Lipoxin A4 prevents tight junction disruption and delays the colonization of cystic fibrosis bronchial epithelial cells by Pseudomonas aeruginosa

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 310, Issue 11, 2016, Pages L1053-L1061

  Higgins, Gerard ^a,b   Torre, Coral Fustero ^a   Tyrrell, Jean ^b   McNally, Paul ^a,c   Harvey, Brian J ^b   Urbach, Valerie ^a,b,d  

^a NATIONAL CHILDREN S RESEARCH CENTRE   (Ireland)

^b BEAUMONT HOSPITAL   (Ireland)

^c OUR LADY S CHILDREN S HOSPITAL   (Ireland)

^d INSTITUT NECKER ENFANTS MALADES   (France)

Author keywords

Cystic fibrosis; Lipoxin A4; Pseudomonas aeruginosa; Tight junction; ZO 1

Indexed keywords

GENTAMICIN; LIPOXIN A; MESSENGER RNA; PROTEIN ZO1; FORMYLPEPTIDE RECEPTOR; FPR2 PROTEIN, HUMAN; LIPOXIN; LIPOXIN RECEPTOR; NONSTEROID ANTIINFLAMMATORY AGENT; TJP1 PROTEIN, HUMAN;

AIRWAY EPITHELIAL CELL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BRONCHUS BIOPSY; BRONCHUS MUCOSA; CHILD; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMORTALIZED CELL LINE; LUNG FIBROSIS; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RNA SYNTHESIS; TIGHT JUNCTION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; CELL LINE; CYSTIC FIBROSIS; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION; GENETICS; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; PRECLINICAL STUDY; PSEUDOMONAS INFECTIONS; RESPIRATORY MUCOSA;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CELL LINE; CYSTIC FIBROSIS; DRUG EVALUATION, PRECLINICAL; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; LIPOXINS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, LIPOXIN; RESPIRATORY MUCOSA; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84984601413     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00368.2015     Document Type: Article

References (46)

