The Pseudomonas aeruginosa autoinducer 3O-C12 homoserine lactone provokes hyperinflammatory responses from cystic fibrosis airway epithelial cells

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Mayer, Matthew L ^a   Sheridan, Jared A ^a   Blohmke, Christoph J ^a,b   Turvey, Stuart E ^a,b   Hancock, Robert E W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BC CHILDREN S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; INTERLEUKIN 6; LACTONE DERIVATIVE; N 3 OXODODECANOYL HOMOSERINE LACTONE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VIRULENCE FACTOR; CALCIUM; DRUG DERIVATIVE; GAMMA BUTYROLACTONE; HOMOSERINE; LACTONE; N (3 OXODODECANOYL)HOMOSERINE LACTONE; N-(3-OXODODECANOYL)HOMOSERINE LACTONE; PSEUDOMONAS AERUGINOSA AUTOINDUCER;

ARTICLE; ASSAY; BRONCHUS MUCOSA; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL TYPE; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE PRODUCTION; EPITHELIUM CELL; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFLAMMATION; INNATE IMMUNITY; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; RESPIRATORY EPITHELIUM; BIOSYNTHESIS; CHEMICALLY INDUCED DISORDER; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; RESPIRATORY SYSTEM;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

4-BUTYROLACTONE; CALCIUM; CYSTIC FIBROSIS; CYTOKINES; EPITHELIAL CELLS; HOMOSERINE; HUMANS; INFLAMMATION; LACTONES; PSEUDOMONAS AERUGINOSA; RESPIRATORY SYSTEM;

EID: 79551629639     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016246     Document Type: Article

References (58)

