulmonary disease. Clin. Infect. Dis. 2008, 47:1534-1536.
3. Cohen T.S., Prince A. Cystic fibrosis: a mucosal immunodeficiency syndrome. Nat. Med. 2012, 18:509-519.
4. Campodonico V.L., et al. Airway epithelial control of Pseudomonas aeruginosa infection in cystic fibrosis. Trends Mol. Med. 2008, 14:120-133.
5. Lipuma J.J. The changing microbial epidemiology in cystic fibrosis. Clin. Microbiol. Rev. 2010, 23:299-323.
6. Silby M.W., et al. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol. Rev. 2011, 35:652-680.
7. Hoiby N., et al. Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol. 2010, 5:1663-1674.
8. Breidenstein E.B., et al. Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol. 2011, 19:419-426.
9. Pierson L.S., Pierson E.A. Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl. Microbiol. Biotechnol. 2010, 86:1659-1670.
10. Reszka K.J., et al. Oxidation of pyocyanin, a cytotoxic product from Pseudomonas aeruginosa, by microperoxidase 11 and hydrogen peroxide. Free Radic. Biol. Med. 2004, 36:1448-1459.
11. Price-Whelan A., et al. Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nat. Chem. Biol. 2006, 2:71-78.
12. Rada B., et al. The Pseudomonas toxin pyocyanin inhibits the dual oxidase-based antimicrobial system as it imposes oxidative stress on airway epithelial cells. J. Immunol. 2008, 181:4883-4893.
13. Dietrich L.E., et al. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 2008, 321:1203-1206.
14. Koley D., et al. Discovery of a biofilm electrocline using real-time 3D metabolite analysis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:19996-20001.
15. Moreau-Marquis S., et al. The DeltaF508-CFTR mutation results in increased biofilm formation by Pseudomonas aeruginosa by increasing iron availability. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 295:L25-L37.
16. Dietrich L.E., et al. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 2006, 61:1308-1321.
17. Rahme L.G., et al. Plants and animals share functionally common bacterial virulence factors. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8815-8821.
18. Mahajan-Miklos S., et al. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 1999, 96:47-56.
19. Lau G.W., et al. The Drosophila melanogaster toll pathway participates in resistance to infection by the Gram-negative human pathogen Pseudomonas aeruginosa. Infect. Immun. 2003, 71:4059-4066.
20. Cao H., et al. Common mechanisms for pathogens of plants and animals. Annu. Rev. Phytopathol. 2001, 39:259-284.
21. Lau G.W., et al. Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice. Infect. Immun. 2004, 72:4275-4278.
22. Rada B., Leto T.L. Redox warfare between airway epithelial cells and Pseudomonas: dual oxidase versus pyocyanin. Immunol. Res. 2009, 43:198-209.
23. Lau G.W., et al. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol. Med. 2004, 10:599-606.
24. Hao Y., et al. Pseudomonas aeruginosa pyocyanin causes airway goblet cell hyperplasia and metaplasia and mucus hypersecretion by inactivating the transcriptional factor FoxA2. Cell. Microbiol. 2012, 14:401-415.
25. Bianconi I., et al. Positive signature-tagged mutagenesis in Pseudomonas aeruginosa: tracking patho-adaptive mutations promoting airways chronic infection. PLoS Pathog. 2011, 7:e1001270.
26. Wilson R., et al. Measurement of Pseudomonas aeruginosa phenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory epithelium. Infect. Immun. 1988, 56:2515-2517.
27. Hunter R.C., et al. Phenazine content in the cystic fibrosis respiratory tract negatively correlates with lung function and microbial complexity. Am. J. Respir. Cell Mol. Biol. 2012, 47:738-745.
28. Caldwell C.C., et al. Pseudomonas aeruginosa exotoxin pyocyanin causes cystic fibrosis airway pathogenesis. Am. J. Pathol. 2009, 175:2473-2488.