1. Al-Alawi M, Buchanan P, Verriere V, Higgins G, McCabe O, Costello RW, McNally P, Urbach V, Harvey BJ. Physiological levels of lipoxin A4 inhibit ENaC and restore airway surface liquid height in cystic fibrosis bronchial epithelium. Physiol Rep 2: e12093, 2014.
2. Anderson JM, Van Itallie CM. Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 1: a002584, 2009.
3. Angus AA, Lee AA, Augustin DK, Lee EJ, Evans DJ, Fleiszig SM. Pseudomonas aeruginosa induces membrane blebs in epithelial cells, which are utilized as a niche for intracellular replication and motility. Infect Immun 76: 1992-2001, 2008.
4. Bajmoczi M, Gadjeva M, Alper SL, Pier GB, Golan DE. Cystic fibrosis transmembrane conductance regulator and caveolin-1 regulate epithelial cell internalization of Pseudomonas aeruginosa. Am J Physiol Cell Physiol 297: C263-C277, 2009.
5. Bonnans C, Fukunaga K, Levy MA, Levy BD. Lipoxin A4 regulates bronchial epithelial cell responses to acid injury. Am J Pathol 168: 1064-1072, 2006.
6. Buchanan PJ, McNally P, Harvey BJ, Urbach V. Lipoxin A4-mediated KATP potassium channel activation results in cystic fibrosis airway epithelial repair. Am J Physiol Lung Cell Mol Physiol 305: L193-L201, 2013.
7. Campodonico VL, Gadjeva M, Paradis-Bleau C, Uluer A, Pier GB. Airway epithelial control of Pseudomonas aeruginosa infection in cystic fibrosis. Trends Mol Med 14: 120-133, 2008.
8. Cattaneo F, Parisi M, Ammendola R. Distinct signaling cascades elicited by different formyl peptide receptor 2 (FPR2) agonists. Int J Mol Sci 14: 7193-7230, 2013.
9. Chi E, Mehl T, Nunn D, Lory S. Interaction of Pseudomonas aeruginosa with A549 pneumocyte cells. Infect Immun 59: 822-828, 1991.
10. Chroneos ZC, Wert SE, Livingston JL, Hassett DJ, Whitsett JA. Role of cystic fibrosis transmembrane conductance regulator in pulmonary clearance of Pseudomonas aeruginosa in vivo. J Immunol 165: 3941-3950, 2000.
11. Citi S. Protein kinase inhibitors prevent junction dissociation induced by low extracellular calcium in MDCK epithelial cells. J Cell Biol 117: 169-178, 1992.
12. de Bentzmann S, Plotkowski C, Puchelle E. Receptors in the Pseudomonas aeruginosa adherence to injured and repairing airway epithelium. Am J Respir Crit Care Med 154: S155-S162, 1996.
13. de Bentzmann S, Roger P, Puchelle E. Pseudomonas aeruginosa adherence to remodelling respiratory epithelium. Eur Respir J 9: 2145-2150, 1996.
14. De Y, Chen Q, Schmidt AP, Anderson GM, Wang JM, Wooters J, Oppenheim JJ, Chertov O. LL-37, the neutrophil granule-and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J Exp Med 192: 1069-1074, 2000.
15. Denker BM, Nigam SK. Molecular structure and assembly of the tight junction. Am J Physiol Renal Physiol 274: F1-F9, 1998.
16. Evans DJ, Frank DW, Finck-Barbancon V, Wu C, Fleiszig SM. Pseudomonas aeruginosa invasion and cytotoxicity are independent events, both of which involve protein tyrosine kinase activity. Infect Immun 66: 1453-1459, 1998.
17. Fanning AS, Anderson JM. Zonula occludens-1 and-2 are cytosolic scaffolds that regulate the assembly of cellular junctions. Ann NY Acad Sci 2009.
18. Fleiszig SM, Zaidi TS, Fletcher EL, Preston MJ, Pier GB. Pseudomonas aeruginosa invades corneal epithelial cells during experimental infection. Infect Immun 62: 3485-3493, 1994.
19. Fleiszig SM, Zaidi TS, Pier GB. Pseudomonas aeruginosa invasion of and multiplication within corneal epithelial cells in vitro. Infect Immun 63: 4072-4077, 1995.
20. Garcia-Medina R, Dunne WM, Singh PK, Brody SL. Pseudomonas aeruginosa acquires biofilm-like properties within airway epithelial cells. Infect Immun 73: 8298-8305, 2005.
21. 4 stimulates ZO-1 expression and transepithelial electrical resistance in human airway epithelial (16HBE14o−) cells. Am J Physiol Lung Cell Mol Physiol 296: L101-L108, 2009.
22. He HQ, Troksa EL, Caltabiano G, Pardo L, Ye RD. Structural determinants for the interaction of formyl peptide receptor 2 with peptide ligands. J Biol Chem 289: 2295-2306, 2014.
23. Higgins G, Buchanan P, Perriere M, Al-Alawi M, Costello R, Verriere V, McNally P, Harvey BJ, Urbach V. Activation of P2RY11 and ATP release by LXA4 restores the airway surface liquid layer and epithelial repair in cystic fibrosis. Am J Respir Cell Mol Biol 51: 178-190, 2014.
24. Higgins G, Ringholz F, Buchanan P, McNally P, Urbach V. Physiological impact of abnormal lipoxin A4 production on cystic fibrosis airway epithelium and therapeutic potential. Biomed Res Int 2015: 781087, 2015.
25. Hoiby N, Ciofu O, Bjarnsholt T. Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol 5: 1663-1674, 2010.
