Physiological levels of lipoxin A4 inhibit ENaC and restore airway surface liquid height in cystic fibrosis bronchial epithelium

Physiological Reports

Volumn 2, Issue 8, 2014, Pages

  Al Alawi, Mazen ^a   Buchanan, Paul ^b   Verriere, Valia ^a   Higgins, Gerard ^b   McCabe, Olive ^a   Costello, Richard W ^a   McNally, Paul ^b   Urbach, Valérie ^a,b,c   Harvey, Brian J ^a  

^a BEAUMONT HOSPITAL   (Ireland)

^b CHI Crumlin   (Ireland)

^c INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

Author keywords

Cystic fibrosis; ENaC; Lipoxin A4

Indexed keywords

AMILORIDE; BUMETANIDE; EPITHELIAL SODIUM CHANNEL; FORMYLPEPTIDE RECEPTOR; FORMYLPEPTIDE RECEPTOR LIKE 1; LIPOXIN A;

AIRWAY; AIRWAY SURFACE LIQUID HEIGHT; ARTICLE; BRONCHUS MUCOSA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; DOSE RESPONSE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; ION TRANSPORT; PROTEIN EXPRESSION; RECEPTOR BLOCKING; SODIUM ABSORPTION; SODIUM CURRENT; SODIUM TRANSPORT;

EID: 85002707707     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12093     Document Type: Article

References (36)