29. Mowat E., et al. Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am. J. Respir. Crit. Care Med. 2011, 183:1674-1679.
30. Fothergill J.L., et al. Widespread pyocyanin over-production among isolates of a cystic fibrosis epidemic strain. BMC Microbiol. 2007, 7:45.
31. Lore N.I., et al. Cystic fibrosis-niche adaptation of Pseudomonas aeruginosa reduces virulence in multiple infection hosts. PLoS ONE 2012, 7:e35648.
32. Carlsson M., et al. Pseudomonas aeruginosa in cystic fibrosis: pyocyanin negative strains are associated with BPI-ANCA and progressive lung disease. J. Cyst. Fibros. 2011, 10:265-271.
33. Bohn Y.S., et al. Multiple roles of Pseudomonas aeruginosa TBCF10839 PilY1 in motility, transport and infection. Mol. Microbiol. 2009, 71:730-747.
34. Mavrodi D.V., et al. Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu. Rev. Phytopathol. 2006, 44:417-445.
35. Schwarzer C., et al. Oxidative stress caused by pyocyanin impairs CFTR Cl(-) transport in human bronchial epithelial cells. Free Radic. Biol. Med. 2008, 45:1653-1662.
36. O'Malley Y.Q., et al. Pseudomonas aeruginosa pyocyanin directly oxidizes glutathione and decreases its levels in airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2004, 287:L94-L103.
37. Muller M. Glutathione modulates the toxicity of, but is not a biologically relevant reductant for, the Pseudomonas aeruginosa redox toxin pyocyanin. Free Radic. Biol. Med. 2011, 50:971-977.
38. O'Malley Y.Q., et al. Subcellular localization of Pseudomonas pyocyanin cytotoxicity in human lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 284:L420-L430.
39. Jimenez P.N., et al. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 2012, 76:46-65.
40. Parker D., Prince A. Innate immunity in the respiratory epithelium. Am. J. Respir. Cell Mol. Biol. 2011, 45:189-201.
41. Munro N.C., et al. Effect of pyocyanin and 1-hydroxyphenazine on in vivo tracheal mucus velocity. J. Appl. Physiol. 1989, 67:316-323.
42. Britigan B.E., et al. The Pseudomonas aeruginosa secretory product pyocyanin inactivates alpha(1) protease inhibitor: implications for the pathogenesis of cystic fibrosis lung disease. Infect. Immun. 1999, 67:1207-1212.
43. Kong F., et al. Pseudomonas aeruginosa pyocyanin inactivates lung epithelial vacuolar ATPase-dependent cystic fibrosis transmembrane conductance regulator expression and localization. Cell. Microbiol. 2006, 8:1121-1133.
44. O'Malley Y.Q., et al. The Pseudomonas secretory product pyocyanin inhibits catalase activity in human lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 285:L1077-L1086.
45. Geiszt M., et al. Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J. 2003, 17:1502-1504.
46. Forteza R., et al. Regulated hydrogen peroxide production by Duox in human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 2005, 32:462-469.
47. Shao M.X., Nadel J.A. Dual oxidase 1-dependent MUC5AC mucin expression in cultured human airway epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:767-772.
48. Boots A.W., et al. ATP-mediated activation of the NADPH oxidase DUOX1 mediates airway epithelial responses to bacterial stimuli. J. Biol. Chem. 2009, 284:17858-17867.
49. Rada B., Leto T.L. Characterization of hydrogen peroxide production by Duox in bronchial epithelial cells exposed to Pseudomonas aeruginosa. FEBS Lett. 2010, 584:917-922.
50. Moskwa P., et al. A novel host defense system of airways is defective in cystic fibrosis. Am. J. Respir. Crit. Care Med. 2007, 175:174-183.
51. Rada B., et al. Reactive oxygen species mediate inflammatory cytokine release and EGFR-dependent mucin secretion in airway epithelial cells exposed to Pseudomonas pyocyanin. Mucosal Immunol. 2011, 4:158-171.