26. Hussain R, Shahror R, Karpati F, Roomans GM. Glucocorticoids can affect Pseudomonas aeruginosa (ATCC 27853) internalization and intracellular calcium concentration in cystic fibrosis bronchial epithelial cells. Exp Lung Res 41: 383-392, 2015.
27. Karp CL, Flick LM, Park KW, Softic S, Greer TM, Keledjian R, Yang R, Uddin J, Guggino WB, Atabani SF, Belkaid Y, Xu Y, Whitsett JA, Accurso FJ, Wills-Karp M, Petasis NA. Defective lipoxinmediated anti-inflammatory activity in the cystic fibrosis airway. Nat Immunol 5: 388-392, 2004.
28. Li T, Cowley EA. Reduced expression of psoriasin in human airway cystic fibrosis epithelia. Respir Physiol Neurobiol 183: 177-185, 2012.
29. Lovewell RR, Patankar YR, Berwin B. Mechanisms of phagocytosis and host clearance of Pseudomonas aeruginosa. Am J Physiol Lung Cell Mol Physiol 306: L591-L603, 2014.
30. Mattoscio D, Evangelista V, De Cristofaro R, Recchiuti A, Pandolfi A, Di Silvestre S, Manarini S, Martelli N, Rocca B, Petrucci G, Angelini DF, Battistini L, Robuffo I, Pensabene T, Pieroni L, Furnari ML, Pardo F, Quattrucci S, Lancellotti S, Davi G, Romano M. Cystic fibrosis transmembrane conductance regulator (CFTR) expression in human platelets: impact on mediators and mechanisms of the inflammatory response. FASEB J 24: 3970-3980, 2010.
31. Millsap SD, Blankenship AL, Bradley PW, Jones PD, Kay D, Neigh A, Park C, Strause KD, Zwiernik MJ, Giesy JP. Comparison of risk assessment methodologies for exposure of mink to PCBs on the Kalamazoo River, Michigan. Environ Sci Technol 38: 6451-6459, 2004.
32. Molina SA, Stauffer B, Moriarty HK, Kim AH, McCarty NA, Koval M. Junctional abnormalities in human airway epithelial cells expressing F508del CFTR. Am J Physiol Lung Cell Mol Physiol 309: L475-L487, 2015.
33. Moreau-Marquis S, Stanton BA, O’Toole GA. Pseudomonas aeruginosa biofilm formation in the cystic fibrosis airway. Pulm Pharmacol Ther 21: 595-599, 2008.
34. Pier GB, Grout M, Zaidi TS, Olsen JC, Johnson LG, Yankaskas JR, Goldberg JB. Role of mutant CFTR in hypersusceptibility of cystic fibrosis patients to lung infections. Science 271: 64-67, 1996.
35. Plotkowski MC, de Bentzmann S, Pereira SH, Zahm JM, Bajolet-Laudinat O, Roger P, Puchelle E. Pseudomonas aeruginosa internalization by human epithelial respiratory cells depends on cell differentiation, polarity, and junctional complex integrity. Am J Respir Cell Mol Biol 20: 880-890, 1999.
36. Ringholz FC, Buchanan PJ, Clarke DT, Millar RG, McDermott M, Linnane B, Harvey BJ, McNally P, Urbach V. Reduced 15-lipoxygenase 2 and lipoxin A4/leukotriene B4 ratio in children with cystic fibrosis. Eur Respir J 2: 394-404, 2014.
37. Sajjan U, Wang Q, Zhao Y, Gruenert DC, Hershenson MB. Rhinovirus disrupts the barrier function of polarized airway epithelial cells. Am J Respir Crit Care Med 178: 1271-1281, 2008.
38. Schroeder TH, Reiniger N, Meluleni G, Grout M, Coleman FT, Pier GB. Transgenic cystic fibrosis mice exhibit reduced early clearance of Pseudomonas aeruginosa from the respiratory tract. J Immunol 166: 7410-7418, 2001.
39. Serhan CN. Pro-resolving lipid mediators are leads for resolution physiology. Nature 510: 92-101, 2014.
40. Serhan CN, Hamberg M, Samuelsson B. Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. Proc Natl Acad Sci USA 81: 5335-5339, 1984.
41. Stuart RO, Sun A, Panichas M, Hebert SC, Brenner BM, Nigam SK. Critical role for intracellular calcium in tight junction biogenesis. J Cell Physiol 159: 423-433, 1994.
42. Swanson B, Savel R, Szoka F, Sawa T, Wiener-Kronish J. Development of a high throughput Pseudomonas aeruginosa epithelial cell adhesion assay. J Microbiol Methods 52: 361-366, 2003.
43. Van Itallie CM, Fanning AS, Bridges A, Anderson JM. ZO-1 stabilizes the tight junction solute barrier through coupling to the perijunctional cytoskeleton. Mol Biol Cell 20: 3930-3940, 2009.
44. Verriere V, Higgins G, Al-Alawi M, Costello RW, McNally P, Chiron R, Harvey BJ, Urbach V. Lipoxin A4 stimulates calcium-activated chloride currents and increases airway surface liquid height in normal and cystic fibrosis airway epithelia. PLoS One 7: e37746, 2012.
45. Yeo NK, Jang YJ. Rhinovirus infection-induced alteration of tight junction and adherens junction components in human nasal epithelial cells. Laryngoscope 120: 346-352, 2010.
46. Zabner J, Karp P, Seiler M, Phillips SL, Mitchell CJ, Saavedra M, Welsh M, Klingelhutz AJ. Development of cystic fibrosis and noncystic fibrosis airway cell lines. Am J Physiol Lung Cell Mol Physiol 284: L844-L854, 2003.