1. Blouquit-Laye, S., and T. Chinet. 2007. Ion and liquid transport across the bronchiolar epithelium. Respir. Physiol. Neurobiol. 159: 278-282.
2. Bonnans, C., B. Mainprice, P. Chanez, J. Bousquet, and V. Urbach. 2003. Lipoxin A4 stimulates a cytosolic Ca2+ increase in human bronchial epithelium. J. Biol. Chem. 278: 10879-10884.
3. Bonnans, C., K. Fukunaga, M. A. Levy, and B. D. Levy. 2006. Lipoxin A(4) regulates bronchial epithelial cell responses to acid injury. Am. J. Pathol. 168: 1064-1072.
4. Boucher, R. C. 2004a. New concepts of the pathogenesis of cystic fibrosis lung disease. Eur. Respir. J. 23: 146-158.
5. Boucher, R. C. 2004b. Relationship of airway epithelial ion transport to chronic bronchitis. Proc. Am. Thorac. Soc. 1: 66-70.
6. Buchanan, P. J., P. McNally, B. J. Harvey, and V. Urbach. 2013. Lipoxin A(4)-mediated KATP potassium channel activation results in cystic fibrosis airway epithelial repair. Am. J. Physiol. Lung Cell. Mol. Physiol. 305: L193-L201.
7. Chen, J. H., D. A. Stoltz, P. H. Karp, S. E. Ernst, A. A. Pezzulo, T. O. Moninger, et al. 2010. Loss of anion transport without increased sodium absorption characterizes newborn porcine cystic fibrosis airway epithelia. Cell 143: 911-923.
8. Clish, C. B., B. D. Levy, N. Chiang, H. H. Tai, and C. N. Serhan. 2000. Oxidoreductases in lipoxin A4 metabolic inactivation: a novel role for 15-onoprostaglandin 13-reductase/leukotriene B4 12-hydroxydehydrogenase in inflammation. J. Biol. Chem. 275: 25372-25380.
9. Donabedian, H., and J. I. Gallin. 1981. Deactivation of human neutrophil chemotaxis by chemoattractants: effect on receptors for the chemotactic factor f-Met-Leu-Phe. J. Immunol. 127: 839-844.
10. Gavins, F. N., S. Yona, A. M. Kamal, R. J. Flower, and M. Perretti. 2003. Leukocyte antiadhesive actions of annexin 1: ALXR- and FPR-related anti-inflammatory mechanisms. Blood 101: 4140-4147.
11. Grumbach, Y., N. V. Quynh, R. Chiron, and V. Urbach. 2009. LXA4 stimulates ZO-1 expression and transepithelial electrical resistance in human airway epithelial (16HBE14o-) cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 296: L101-L108.
12. Hummler, E., P. Barker, J. Gatzy, F. Beermann, C. Verdumo, A. Schmidt, et al. 1996. Early death due to defective neonatal lung liquid clearance in alpha-ENaC-deficient mice. Nat Genet. 12: 325-328.
13. Jensen, B. S., D. Strøbaek, S. P. Olesen, and P. Christophersen. 2001. The Ca2+-activated K+ channel of intermediate conductance: a molecular target for novel treatments? Curr. Drug Targets 2: 401-422.
14. Jesaitis, A. J., J. R. Naemura, L. A. Sklar, C. G. Cochrane, and R. G. Painter. 1984. Rapid modulation of N-formyl chemotactic peptide receptors on the surface of human granulocytes: formation of high-affinity ligand-receptor complexes in transient association with cytoskeleton. J. Cell Biol. 98: 1378-1387.
15. Jesaitis, A. J., J. O. Tolley, R. G. Painter, L. A. Sklar, and C. G. Cochrane. 1985. Membrane-cytoskeleton interactions and the regulation of chemotactic peptide-induced activation of human granulocytes: the effects of dihydrocytochalasin B. J. Cell. Biochem. 27: 241-253.
16. Karp, C. L., L. M. Flick, K. W. Park, S. Softic, T. M. Greer, R. Keledjian, et al. 2004. Defective lipoxin-mediated anti-inflammatory activity in the cystic fibrosis airway. Nat. Immunol. 5: 388-392.
17. Kerem, E., T. Bistritzer, A. Hanukoglu, T. Hofmann, Z. Zhou, W. Bennett, et al. 1999. Pulmonary epithelial sodium-channel dysfunction and excess airway liquid in pseudohypoaldosteronism. N Engl J Med. 341: 156-162.
18. Kunzelmann, K. 2003. ENaC is inhibited by an increase in the intracellular Cl(-) concentration mediated through activation of Cl(-) channels. Pflugers Arch. 445: 504-512.
19. Kunzelmann, K., G. L. Kiser, R. Schreiber, and J. R. Riordan. 1997. Inhibition of epithelial Na+ currents by intracellular domains of the cystic fibrosis transmembrane conductance regulator. FEBS Lett. 400: 341-344.
20. Maderna, P., D. C. Cottell, G. Berlasconi, N. A. Petasis, H. R. Brady, and C. Godson. 2002. Lipoxins induce actin reorganization in monocytes and macrophages but not in neutrophils: differential involvement of rho GTPases. Am. J. Pathol. 160: 2275-2283.
21. Matsui, H., B. R. Grubb, R. Tarran, S. H. Randell, J. T. Gatzy, C. W. Davis, et al. 1998. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95: 1005-1015.
22. Matsui, H., C. W. Davis, R. Tarran, and R. C. Boucher. 2000. Osmotic water permeabilities of cultured, well-differentiated normal and cystic fibrosis airway epithelia. J. Clin. Invest. 105: 1419-1427.
23. Pisi, G., and A. Chetta. 2009. Airway clearance therapy in cystic fibrosis patients. Acta Biomed. 80: 102-106.
24. Prossnitz, E. R., O. Quehenberger, C. G. Cochrane, and R. D. Ye. 1993. Signal transducing properties of the N-formyl peptide receptor expressed in undifferentiated HL60 cells. J. Immunol. 151: 5704-5715.
25. Riordan, J. R., J. M. Rommens, B. Kerem, N. Alon, R. Rozmahel, Z. Grzelczak, et al. 1989. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245: 1066-1073.
26. Serhan, C. N. 1997. Lipoxins and novel aspirin-triggered 15-epi-lipoxins (ATL): a jungle of cell-cell interactions or a therapeutic opportunity? Prostaglandins 53: 107-137.
27. Serhan, C. N., and M. Romano. 1995. Lipoxin biosynthesis and actions: role of the human platelet LX-synthase. J. Lipid Mediat. Cell Signal. 12: 293-306.
28. Serhan, C. N., and J. Savill. 2005. Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6: 1191-1197.
29. Serhan, C. N., M. Hamberg, and B. Samuelsson. 1984. Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. Proc. Natl Acad. Sci. USA 81: 5335-5339.
30. Starosta, V., F. Ratjen, E. Rietschel, K. Paul, and M. Griese. 2006. Anti-inflammatory cytokines in cystic fibrosis lung disease. Eur. Respir. J. 28: 581-587.
31. Stutts, M. J., C. M. Canessa, J. C. Olsen, M. Hamrick, J. A. Cohn, B. C. Rossier, et al. 1995. CFTR as a cAMP-dependent regulator of sodium channels. Science 269: 847-850.
32. Tarran, R., and R. C. Boucher. 2002. Thin-film measurements of airway surface liquid volume/composition and mucus transport rates in vitro. Methods Mol. Med. 70: 479-492.
33. Tarran, R., B. R. Grubb, D. Parsons, M. Picher, A. J. Hirsh, C. W. Davis, et al. 2001. The CF salt controversy: in vivo observations and therapeutic approaches. Mol. Cell 8: 149-158.
34. Verriere, V., G. Higgins, M. Al-Alawi, R. W. Costello, P. McNally, R. Chiron, et al. 2012. Lipoxin A4 stimulates calcium-activated chloride currents and increases airway surface liquid height in normal and cystic fibrosis airway epithelia. PLoS ONE 7: e37746.
35. Wang, Q., Q. Q. Lian, R. Li, B. Y. Ying, Q. He, F. Chen, et al. 2013. Lipoxin A4 activates alveolar epithelial sodium channel, Na, K-ATPase, and increases alveolar fluid clearance. Am. J. Respir. Cell Mol. Biol. 48: 610-618.
36. Zabner, J., P. Karp, M. Seiler, S. L. Phillips, C. J. Mitchell, M. Saavedra, et al. 2003. Development of cystic fibrosis and noncystic fibrosis airway cell lines. Am. J. Physiol. Lung Cell. Mol. Physiol. 284: L844-L854.