1. Levy H, Murphy A, Zou F, Gerard C, Klanderman B, et al. (2009) IL1B polymorphisms modulate cystic fibrosis lung disease. Pediatr Pulmonol 44: 580-593.
2. Muselet-Charlier C, Roque T, Boncoeur E, Chadelat K, Clement A, et al. (2007) Enhanced IL-1beta-induced IL-8 production in cystic fibrosis lung epithelial cells is dependent of both mitogen-activated protein kinases and NFkappaB signaling. Biochem Biophys Res Commun 357: 402-407.
3. Tabary O, Boncoeur E, Martin R de, Pepperkok R, Clément A, et al. (2006) Calcium-dependent regulation of NF-(kappa)B activation in cystic fibrosis airway epithelial cells. Cell Signal 18: 652-660.
4. Blohmke CJ, Victor RE, Hirschfeld AF, Elias IM, Hancock DG, et al. (2008) Innate immunity mediated by TLR5 as a novel antiinflammatory target for cystic fibrosis lung disease. J Immunol 180: 7764-7773.
5. Ierano T, Cescutti P, Leone MR, Luciani A, Rizzo R, et al. (2010) The lipid A of Burkholderia multivorans C1576 smooth-type lipopolysaccharide and its proinflammatory activity in a cystic fibrosis airways model. Innate Immun 16: 354-365.
6. Ornatowski W, Poschet JF, Perkett E, Taylor-Cousar JL, Deretic V (2007) Elevated furin levels in human cystic fibrosis cells result in hypersusceptibility to exotoxin A-induced cytotoxicity. J Clin Invest 117: 3489-3497.
7. Erickson DL, Endersby R, Kirkham A, Stuber K, Vollman DD, et al. (2002) Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infect Immun 70: 1783-1790.
8. Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, et al. (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407: 762-764.
9. Möker N, Dean CR, Tao J (2010) Pseudomonas aeruginosa increases formation of multidrug-tolerant persister cells in response to quorum-sensing signaling molecules. J Bacteriol 192: 1946-1955.
10. Smith RS, Harris SG, Phipps R, Iglewski B (2002) The Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)homoserine lactone contributes to virulence and induces inflammation in vivo. J Bacteriol 184: 1132-1139.
11. Imamura Y, Yanagihara K, Tomono K, Ohno H, Higashiyama Y, et al. (2005) Role of Pseudomonas aeruginosa quorum-sensing systems in a mouse model of chronic respiratory infection. J Med Microbiol 54: 515-518.
12. Hartman G, Wise R (1998) Quorum sensing: potential means of treating gramnegative infections? Lancet 351: 848-849.
13. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, et al. (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22: 3803-3815.
14. Bjarnsholt T, Gennip M van, Jakobsen TH, Christensen LD, Jensen PØ, et al. (2010) In vitro screens for quorum sensing inhibitors and in vivo confirmation of their effect. Nat Protoc 5: 282-293.
15. Boontham P, Robins A, Chandran P, Pritchard D, Cámara M, et al. (2008) Significant immunomodulatory effects of Pseudomonas aeruginosa quorumsensing signal molecules: possible link in human sepsis. Clin Sci (Lond) 115: 343-351.
16. Li H, Wang L, Ye L, Mao Y, Xie X, et al. (2009) Influence of Pseudomonas aeruginosa quorum sensing signal molecule N-(3-oxododecanoyl) homoserine lactone on mast cells. Med Microbiol Immunol 198: 113-121.
17. Jacobi C a, Schiffner F, Henkel M, Waibel M, Stork B, et al. (2009) Effects of bacterial N-acyl homoserine lactones on human Jurkat T lymphocytes-OdDHL induces apoptosis via the mitochondrial pathway. Int J Med Microbiol 299: 509-19.
18. Tateda K, Ishii Y, Horikawa M, Matsumoto T, Miyairi S, et al. (2003) The Pseudomonas aeruginosa Autoinducer N-3-Oxododecanoyl Homoserine Lactone Accelerates Apoptosis in Macrophages and Neutrophils. Infect Immun 71: 5785-5793.
19. Kravchenko VV, Kaufmann GF, Mathison JC, Scott DA, Katz AZ, et al. (2008) Modulation of gene expression via disruption of NF-kappaB signaling by a bacterial small molecule. Science 321: 259-263.
20. Smith RS, Kelly R, Iglewski BH, Phipps RP (2002) The Pseudomonas autoinducer N-(3-oxododecanoyl) homoserine lactone induces cyclooxygenase-2 and prostaglandin E2 production in human lung fibroblasts: implications for inflammation. J Immunol 169: 2636-2642.
21. Smith RS, Fedyk ER, Springer TA, Mukaida N, Iglewski BH, et al. (2001) IL-8 production in human lung fibroblasts and epithelial cells activated by the Pseudomonas autoinducer N-3-oxododecanoyl homoserine lactone is transcriptionally regulated by NF-kappa B and activator protein-2. J Immunol 167: 366-374.
22. Sbarbati A, Tizzano M, Merigo F, Benati D, Nicolato E, et al. (2009) Acyl homoserine lactones induce early response in the airway. Anat Rec (Hoboken) 292: 439-448.
23. Zimmermann S, Wagner C, Müller W, Brenner-Weiss G, Hug F, et al. (2006) Induction of neutrophil chemotaxis by the quorum-sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone. Infect Immun 74: 5687-5692.
24. Bérubé J, Roussel L, Nattagh L, Rousseau S (2010) Loss of cystic fibrosis transmembrane conductance regulator (CFTR) function enhances p38 and ERK MAPKs activation increasing IL-6 synthesis in airway epithelial cells exposed to Pseudomonas aeruginosa. J Biol Chem 285: 22299-22307.
25. Borgatti M, Bezzerri V, Mancini I, Nicolis E, Dechecchi MC, et al. (2007) Induction of IL-6 gene expression in a CF bronchial epithelial cell line by Pseudomonas aeruginosa is dependent on transcription factors belonging to the Sp1 superfamily. Biochem Biophys Res Commun 357: 977-983.
26. Delgado MA, Poschet JF, Deretic V (2006) Nonclassical pathway of Pseudomonas aeruginosa DNA-induced interleukin-8 secretion in cystic fibrosis airway epithelial cells. Infect Immun 74: 2975-2984.
27. Joseph T, Look D, Ferkol T (2005) NF-kappaB activation and sustained IL-8 gene expression in primary cultures of cystic fibrosis airway epithelial cells stimulated with Pseudomonas aeruginosa. Am J Physiol Lung Cell Mol Physiol 288: L471-L479.
28. Blohmke CJ, Park J, Hirschfeld AF, Victor RE, Schneiderman J, et al. (2010) TLR5 as an anti-inflammatory target and modifier gene in cystic fibrosis. J Immunol 185: 7731-7738.