52. Gloyne L.S., et al. Pyocyanin-induced toxicity in A549 respiratory cells is causally linked to oxidative stress. Toxicol. In Vitro 2011, 25:1353-1358.
53. Schwarzer C., et al. Redox-independent activation of NF-kappaB by Pseudomonas aeruginosa pyocyanin in a cystic fibrosis airway epithelial cell line. J. Biol. Chem. 2008, 283:27144-27153.
54. O'Malley Y.X.Q., et al. The Pseudomonas secretory product pyocyanin inhibits catalase activity in human lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 285:L1077-L1086.
55. Denning G.M., et al. Pseudomonas pyocyanin increases interleukin-8 expression by human airway epithelial cells. Infect. Immun. 1998, 66:5777-5784.
56. Look D.C., et al. 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. 2005, 175:4017-4023.
57. Sadik C.D., et al. Neutrophils cascading their way to inflammation. Trends Immunol. 2011, 32:452-460.
58. Ratner D., Mueller C. Immune responses in cystic fibrosis: are they intrinsically defective?. Am. J. Respir. Cell Mol. Biol. 2012, 46:715-722.
59. Lauredo I.T., et al. Mechanism of pyocyanin- and 1-hydroxyphenazine-induced lung neutrophilia in sheep airways. J. Appl. Physiol. 1998, 85:2298-2304.
60. Jensen P.O., et al. Increased serum concentration of G-CSF in cystic fibrosis patients with chronic Pseudomonas aeruginosa pneumonia. J. Cyst. Fibros. 2006, 5:145-151.
61. Osika E., et al. Distinct sputum cytokine profiles in cystic fibrosis and other chronic inflammatory airway disease. Eur. Respir. J. 1999, 14:339-346.
62. Wyatt H.A., et al. Production of the potent neutrophil chemokine, growth-related protein alpha (GROalpha), is not elevated in cystic fibrosis children. Respir. Med. 2000, 94:106-111.
63. McAllister F., et al. Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J. Immunol. 2005, 175:404-412.
64. Hartl D., et al. Pulmonary T(H)2 response in Pseudomonas aeruginosa-infected patients with cystic fibrosis. J. Allergy Clin. Immunol. 2006, 117:204-211.
65. Nixon L.S., et al. Circulating immunoreactive interleukin-6 in cystic fibrosis. Am. J. Respir. Crit. Care Med. 1998, 157:1764-1769.
66. Carpagnano G.E., et al. Increased leukotriene B4 and interleukin-6 in exhaled breath condensate in cystic fibrosis. Am. J. Respir. Crit. Care Med. 2003, 167:1109-1112.
67. Zakrzewski J.T., et al. Detection of sputum eicosanoids in cystic fibrosis and in normal saliva by bioassay and radioimmunoassay. Br. J. Clin. Pharmacol. 1987, 23:19-27.
68. Dubin P.J., Kolls J.K. IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 292:L519-L528.
69. Rose M.C., Voynow J.A. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol. Rev. 2006, 86:245-278.
70. Thai P., et al. Regulation of airway mucin gene expression. Annu. Rev. Physiol. 2008, 70:405-429.
71. Kim H.J., et al. The role of Nox4 in oxidative stress-induced MUC5AC overexpression in human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 2008, 39:598-609.
72. Shao M.X.G., Nadel J.A. Dual oxidase 1-dependent MUC5AC mucin expression in cultured human airway epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:767-772.
73. Burgel P.R., Nadel J.A. Epidermal growth factor receptor-mediated innate immune responses and their roles in airway diseases. Eur. Respir. J. 2008, 32:1068-1081.
74. Tyner J.W., et al. Blocking airway mucous cell metaplasia by inhibiting EGFR antiapoptosis and IL-13 transdifferentiation signals. J. Clin. Invest. 2006, 116:309-321.