29. Stoltz Da, Ozer Ea, Ng CJ, Yu JM, Reddy ST, et al. (2007) Paraoxonase-2 deficiency enhances Pseudomonas aeruginosa quorum sensing in murine tracheal epithelia. Am J Physiol Lung Cell Mol Physiol 292: L852-L860.
30. Zhu H, Conibear TCR, Thuruthyil SJ, Willcox MDP (2008) Pseudomonas aeruginosa quorum-sensing signal molecules induce IL-8 production by human corneal epithelial cells. Eye Contact Lens 34: 179-181.
31. Cooley MA, Whittall C, Rolph MS (2010) Pseudomonas signal molecule 3-oxo- C12-homoserine lactone interferes with binding of rosiglitazone to human PPARgamma. Microbes infect 12: 231-237.
32. Horke S, Witte I, Altenhöfer S, Wilgenbus P, Goldeck M, et al. (2010) Paraoxonase 2 is down-regulated by the Pseudomonas aeruginosa quorumsensing signal N-(3-oxododecanoyl)-L-homoserine lactone and attenuates oxidative stress induced by pyocyanin. Biochem J 426: 73-83.
33. Bryan A, Watters C, Koenig L, Youn E, Olmos A, et al. (2010) Human transcriptome analysis reveals a potential role for active transport in the metabolism of Pseudomonas aeruginosa autoinducers. Microbes Infect 12: 1042-1050.
34. Ideker T, Ozier O, Schwikowski B, Siegel AF (2002) Discovering regulatory and signalling circuits in molecular interaction networks. Bioinformatics 18 Suppl 1: S233-S240.
35. Tan K, Tegner J, Ravasi T (2008) Integrated approaches to uncovering transcription regulatory networks in mammalian cells. Genomics 91: 219-231.
36. Shiner EK, Terentyev D, Bryan A, Sennoune S, Martinez-Zaguilan R, et al. (2006) Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling. Cell Microbiol 8: 1601-1610.
37. Elizur A, Cannon CL, Ferkol TW (2008) Airway inflammation in cystic fibrosis. Chest 133: 489-495.
38. Miyairi S, Tateda K, Fuse ET, Ueda C, Saito H, et al. (2006) Immunization with 3-oxododecanoyl-L-homoserine lactone-protein conjugate protects mice from lethal Pseudomonas aeruginosa lung infection. J Med Microbiol 55: 1381-1387.
39. Charlton TS, Nys R de, Netting a, Kumar N, Hentzer M, et al. (2000) A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ Microbiol 2: 530-541.
40. Gomperts BN, Belperio JA, Rao PN, Randell SH, Fishbein MC, et al. (2006) Circulating progenitor epithelial cells traffic via CXCR4/CXCL12 in response to airway injury. J Immunol 176: 1916-1927.
41. Palfreyman RW, Watson ML, Eden C, Smith AW (1997) Induction of biologically active interleukin-8 from lung epithelial cells by Burkholderia (Pseudomonas) cepacia products. Infect Immun 65: 617-622.
42. Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M (2002) Multiple control of interleukin-8 gene expression. J Leukoc Biol 72: 847-855.
43. Kravchenko VV, Kaufmann GF, Mathison JC, Scott D a, Katz AZ, et al. (2006) N-(3-oxo-acyl)homoserine lactones signal cell activation through a mechanism distinct from the canonical pathogen-associated molecular pattern recognition receptor pathways. J Biol Chem 281: 28822-28830.
44. Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI (1997) Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386: 855-858.
45. Schwarzer C, Wong S, Shi J, Matthes E, Illek B, et al. (2010) Pseudomonas aeruginosa homoserine lactone activates store-operated cAMP and CFTRdependent Cl secretion by human airway epithelia. J Biol Chem 285: 34850-34863.
46. Vikström E, Bui L, Konradsson P, Magnusson K-E (2010) Role of calcium signalling and phosphorylations in disruption of the epithelial junctions by Pseudomonas aeruginosa quorum sensing molecule. Eur J Cell Biol 89: 584-597.
47. Martino MEB, Olsen JC, Fulcher NB, Wolfgang MC, O'Neal WK, et al. (2009) Airway epithelial inflammation-induced endoplasmic reticulum Ca2+ store expansion is mediated by X-box binding protein-1. J Biol Chem 284: 14904-14913.
48. Ribeiro CMP, Paradiso AM, Schwab U, Perez-Vilar J, Jones L, et al. (2005) Chronic airway infection/inflammation induces a Ca2+i-dependent hyperinflammatory response in human cystic fibrosis airway epithelia. J Biol Chem 280: 17798-17806.
49. Wu H, Song Z, Hentzer M, Andersen JB, Molin S, et al. (2004) Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 53: 1054-1061.
50. Amara N, Mashiach R, Amar D, Krief P, Spieser SAH, et al. (2009) Covalent inhibition of bacterial quorum sensing. J Am Chem Soc 131: 10610-10619.
51. Flotte TR, Afione SA, Solow R, Drumm ML, Markakis D, et al. (1993) Expression of the cystic fibrosis transmembrane conductance regulator from a novel adeno-associated virus promoter. J Biol Chem 268: 3781-3790.
52. Zabner J, Karp P, Seiler M, Phillips SL, Mitchell CJ, et al. (2003) Development of cystic fibrosis and noncystic fibrosis airway cell lines. Am J Physiol Lung Cell Mol Physiol 284: L844-L854.
53. Gee KR, Brown K a, Chen WN, Bishop-Stewart J, Gray D, et al. (2000) Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes. Cell Calcium 27: 97-106.
54. Lynn DJ, Winsor GL, Chan C, Richard N, Laird MR, et al. (2008) InnateDB: facilitating systems-level analyses of the mammalian innate immune response. Mol Syst Biol 4: 218.
55. Lynn DJ, Chan C, Naseer M, Yau M, Lo R, et al. (2010) Curating the innate immunity interactome. BMC Syst Biol 4: 117.
56. Mookherjee N, Hamill P, Gardy J, Blimkie D, Falsafi R, et al. (2009) Systems biology evaluation of immune responses induced by human host defence peptide LL-37 in mononuclear cells. Mol Biosyst 5: 483-496.
57. Lee SMY, Gardy JL, Cheung CY, Cheung TKW, Hui KPY, et al. (2009) Systems-level comparison of host-responses elicited by avian H5N1 and seasonal H1N1 influenza viruses in primary human macrophages. PLoS One 4: e8072.
58. Barsky A, Gardy JL, Hancock RE, Munzner T (2007) Cerebral: a Cytoscape plugin for layout of and interaction with biological networks using subcellular localization annotation. Bioinformatics 23: 1040-1042.